UBC Theses and Dissertations

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UBC Theses and Dissertations

Metavariation and long term evolutionary patterns Blachford, Alistair M 1984

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METAVARIATION AND LONG TERM EVOLUTIONARY PATTERNS by ALISTAIR M. BLACHFORD B.Sc.(Honours) Queen's U n i v e r s i t y , K i n g s t o n , 1978 A THESIS SUBMITTED IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF MASTER OF SCIENCE i n THE FACULTY OF GRADUATE STUDIES (Department of Zoology) We a c c e p t t h i s t h e s i s as c o n f o r m i n g t o the r e q u i r e d s t a n d a r d THE UNIVERSITY OF BRITISH COLUMBIA November 1984 © A l i s t a i r M. B l a c h f o r d , 1984 In p r e s e n t i n g t h i s t h e s i s i n p a r t i a l f u l f i l m e n t o f t h e r e q u i r e m e n t s f o r an advanced degree a t t h e U n i v e r s i t y o f B r i t i s h C o l u m b i a , I agree t h a t t h e L i b r a r y s h a l l make i t f r e e l y a v a i l a b l e f o r r e f e r e n c e and s t u d y . I f u r t h e r agree t h a t p e r m i s s i o n f o r e x t e n s i v e c o p y i n g o f t h i s t h e s i s f o r s c h o l a r l y purposes may be g r a n t e d by t h e head o f my department o r by h i s o r h e r r e p r e s e n t a t i v e s . I t i s u n d e r s t o o d t h a t c o p y i n g o r p u b l i c a t i o n o f t h i s t h e s i s f o r f i n a n c i a l g a i n s h a l l n o t be a l l o w e d w i t h o u t my w r i t t e n p e r m i s s i o n . The U n i v e r s i t y o f B r i t i s h Columbia 1956 Main Mall Vancouver, Canada V6T 1Y3 Department o f DE-6 (3/81) i i ABSTRACT By d e f i n i t i o n " a d a p t a b i l i t y " i s the a b i l i t y of l i v i n g systems t o cope w i t h change. G e n e t i c a d a p t a b i l i t y r e q u i r e s the p r o d u c t i o n of g e n e t i c v a r i a t i o n . The view t h a t v a r i a t i o n p r o d u c t i o n i s u n d i r e c t e d or random, i . e . unconnected w i t h s e l e c t i o n , i m p l i e s t h a t s e l e c t i o n does not t a i l o r g e n e t i c a d a p t a b i l i t y . But many g e n e t i c elements a r e known t o modify p r o c e s s e s of v a r i a t i o n p r o d u c t i o n , and secondary s e l e c t i o n can a c t on them, so t h a t view i s not j u s t i f i e d . Over the l o n g e r term, n a t u r a l s e l e c t i o n ' f a v o r s ' p r o p e r t i e s important, i n m a i n t a i n i n g immediate f i t n e s s , as w e l l as p r o p e r t i e s i m p o r t a n t f o r p e r s i s t e n c e i n the s h o r t term. G e n e t i c a d a p t a b i l i t y i s l e s s i m p o r t a n t i n the s h o r t term, and i s i g n o r e d i n models based on s h o r t term d e f i n i t i o n s of f i t n e s s ( e.g. r e l a t i v e e f f e c t i v e r a t e of i n c r e a s e ) . I f " f i t n e s s " i s t o be "the p r o p e r t i e s f a v o r e d by n a t u r a l s e l e c t i o n " , then i t s d e f i n i t i o n s h o u l d be time s c a l e dependent. C u r r e n t l y p r e v a l e n t s h o r t term d e f i n i t i o n s of the a c t i o n of n a t u r a l s e l e c t i o n s h o u l d not be a l l o w e d t o hamper c o n s i d e r a t i o n of the r o l e of slow p r o c e s s e s i n d e t e r m i n i n g l o n g term e v o l u t i o n a r y p a t t e r n s . A r e v i e w of p a t t e r n s i n genome s i z e , and the e x i s t i n g e x p l a n a t i o n s f o r them, r e v e a l s t h a t most e x p l a n a t i o n s are based on n o t i o n s of adaptedness t o the s t a t e of the environment. An e x p l a n a t i o n of genome s i z e p a t t e r n s based on the r a t e of change of environments is proposed. It i s hypothesized that part of the genome is involved in regulating variation production, and that more DNA means slower production of additive genetic var i a t i o n . This new hypothesis is simple, general, and testable, but requires more evidence. The question is raised of whether genomes might be organized to f a c i l i t a t e the adjustment of genetic variation production by natural sele c t i o n . i v TABLE OF CONTENTS ABSTRACT i i LIST OF TABLES v i i LIST OF FIGURES v i i ACKNOWLEDGEMENTS i x INTRODUCTION 1 PART ONE Chapter One Some B a s i c Concepts 3 "Random" v e r s u s " D i r e c t e d " 3 Randomness and S c a l e 3 K i n d s of V a r i a t i o n 4 Time S c a l e s and N a t u r a l S e l e c t i o n 5 Chapter Two S e l e c t i o n of V a r i a t i o n P r o d u c t i o n P a t t e r n s i n V a r i a t i o n P r o d u c t i o n 7 M o d i f i e r s of v a r i a t i o n p r o d u c t i o n p r o c e s s e s 9 S e l e c t i o n Mechanisms 13 Secondary s e l e c t i o n 14 The L a y z e r Model 17 A time s c a l e s c o n s i d e r a t i o n 20 Di s c u s s i o n 22 Chapter Three Metavar i a t i o n 27 An o p t i m a l r a t e of v a r i a t i o n p r o d u c t i o n 27 To t r a c k or not t o t r a c k ? 30 Metavar i a t i o n 31 Time s c a l e dependence 32 V When i s m e t a v a r i a t i o n i m p o r t a n t ? 33 The r e a l w o r l d i s m u l t i d i m e n s i o n a l 40 V a r i a t i o n p r o d u c t i o n and g e n e t i c memory 42 PART TWO Chapter Four Genome S i z e P a t t e r n s 44 The P a t t e r n s and the C-value Paradox 44 The E x p l a n a t i o n s 47 D i s c u s s i o n 63 Genome S i z e and Rates of E v o l u t i o n 65 A New E x p l a n a t i o n of Genome S i z e P a t t e r n s 66 Support f o r the Genome S i z e / V a r i a t i o n P r o d u c t i o n H y p o t h e s i s 67 C o n c l u s i o n 70 Chapter F i v e T e s t i n g the Ideas 72 Where t o Look 73 S p e c u l a t i o n on M e t a v a r i a t i o n System S t r u c t u r e 73 E p i g e n e s i s and C a n a l i z a t i o n 77 On Mea s u r i n g G e n e t i c V a r i a t i o n P r o d u c t i o n 78 Suggested Experiment 79 P r e v i o u s E x p e r i m e n t s 83 M e t a v a r i a t i o n as E x p l a n a t i o n i n Two Bandwagon T o p i c s 84 DISCUSSION P o p u l a t i o n - l e v e l G e n e t i c Memory 87 ' V a r i a t i o n P r o d u c t i o n and E v o l u t i o n a r y P a t t e r n s 89 O l d Ideas 91 v i SUMMARY 92 REFERENCES 94 APPENDICES I . F i t n e s s , P e r s i s t e n c e and Time S c a l e s 104 I I . The F u n c t i o n a l H i e r a r c h y . , 108 I I I . A computer game f o r e x p l o r i n g v a r i a t i o n p r o d u c t i o n s t r a t e g i e s 119 v i i LIST OF TABLES TABLE 1. Known m o d i f i e r s of g e n e t i c v a r i a t i o n 10 TABLE 2. P a t t e r n s i n genome s i z e 48 TABLE 3. The range i n genome s i z e compared w i t h the minimum and maximum f o r the taxon 59 TABLE 4. P r o p e r t i e s r e q u i r e d f o r p e r s i s t e n c e under v a r i o u s e n v i r o n m e n t a l c o n d i t i o n s 112 LIST OF FIGURES FIGURE 1. F i t n e s s f u n c t i o n and two phenotype f r e q u e n c y d i s t r i b u t i o n s 19 FIGURE 2. V i s u a l d e s c r i p t i o n of the i n i t i a l c o n d i t i o n s of a computer s i m u l a t i o n t h a t compares d i f f e r i n g r a t e s of v a r i a t i o n p r o d u c t i o n 23 FIGURE 3. R e s u l t s of a computer s i m u l a t i o n comparing two s u b p o p u l a t i o n s d i f f e r i n g i n r a t e s of v a r i a t i o n p r o d u c t i o n , undergoing d i r e c t i o n a l s e l e c t i o n 24 FIGURE 4. The r e l a t i o n s h i p of a l p h a and beta genes, and the l e v e l s of i n d i r e c t i o n i n secondary s e l e c t i o n 38 v i i i FIGURE 5. I l l u s t r a t i o n of the amount of v a r i a t i o n i n genome s i z e among s p e c i e s 45 FIGURE 6. A h i e r a r c h i c a l c o n t r o l system of b i o l o g i c a l p e r s i s t e n c e - o r i e n t e d s t r a t e g i e s 1 15 FIGURE 7. P i c t o r i a l d e s c r i p t i o n of some of the model's parameters 120 FIGURE 8. Example run of the s i m u l a t i o n model 125 FIGURE 9. S i m u l a t i o n model o u t p u t : p o p u l a t i o n s i z e s over time 127 FIGURE 10. S i m u l a t i o n model o u t p u t : average phenotypes over time 128 FIGURE 11. S i m u l a t i o n model o u t p u t : r e l a t i v e average f i t n e s s e s over time 129 FIGURE 12. S i m u l a t i o n model o u t p u t : average " s t e p - s i z e s " over time 130 FIGURE 13. The s i m u l a t i o n model program l i s t i n g s 131 i x ACKNOWLEDGEMENTS T h i s t h e s i s has been q u i t e an adventure f o r me. Al t h o u g h I t h i n k of myself as an e c o l o g i s t , the glimmer of some of the id e a s e x p l o r e d i n t h i s t h e s i s l u r e d me almost c o m p l e t e l y out of my " s t a n d a r d e c o l o g y " background. I would l i k e t o acknowledge the supp o r t I had w h i l e a d a p t i n g t o t h i s new " h a b i t a t " : I am most g r a t e f u l t o a l l of t h o s e who encouraged me. S t e f a n Tamm was t h a t s p e c i a l person w i t h whom I f e l t I c o u l d d i s c u s s i d e a s t h a t were so raw t h a t they were almost e m b a r r a s s i n g . He spent a l o t of time r e v i e w i n g my e a r l i e s t d r a f t s . Marco Ro d r i g u e z i s an e n t h u s i a s t i c j u g g l e r of i d e a s , and our many c h a t s were v e r y h e l p f u l . S c o t t C a r l e y h e l p e d g i v e me a wider p e r s p e c t i v e on some of my i d e a s , and t h a t was both i n t r i g u i n g and en c o u r a g i n g . I owe perhaps my g r e a t e s t thanks t o Don Ludwig. He p r o v i d e d me w i t h v a l u a b l e c o a c h i n g , and f i n a n c i a l a s s i s t a n c e (NSERC g r a n t #9239). C a r l W a l t e r s ' thorough e f f o r t s i n r e v i e w i n g my d r a f t s improved t h i s t h e s i s . Con Wehrhahn made h i m s e l f v e r y a p p r o a c h a b l e , and I thank him f o r encouragement, our d i s c u s s i o n s , and h i s prompt X r e a d i n g of my d r a f t s . Judy Myers' honest c r i t i c i s m s were not always i m m e d i a t e l y welcome, but they were v a l u a b l e . I thank my f a m i l y , f o r moral and m a t e r i a l s u p p o r t , and my f e l l o w roomies a t 4460 W. 11th. Thanks t o a l l of my f r i e n d s , e s p e c i a l l y J oyce Andrew, who a l s o h e l p e d c o n s t r u c t the f i g u r e s and t a b l e s , Jay H e s tbeck, who c o n v i n c e d me t h a t I was ready t o f i n i s h , and Glenn S u t h e r l a n d , who encouraged me down the f i n a l s t r e t c h . I t was d e c i d e d t o f i x the p r o p o r t i o n of v a r i a n t o f f s p r i n g a r b i t r a r i l y ( a t two t h i r d s ) and v a r y o n l y the o f f s p r i n g d i s t r i b u t i o n s . The l a t t e r a r e s y m m e t r i c a l ( u n d i r e c t e d ) , b i m o d a l , and v a r y o n l y i n the d e v i a t i o n of the v a r i a n t o f f s p r i n g from the p a r e n t a l phenotype. The p a r t i c u l a r d e v i a t i o n c h a r a c t e r i s t i c of a g i v e n p l a y e r w i l l be r e f e r r e d t o as i t s " s t e p - s i z e " . F i g u r e S shows a segment of a p o p u l a t i o n b e f o r e ( a ) , and a f t e r (b) 1 INTRODUCTION The Neo-Darwinian t r a d i t i o n r e g a r d s the g e n e r a t i o n of new genotypes as a random p r o c e s s , u n d i r e c t e d w i t h r e s p e c t t o the a d a p t i v e needs of the s p e c i e s . Dobzhansky (1970) s t a t e s " M u t a t i o n s . . . a r i s e r e g a r d l e s s of t h e i r a c t u a l or p o t e n t i a l u s e f u l n e s s . I t may seem a d e p l o r a b l e i m p e r f e c t i o n of n a t u r e t h a t m u t a b i l i t y i s not r e s t r i c t e d t o changes t h a t enhance the adaptedness of t h e i r c a r r i e r s . However, o n l y a v i t a l i s t P a n g l o s s c o u l d imagine t h a t the genes know how and when i t i s good f o r them t o mutate". The i n t e n t of t h i s t h e s i s i s t o examine the p o s s i b i l i t y t h a t p a r t of an organism's genome i s i n v o l v e d i n a d a p t i v e l y r e g u l a t i n g the p r o d u c t i o n of g e n e t i c v a r i a t i o n t h a t g e n e t i c c o n t r o l can r e g u l a t e g e n e t i c v a r i a t i o n p r o d u c t i o n a c c o r d i n g t o i t s p o t e n t i a l u s e f u l n e s s . T h i s t h e s i s developed from a s e a r c h f o r a framework i n which t o c a s t e v o l u t i o n a r y hypotheses i n terms of p a t t e r n s of change i n , r a t h e r than the s t a t e o f , an environment. E v o l u t i o n can be viewed as a c o n t i n u a l p r o c e s s of c r e a t i o n of new genotypes and a l t e r a t i o n of genotype f r e q u e n c i e s , or of v a r i a n t p r o d u c t i o n and v a r i a n t l o s s . I t i s o b v i o u s t h a t p a t t e r n s of e v o l u t i o n a r y change c o u l d be det e r m i n e d by both p a t t e r n s i n v a r i a n t p r o d u c t i o n and p a t t e r n s i n v a r i a n t l o s s . But the burden of e x p l a n a t i o n has always been p l a c e d on the p r o c e s s e s of v a r i a n t l o s s , e.g. n a t u r a l s e l e c t i o n and chance. Why? A l t h o u g h we need t o und e r s t a n d s e l e c t i o n t o judge which, i f any, of a s e t of new v a r i a n t s are r e l a t i v e l y b e t t e r , we need t o know about v a r i a n t p r o d u c t i o n t o say what ty p e s might appear. So u n l e s s we can say t h a t a l l c o n c e i v a b l e v a r i a n t s a r e always p r e s e n t , 2 v a r i a t i o n p r o d u c t i o n , not s e l e c t i o n , i s l i m i t i n g . I t seems l o g i c a l , t h e r e f o r e , t o have a good look at the p o t e n t i a l i n f l u e n c e on e v o l u t i o n of p a t t e r n s i n v a r i a t i o n p r o d u c t i o n --even i f we end up r u l i n g them u n i m p o r t a n t . I w i l l d e s c r i b e how a change i n emphasis from v a r i a t i o n l o s s to v a r i a t i o n p r o d u c t i o n amounts t o i n c r e a s e d a t t e n t i o n t o a d a p t a b i l i t y and change, r a t h e r than adaptedness and s t a t e of the environment. T h i s t h e s i s i s w r i t t e n i n two p a r t s . In the f i r s t p a r t I e s t a b l i s h the p l a u s i b i l i t y of p a t t e r n e d v a r i a t i o n p r o d u c t i o n , and d e s c r i b e a g e n e r a l mechanism by which n a t u r a l s e l e c t i o n can a d j u s t v a r i a t i o n p r o d u c t i o n p a t t e r n s . I then expand on the r e q u i r e m e n t s and c o n s t r a i n t s of a r e g u l a t i o n system f o r v a r i a t i o n p r o d u c t i o n . The m e r i t of a d i f f e r e n t i d e a or p e r s p e c t i v e i n s c i e n c e i s d e t e r m i n e d by i t s s u c c e s s i n e x p l a i n i n g e x i s t i n g o b s e r v a t i o n s , and i n g e n e r a t i n g new q u e s t i o n s . P a r t Two i s devoted t o e x e r c i s i n g the i d e a s of P a r t One i n t h i s way. I c o n s i d e r p a t t e r n s i n genome s i z e as an example of an a r e a where t r a d i t i o n a l e x p l a n a t i o n s have not proved f r u i t f u l , and where a h y p o t h e s i s based on v a r i a t i o n p r o d u c t i o n might be more s u c c e s s f u l . A f t e r d i s c u s s i n g ways i n which the h y p o t h e s i z e d r e g u l a t i o n system might be d e t e c t e d , I c o n c l u d e by u s i n g the i d e a s t o g e n e r a t e new q u e s t i o n s f o r two "bandwagon" t o p i c s . 3 CHAPTER ONE  SOME BASIC CONCEPTS In t h i s c h a p t e r I w i l l d e f i n e a few terms, and i n t r o d u c e some of the c o n c e p t s t h a t u n d e r l y the arguments t o be de v e l o p e d l a t e r . "Random" v s . " D i r e c t e d " How does one d i s t i n g u i s h "random" or " u n d i r e c t e d " p a t t e r n s i n v a r i a t i o n p r o d u c t i o n from those which a r e " a d a p t i v e " or " d i r e c t e d " ? Random v a r i a t i o n i s u n c o r r e l a t e d w i t h , i . e . not " d i r e c t e d " by, the s e l e c t i o n p r o c e s s e s t o which i t w i l l be s u b j e c t e d . I t i s by reason of the g e n e r a l l y assumed l a c k of c o n n e c t i o n t h a t " E v o l u t i o n i s (I r e p e a t ! ) a two s t e p p r o c e s s " (Mayr 1978) of v a r i a t i o n p r o d u c t i o n and v a r i a t i o n l o s s . Randomness and S c a l e I w i l l n o t , i n t h i s t h e s i s , be s u g g e s t i n g a l e v e l of c o n t r o l t h a t can program m u t a t i o n at a g i v e n l o c u s t o a p a r t i c u l a r end r e s u l t . I w i l l assume v a r i a t i o n p r o d u c t i o n a t t h i s l e v e l t o be u n c o n t r o l l e d , and " u n d i r e c t e d " by any i n f l u e n c e of s e l e c t i o n . I w i l l argue f o r c o n s i d e r a t i o n of p o s s i b l e c o n t r o l of m u t a t i o n r a t e s a c r o s s l o c i , and hence, a c r o s s t r a i t s . G i v e n t h a t the p r o d u c t i o n of g e n e t i c v a r i a t i o n were not always s e l e c t e d a g a i n s t , the e x i s t e n c e of a h e r i t a b l e system f o r c o n t r o l l i n g m u t a t i o n r a t e s a c r o s s l o c i would make i t p o s s i b l e f o r s e l e c t i o n t o i n f l u e n c e the p a t t e r n of v a r i a t i o n p r o d u c t i o n on the l e v e l of the genotype, and i n the p o p u l a t i o n as a whole. 4 With t h i s feedback from s e l e c t i o n t o v a r i a t i o n p r o d u c t i o n , e v o l u t i o n i s no l o n g e r a s i m p l e two s t e p p r o c e s s of v a r i a t i o n p r o d u c t i o n f o l l o w e d by s e l e c t i o n , at the g e n o t y p i c or o r g a n i s m a l l e v e l , because s t e p two can i n f l u e n c e s t e p one. These p o i n t s w i l l be d i s c u s s e d i n f u r t h e r d e t a i l l a t e r . At p r e s e n t i t s u f f i c e s to note t h a t "random v a r i a t i o n p r o d u c t i o n " and " d i r e c t e d v a r i a t i o n p r o d u c t i o n " are too vague i n t h e m s e l v e s , because the randomness of a phenomenon can depend on the s c a l e on which i t i s c o n s i d e r e d . S e c o n d l y , I must emphasize t h a t m u t a t i o n i s but one of many p r o c e s s e s of g e n e t i c v a r i a t i o n p r o d u c t i o n i n a p o p u l a t i o n . Above i t was d i s c u s s e d a l o n e to s i m p l i f y e x p l a n a t i o n . K i n d s of Var i a t i o n I f we a r e t o d e a l w i t h the p o s s i b l e c o n n e c t i o n between s e l e c t i o n and v a r i a t i o n p r o d u c t i o n , then i t w i l l be c o n v e n i e n t t o d i s t i n g u i s h among t y p e s of v a r i a t i o n a c c o r d i n g t o t h e i r d i f f e r e n c e s i n i n t e r a c t i o n w i t h s e l e c t i o n . L e v i n s (1964a) d e s c r i b e s the d i f f e r e n t s e l e c t i o n regimes f a v o r i n g n o n - a d d i t i v e and a d d i t i v e v a r i a t i o n r e s p e c t i v e l y : In a p a t c h y environment i n which the p a t c h e s are s u f f i c i e n t l y d i f f e r e n t , r e l a t i v e to the t o l e r a n c e of an i n d i v i d u a l , t o make a "patch g e n e r a l i s t " s t r a t e g y i n e f f i c i e n t compared w i t h a "patch s p e c i a l i s t " s t r a t e g y , NON-ADDITIVE v a r i a t i o n i n e f f e c t p e r m i t s a s i n g l e p o p u l a t i o n t o r e t a i n genotypes i n c o n s t a n t f r e q u e n c i e s and become a mosaic of p a t c h s p e c i a l i s t s . The f u n c t i o n of ADDITIVE v a r i a t i o n , on the o t h e r hand, i s 5 t o p e r m i t change i n gene f r e q u e n c i e s , and e v o l u t i o n a r y r e s p o n s i v e n e s s . A d d i t i v e v a r i a t i o n and g e n e t i c response are f a v o r e d i f p r e s e n t s e l e c t i o n p r e s s u r e s are good p r e d i c t o r s of f u t u r e s e l e c t i o n p r e s s u r e s . I t i s the k i n d of change i n an environment, r a t h e r than the s t a t e of the environment, which d e t e r m i n e s the importance of a d a p t a b i l i t y , and a d d i t i v e v a r i a t i o n p r o d u c t i o n . In t h i s t h e s i s I w i l l be t a l k i n g about a d d i t i v e v a r i a t i o n because I am concerned w i t h g e n e t i c a d a p t a b i l i t y , i . e . e v o l u t i o n a r y r e s p o n s i v e n e s s . F u r t h e r m o r e , I w i l l be d i s c u s s i n g a d d i t i v e v a r i a t i o n p r o d u c t i o n as a p r o c e s s and s t r a t e g y , r a t h e r than as a measure of the amount of a d d i t i v e v a r i a t i o n i n a p o p u l a t i o n . Time S c a l e s and N a t u r a l S e l e c t i o n N a t u r a l s e l e c t i o n i s not an a g e n t , but a p r o c e s s , and i t s components a r e t h e r e f o r e s u b - p r o c e s s e s ( G h i s e l i n 1981). The r e s u l t s of s e l e c t i o n are the combined r e s u l t s of i t s many sub-p r o c e s s e s , such as c o m p e t i t i o n and p r e d a t i o n . U n f o r t u n a t e l y the f o r m u l a t i o n of N e o - D a r w i n i s t models, w i t h s e l e c t i o n c o e f f i c i e n t s summarizing the r e s u l t s of a l l d e t e r m i n i s t i c p r o c e s s e s a f f e c t i n g d i f f e r e n t i a l r e p r o d u c t i o n , tends t o c o n j u r e up the i l l u s i o n of a s e l e c t i o n " f o r c e " (agent) a c t i n g on " u n i t s " ( p a t i e n t s , i n the t e r m i n o l o g y G h i s e l i n 1981 u s e s ) . The " r e s u l t s of s e l e c t i o n " w i l l depend on what sub-p r o c e s s e s a r e i n v o l v e d . Longer time s c a l e s ( l o n g e r p e r i o d s of o b s e r v a t i o n ) a l l o w the a c t i o n s of s l o w e r p r o c e s s e s t o show themselves i n the r e s u l t s ( i . e . t o become " i m p o r t a n t " ) . T h i s 6 i m p l i e s t h a t the r e s u l t s of s e l e c t i o n can d i f f e r q u a l i t a t i v e l y depending on the time s c a l e over which we p e r c e i v e them. (See Appendices I ~atid I I f o r f u r t h e r d i s c u s s i o n of t h i s i d e a . ) 7 CHAPTER TWO  SELECTION OF VARIATION PRODUCTION I f t h e r e e x i s t s h e r i t a b l e c o n t r o l of a d a p t a b i l i t y , then s e l e c t i o n , i n the form of k i n d s of e n v i r o n m e n t a l change, can mold g e n e t i c a d a p t a b i l i t y , i . e . a d d i t i v e g e n e t i c v a r i a t i o n p r o d u c t i o n . T h i s would j u s t i f y the f o r m u l a t i o n of hypotheses i n terms of a d a p t a b i l i t y and the way environments change (Chapter F o u r ) . Hypotheses are more commonly phrased i n terms of adaptedness, and the way environments a r e . The purpose of t h i s c h a p t e r i s t o e s t a b l i s h the p l a u s i b i l i t y of d i r e c t e d v a r i a t i o n p r o d u c t i o n , an a l t e r n a t i v e e x p l a n a t i o n f o r observed p a t t e r n s of g e n e t i c v a r i a b i l i t y . Many known h e r i t a b l e f a c t o r s i n f l u e n c e the p r o d u c t i o n of g e n e t i c v a r i a t i o n , and can be p e r c e i v e d as b e i n g p a r t of a v a r i a t i o n r e g u l a t i o n system. A s e l e c t i o n mechanism which can modify such a r e g u l a t i o n system i s d e s c r i b e d by way of a n a l y z i n g a s i m p l e model from the l i t e r a t u r e . P a t t e r n s i n V a r i a t i o n P r o d u c t i o n There i s no q u e s t i o n t h a t t h e r e a r e p a t t e r n s i n the p r o d u c t i o n of g e n e t i c v a r i a t i o n -- the q u e s t i o n i s whether the p a t t e r n s a r e "random" or n o t . M u t a t i o n i s one p r o c e s s of v a r i a t i o n p r o d u c t i o n , and p a t t e r n s i n i t i n c l u d e the f o l l o w i n g : 8 . 1. D i f f e r e n t genes have d i f f e r e n t m u t a t i o n r a t e s . T h i s p a t t e r n i s e a s i l y e x p l a i n e d by the assumption t h a t m u t a t i o n r a t e i s an i n t r i n s i c p r o p e r t y of the gene. D i f f e r e n t genes have d i f f e r e n t s t r u c t u r e s , so why not d i f f e r e n t m u t a t i o n r a t e s ? Ohno (1969), f o r example, su g g e s t s t h a t l a r g e r genes p r o b a b l y have h i g h e r m u t a t i o n r a t e s s i n c e m u t a t i o n p r o c e s s e s a c t per base p a i r and not per l o c u s . 2. D e l e t e r i o u s m u t a t i o n s are more f r e q u e n t than b e n e f i c i a l ones. T h i s o b s e r v a t i o n agrees w e l l w i t h the u s u a l model of u n d i r e c t e d m u t a t i o n . An u n d i r e c t e d change i s u n l i k e l y t o improve a h i g h l y o r d e r e d and i n t e g r a t e d system. 3, M u t a t i o n s w i t h s m a l l e f f e c t s a r e much more•frequent than those w i t h l a r g e e f f e c t s ( T i m o f e e f - R e s s o v s k y 1935; K e r k i s 1938; James 1959; Mukai 1964). I t i s l e s s o b v i o u s why t h i s s h o u l d be so, but i t c o u l d be argued t h a t random m u t a t i o n s would n o r m a l l y a f f e c t o n l y one or a few codons and such changes do not u s u a l l y r e s u l t i n c r u c i a l a l t e r a t i o n s of e s s e n t i a l gene p r o d u c t s . T h i s r e f i n e m e n t of the e x p l a n a t i o n of p a t t e r n (2) s h o u l d be n o t e d : the o r g a n i z a t i o n of the genome i s c o n s t r a i n e d enough t h a t changes t o i t a r e v e r y l i k e l y t o be f o r the worse, but u n c o n s t r a i n e d enough t h a t most changes do not matter much. The e x p e r i m e n t a l work r e f e r e n c e d above measured the ' s e v e r i t y ' of a m u t a t i o n by i t s e f f e c t on v i a b i l i t y . The t o o l s of m o l e c u l a r b i o l o g y have r e v e a l e d p a t t e r n s i n 9 g e n e t i c change among n a t u r a l . p o p u l a t i o n s , between genes ( J e f f r e y s 1981), w i t h i n genes between i n t r o n s and exons, and w i t h i n exons (Holmquist et a l . 1983). But these o b s e r v a t i o n s a re i n t e r p r e t e d as b e i n g p o s t - s e l e c t i o n , cannot be a t t r i b u t e d t o p a t t e r n s i n v a r i a t i o n p r o d u c t i o n and, in d e e d , a r e u s u a l l y h y p o t h e s i z e d t o be the r e s u l t of p a t t e r n s i n s e l e c t i o n p r e s s u r e s ( e . g . l e s s c r i t i c a l p a r t s of a p r o t e i n c i s t r o n a re more f r e e t o v a r y (Holmquist et a l . 1983)). An a l t e r n a t i v e t o s e v e r a l of the e x p l a n a t i o n s advanced above i s t h a t m u t a t i o n s occur more f r e q u e n t l y i n l e s s c r i t i c a l p a r t s of the genome o r , e q u i v a l e n t l y , a re s u p p r e s s e d t o a g r e a t e r e x t e n t i n more c r i t i c a l p a r t s of the genome. T h i s h y p o t h e s i s i s uncommon, perhaps because the i m p l i e d system of m u t a t i o n c o n t r o l i s l e s s p a r s i m o n i o u s or because, a t f i r s t g l a n c e , i t seems t o be t e l e o l o g i c a l or L a m a r c k i a n . Modi f i e r s of var i a t i o n p r o d u c t i o n p r o c e s s e s K a r l i n and McGregor (1974) s t a t e t h a t " . ..the e x i s t e n c e of genes c o n t r o l l i n g s p e c i f i c r e c o m b i n a t i o n r a t e s , genes i n f l u e n c i n g m u t a t i o n r a t e s a t p a r t i c u l a r s i t e s , l o c i a f f e c t i n g d i r e c t l y or i n d i r e c t l y r a t e s of m i g r a t i o n , f a c t o r s c o n t r o l l i n g o u t c r o s s i n g r a t e s , e t c . , i s documented, i d e n t i f i e d , and s t u d i e d i n the g e n e t i c s l i t e r a t u r e . " T a b l e 1 l i s t s the many d e t e r m i n a n t s of g e n e t i c v a r i a t i o n i n a p o p u l a t i o n , a l o n g w i t h known examples of g e n e t i c m o d i f i e r s . The f a c t t h a t h e r i t a b l e m o d i f i e r s of p r o c e s s e s of v a r i a t i o n p r o d u c t i o n e x i s t i m p l i e s the p o t e n t i a l f o r a d a p t i v e m o d i f i c a t i o n 10 TABLE 1. The d e t e r m i n a n t s of g e n e t i c v a r i a t i o n i n p o p u l a t i o n s , a l o n g w i t h examples of h e r i t a b l e f a c t o r s t h a t can modify v a r i a t i o n p r o d u c t i o n . MUTATION mutator genes and t r a n s p o s o n s ( I v e s 1950; M c C l i n t o c k 1965; Green 1973; Thompson and Woodruff 1978), genes f o r r e p a i r enzymes and po l y m e r a s e s RECOMBINATION -chromosome number - f r e q u e n c y of c r o s s i n g over ( i n v e r s i o n s , recombinant genes ( C a t c h e s d i d e 1968; Stamberg 1969), B chromosomes ( C a r l s o n 1978)) MEIOTIC DRIVE s e g r e g a t i o n d i s t o r t e r l o c u s (SD) i n D r o s o p h i l a ( H i r a i z u m i e t a l . 1960), t - a l l e l e i n house mouse (Lewontin and Dunn 1960) POPULATION SIZE POPULATION STRUCTURE - d i s p e r s a l r a t e s and m i g r a t i o n "The g e n e t i c c o n t r o l of m i g r a t i o n r a t e s i s e x e m p l i f i e d by genes d e t e r m i n i n g f l a g e l l a i n p r o t o z o a , movements i n Hydra, b i r d m i g r a t i o n , e t c . B i r d and f i s h m i g r a t i o n p a t t e r n s o f t e n 11 T a b l e 1 (co n t ' d ) d i s p l a y the i n t e r e s t i n g phenomenon t h a t p o p u l a t i o n s may v a r y c a t e g o r i c a l l y i n t o m i g r a t o r s and n o n - m i g r a t o r s , and the e v i d e n c e suggests a t t i m e s t h a t m i g r a t i o n per se may be p o l y m o r p h i c w i t h i n p o p u l a t i o n s . " ( K a r l i n and McGregor 1974) BREEDING SYSTEM - f r e q u e n c i e s of ma t i n g t y p e s -mating p a t t e r n s ( a s s o r t a t i v e n e s s ) - a l l of the f a c t o r s t h a t can c o n t r i b u t e t o r e p r o d u c t i v e i s o l a t i o n (see Dobzhansky 1970, p.314), e.g. i n c o m p a t i b i l i t y f a c t o r s i n p l a n t s , genes c o n t r o l l i n g s e a s o n a l t i m i n g of r e p r o d u c t i o n , r e c o g n i t i o n ( o l f a c t i o n , v i s i o n , sound), e t c . "A number of s i m p l e M e n d e l i a n f a c t o r s a f f e c t i n g p r e f e r e n c e s i n mating a r e a s s o c i a t e d w i t h pigment c o l o r or p a t t e r n ( M a i n a r d i 1968)." ( K a r l i n and McGregor 1974) SELECTION -dominance r e l a t i o n s h i p s i n f l u e n c e the e f f e c t s of s e l e c t i o n . G e n e t i c m o d i f i c a t i o n of dominance i s o f t e n assumed (see Wrig h t 1929; Feldman and K a r l i n 1971), but I know of no i d e n t i f i e d g e n e t i c e l e m e n t s . HISTORY 1 2 of variation production by selection. How can selection act on these modifiers? Must 'group' selection be invoked? These questions w i l l be answered next. 13 SELECTION MECHANISMS Perhaps the g r e a t e s t b a r r i e r t o c o n s i d e r a t i o n of p a t t e r n e d v a r i a t i o n p r o d u c t i o n i s the l a c k of an e a s i l y u n d e r s t a n d a b l e , g e n e r a l mechanism e x p l a i n i n g how the p a t t e r n i n g of v a r i a t i o n p r o d u c t i o n can take p l a c e . The l i t e r a t u r e c o n t a i n s s e v e r a l d i f f e r e n t m a t h e m a t i c a l models c o n c e r n i n g the m o d i f i c a t i o n of p r o d u c t i o n of g e n e t i c v a r i a t i o n (e.g. F i s h e r 1930; Kimura 1956,1960,1967; L e v i n s 1967; L e i g h 1970,1973; K a r l i n and MacGregor 1974; C h a r l e s w o r t h 1976; F e l s e n s t e i n and Yokoyama 1976; G i l l e s p i e 1981). But these e q u i l i b r i u m models u s u a l l y seem more concerned about the dynamics of m o d i f i e r f r e q u e n c i e s than on the r e l e v a n c e of a p r o c e s s of m o d i f i c a t i o n of v a r i a t i o n p r o d u c t i o n t o l a r g e s c a l e or l o n g term e v o l u t i o n a r y p a t t e r n s . L a y z e r (1980) d e s c r i b e d a more g e n e r a l mechanism of v a r i a t i o n m o d i f i c a t i o n , and d w e l l e d upon the e v o l u t i o n a r y i m p l i c a t i o n s of a d j u s t a b l e v a r i a t i o n p r o d u c t i o n . There a r e two k i n d s of s e l e c t i o n t h a t can a c t on p r o c e s s e s of v a r i a t i o n p r o d u c t i o n : group s e l e c t i o n , and secondary s e l e c t i o n . The c o n d i t i o n s under which group s e l e c t i o n can take p l a c e a r e r a t h e r s t r i n g e n t ( W i l l i a m s 1966). Secondary s e l e c t i o n i s common, a l t h o u g h of u n c e r t a i n , and v a r i a b l e , i m p o r t a n c e . In the p r e s e n t s e c t i o n I w i l l e x p l a i n secondary s e l e c t i o n and how i t can a c t on v a r i a t i o n p r o d u c t i o n , and c r i t i c i z e L a y z e r ' s mechanism f o r m o d i f y i n g v a r i a t i o n p r o d u c t i o n . 1 4 Secondary s e l e c t i o n Secondary s e l e c t i o n i s the p r o c e s s of d i f f e r e n t i a l t r a n s m i s s i o n of t r a i t s t o the next g e n e r a t i o n , not because s e l e c t i o n ' a c t s ' on them, but because they a re c o r r e l a t e d w i t h t r a i t s t h a t a r e a c t e d on by n a t u r a l s e l e c t i o n . The u s u a l 'primary' s e l e c t i o n a c t s on genes v i a t h e i r c o r r e l a t i o n w i t h phenotype. H e r i t a b i l i t y i s a measure of t h i s c o r r e l a t i o n . The h i g h e r the h e r i t a b i l i t y , the more e f f e c t i v e i s a g i v e n s t r e n g t h of s e l e c t i o n on phenotypes i n cha n g i n g gene f r e q u e n c i e s . There i s a f u r t h e r l e v e l of i n d i r e c t i o n i n secondary s e l e c t i o n --genes are a c t e d upon through t h e i r c o r r e l a t i o n w i t h o t h e r genes t h a t a re a c t e d on i n the u s u a l way. N.B. T h i s second c o r r e l a t i o n i s among genes, not t r a i t s . P l e i o t r o p y (a gene a f f e c t i n g more than one t r a i t ) a s s u r e s the e x i s t e n c e of c o r r e l a t e d c h a r a c t e r s and the d r a g g i n g a l o n g of one c h a r a c t e r by s e l e c t i o n on a n o t h e r . T h i s does not i n v o l v e the c o r r e l a t i o n , or l i n k a g e d i s e q u i l i b r i u m of two genes, and i s not secondary s e l e c t i o n . In the case of v a r i a t i o n p r o d u c t i o n , . secondary s e l e c t i o n can a c t on a l l e l e s t h a t r e g u l a t e p r o c e s s e s of v a r i a t i o n p r o d u c t i o n , i f these a l l e l e s a r e c o r r e l a t e d i n t h e i r d i s t r i b u t i o n w i t h i n a p o p u l a t i o n w i t h a l l e l e s p r o d u c i n g the t r a i t s on which s e l e c t i o n a c t s . For example, l e t us c o n s i d e r the r a t e of p r o d u c t i o n of g e n e t i c and ( g i v e n non-zero h e r i t a b i l i t y ) p h e n o t y p i c v a r i a t i o n f o r some a l l - i m p o r t a n t , q u a n t i t a t i v e t r a i t ( x ) . Suppose the p o p u l a t i o n has been a t e q u i l i b r i u m i n a c o n s t a n t environment. The o b s e r v a t i o n t h a t " f a c t o r s r e s p o n s i b l e f o r i n c r e a s i n g v a r i a t i o n p r o d u c t i o n w i l l be p r e s e n t i n g r e a t e r 15 p r o p o r t i o n i n the p h e n o t y p i c v a r i a n t s of the p o p u l a t i o n " e s t a b l i s h e s the second c o r r e l a t i o n r e q u i r e d f o r the o p e r a t i o n of secondary s e l e c t i o n . To t a k e a c l o s e r l o o k a t t h i s i m p o r t a n t o b s e r v a t i o n , l e t t h e r e be two a l l e l e s (H and L ) , i n an a s e x u a l p o p u l a t i o n , whose o n l y e f f e c t s a r e t o d e t e r m i n e the v a r i a n c e i n the d i s t r i b u t i o n of o f f s p r i n g phenotypes w i t h r e s p e c t t o one t r a i t . One a l l e l e (H) produces a h i g h e r v a r i a n c e than the o t h e r . The f i t n e s s ( s u r v i v a l x f e c u n d i t y ) of a genotype depends o n l y on i t s phenotype, which i s u n a f f e c t e d by the p a r t i c u l a r a l l e l e H or L . In t i m e , because of d i f f e r e n t r a t e s of g e n e r a t i n g v a r i a n c e i n phenotype, the frequency d i s t r i b u t i o n s of the two s u b p o p u l a t i o n s c h a r a c t e r i z e d by the a l l e l e s H and L, a l o n g the r e l e v a n t phenotype dimension ( x , a q u a n t i t a t i v e t r a i t ) , t a k e on the f o l l o w i n g r e l a t i v e shapes: H L u x->-Now we can see t h a t , i n a p o p u l a t i o n composed of these two s u b p o p u l a t i o n s , the genotypes p r o d u c i n g g r e a t e r v a r i a t i o n i n t h e i r o f f s p r i n g are p r e s e n t i n a g r e a t e r p r o p o r t i o n i n the v a r i a n t s of the p o p u l a t i o n . T h i s happens o n l y because of the r e l a t i v e shapes of the f r e q u e n c y d i s t r i b u t i o n s , and r e g a r d l e s s of the r e l a t i v e f r e q u e n c i e s of H and L i n the p o p u l a t i o n . 16 W i t h t h i s p i c t u r e i n mind we may f o l l o w t h e a c t i o n of secondary s e l e c t i o n by c o n s i d e r i n g c e r t a i n p a t t e r n s of s e l e c t i o n on phenotype. I t i s c l e a r t h a t d i s r u p t i v e s e l e c t i o n , f a v o r i n g b o t h t a i l s of the phenotype d i s t r i b u t i o n , would f a v o r g r e a t e r v a r i a t i o n p r o d u c t i o n , and t h a t s t a b i l i z i n g s e l e c t i o n would f a v o r reduced v a r i a t i o n p r o d u c t i o n . But i t i s l e s s easy t o see what d i r e c t i o n a l s e l e c t i o n ( f o r one t a i l ) would do. The a l l e l e f o r g r e a t e r v a r i a t i o n p r o d u c t i o n , w h i l e p r e s e n t i n g r e a t e r p r o p o r t i o n i n the f a v o r e d t a i l , a l s o c o m p r i s e s a g r e a t e r p r o p o r t i o n of the d i s f a v o r e d t a i l . y x-> L e t ' s s t a r t w i t h symmetric d i s t r i b u t i o n s (not n e c e s s a r i l y b e l l -shaped) about the same mean phenotype (M). C o n s i d e r a monotonic l i n e a r f i t n e s s f u n c t i o n f ( x ) . A phenotype t h a t d e v i a t e s t o the r i g h t of the mean i s p r e s e n t i n the p o p u l a t i o n as f r e q u e n t l y as a phenotype e q u a l l y d e v i a n t t o the l e f t of the mean. And the phenotype t o the r i g h t has a f i t n e s s t h a t i s g r e a t e r than t ( n ) by the same amount t h a t the f i t n e s s of the l e f t phenotype i s l e s s than f(/<). The d i f f e r e n c e s c a n c e l , b o t h s y m m e t r i c a l s u b p o p u l a t i o n s have the same mean f i t n e s s £(v) and, w i t h a time h o r i z o n of o n l y 1 g e n e r a t i o n , n e i t h e r a l l e l e has a s e l e c t i v e a dvantage. So no m o d i f i c a t i o n of the r a t e of v a r i a t i o n p r o d u c t i o n w i l l o c c u r . 1 7 I f the f i t n e s s f u n c t i o n f ( x ) i s not l i n e a r , one of the H or L s u b p o p u l a t i o n s w i l l have a h i g h e r average f i t n e s s . I f f ( x ) i s concave up, then the r i g h t t a i l i n c r e a s e s the average f i t n e s s of a s u b p o p u l a t i o n more than the l e f t t a i l d e c r e a s e s i t , and a l l e l e H has an advantage. u x-> I f f ( x ) i s concave down, then members t h a t d e v i a t e t o the l e f t of the mean phenotype w i l l d e c r e a s e average f i t n e s s more than those members e q u a l l y d e v i a n t t o the r i g h t w i l l i n c r e a s e i t . U X->-The ( s y m m e t r i c a l l y d i s t r i b u t e d ) s u b p o p u l a t i o n w i t h the s m a l l e r p r o p o r t i o n of v a r i a n t s (L) w i l l be f a v o r e d , and s e l e c t i o n w i l l have d e c r e a s e d v a r i a t i o n p r o d u c t i o n . The L a y z e r Model L a y z e r ' s (1980) model makes use of the above o b s e r v a t i o n s about the e f f e c t s of c o n c a v i t y of the f i t n e s s f u n c t i o n on the average f i t n e s s of s u b p o p u l a t i o n s of d i f f e r i n g v a r i a n c e s ( F i g u r e 18 1). L a y z e r assumes t h a t the f i t n e s s f u n c t i o n i s b e l l - s h a p e d , and t h a t "...the s p r e a d of f i t n e s s e s i n the p o p u l a t i o n i s s m a l l compared w i t h the t o t a l range of f i t n e s s e s a s s o c i a t e d w i t h the t r a i t i n q u e s t i o n ; see F i g u r e 1. In the neighborhood of the i n s t a n t a n e o u s p o p u l a t i o n mean X = M one may then approximate the f i t n e s s f u n c t i o n by the f i r s t t h r e e terms i n i t s T a y l o r e x p a n s i o n : f ( x ) = f ( j i ) + f ' ( M ) ( x - M ) + 0.5f" (M ) ( X - M ) 2 In t h i s a p p r o x i m a t i o n , which i s adequate i f o i s s u f f i c i e n t l y s m a l l , the mean f i t n e s s a s s o c i a t e d w i t h the t r a i t , o b t a i n e d by a v e r a g i n g f over the normal d i s t r i b u t i o n of x, i s fav= f ( ^ ) + 0 . 5 f " ( M ) a 2 . Thus the mean f i t n e s s fav i s g r e a t e r than the f i t n e s s f.(^) a s s o c i a t e d w i t h the mean v a l u e of x when f"(ju)>0, and i s s m a l l e r than f ( y ) when f"(y)<0. In o t h e r words (see f i g . 1), f a v > f ( y ) d u r i n g the emergent phase i n the e v o l u t i o n of an a d a p t a t i o n , and f a v < f ( / i ) a t or near a f i t n e s s peak." (p. 815) I t i s o b v i o u s t h a t t h i s mechanism works because of the assumed shape of the f i t n e s s f u n c t i o n . Templeton (1981) s e v e r e l y c r i t i c i z e s the model f o r t h i s a s s u m p t i o n , p o i n t i n g out t h a t ( 1 ) , L a y z e r ' s c o n c l u s i o n s about the e v o l u t i o n of genes t h a t c o n t r o l v a r i a t i o n p r o d u c t i o n t h e r e f o r e have l i t t l e g e n e r a l i t y , and t h a t ( 2 ) , G i l l e s p i e , who has done much work on the e v o l u t i o n of m o d i f i e r genes, assumes t h a t a d a p t i v e peaks are dome-shaped, i . e . concave down everywhere ( G i l l e s p i e 1978). I f t h i s were the c a s e , L a y z e r ' s mechanism would not work except t o d e c r e a s e v a r i a t i o n , l e a v i n g h i s e v o l u t i o n a r y consequences of a d j u s t a b l e 19 x -> F i g u r e 1. " F i t n e s s f u n c t i o n f ( x ) and two frequency d i s t r i b u t i o n s P ( x ) f o r an a d a p t a t i o n s p e c i f i e d by parameter x. D u r i n g the emergence of an a d a p t a t i o n the q u a n t i t y c = f " ( x ) i s p o s i t i v e and s e l e c t i o n f a v o r s a broad f r e q u e n c y d i s t r i b u t i o n of x. Near the f i t n e s s peak c i s n e g a t i v e and s e l e c t i o n f a v o r s a narrow frequency d i s t r i b u t i o n . " ( L a y z e r 1980) 20 v a r i a t i o n unfounded. A time s c a l e s c o n s i d e r a t i o n A l e s s o b v i o u s f l a w i n L a y z e r ' s e x p l a n a t i o n i s t h a t i t i s based on a one-generat i o n d e f i n i t i o n of f i t n e s s . Yet he d i s c u s s e s i m p l i c a t i o n s of h i s model on the e v o l u t i o n a r y ( m u l t i -g e n e r a t i o n ) time s c a l e . S i n c e the q u a l i t a t i v e r e s u l t s of s e l e c t i o n d i f f e r on d i f f e r e n t time s c a l e s , as I argue i n Appendices I and I I , L a y z e r ' s c o n c l u s i o n s are unsound. I t i s c o n v e n i e n t t o e x p l a i n t h i s time s c a l e s problem i n terms of 'adaptedness' and ' a d a p t a b i l i t y ' . Adaptedness i s the s u i t a b i l i t y of a phenotype t o the p r e s e n t environment. A one-g e n e r a t i o n e v a l u a t i o n of f i t n e s s would be one way t o measure i t . A d a p t a b i l i t y i s the a b i l i t y t o respond so as to m a i n t a i n adaptedness i n the f a c e of e n v i r o n m e n t a l change. L e v i n s (1964a) d e s c r i b e d the f u n c t i o n of n o n - a d d i t i v e g e n e t i c v a r i a t i o n as b e i n g p o t e n t i a l l y i m p o r t a n t f o r adaptedness t o a g i v e n heterogeneous environment, and a d d i t i v e v a r i a t i o n as b e i n g i m p o r t a n t f o r g e n e t i c r e s p o n s i v e n e s s , or a d a p t a b i l i t y , t o a c h a n g i n g environment (see Chapter One). The Fundamental Theorem of n a t u r a l s e l e c t i o n i s a statement of the r o l e of a d d i t i v e g e n e t i c v a r i a t i o n i n d e t e r m i n i n g e v o l u t i o n a r y r e s p o n s i v e n e s s ( F i s h e r 1958; P r i c e 1972). I t says t h a t the r a t e a t which a p o p u l a t i o n (or s u b p o p u l a t i o n ) e v o l v e s v a r i e s d i r e c t l y w i t h the amount of g e n e t i c a l l y based ( a d d i t i v e ) v a r i a n c e i n phenotype. My c r i t i c i s m of L a y z e r (1980) i s t h a t , a l t h o u g h he i s d e a l i n g w i t h a d d i t i v e v a r i a t i o n (which i s r e s p o n s i v e t o s e l e c t i o n ) the f u n c t i o n of which i s a d a p t a b i l i t y , h i s mechanism 21 and e x p l a n a t i o n of what s o r t of v a r i a t i o n i s advantageous under v a r i o u s c i r c u m s t a n c e s i s based e n t i r e l y on adaptedness. H i s one-g e n e r a t i o n e v a l u a t i o n of f i t n e s s l e a v e s no room f o r e v o l u t i o n a r y r e s p o n s i v e n e s s , which i s the f u n c t i o n of the a d d i t i v e v a r i a t i o n w i t h which he i s d e a l i n g . Given the r e l a t i o n s h i p ( L a y z e r 1980) fav= f U ) + 0 . 5 f " U ) a 2 i t i s o n l y c l e a r , g i v e n a c e r t a i n c o n c a v i t y ( f " ( x ) ) , which v a r i a n c e has the advantage i f the two s u b p o p u l a t i o n s have the same mean. I t c o u l d be, f o r example, t h a t a d i f f e r e n t s u b p o p u l a t i o n mean v more than compensates f o r any l o s s i n average f i t n e s s due t o the term 0 . 5f " (ju) o 2 . The subpopulat ion w i t h the g r e a t e r v a r i a n c e e v o l v e s f a s t e r and i s l i k e l y t o be ne a r e r an a d a p t i v e peak and t h e r e f o r e have a h i g h e r average f i t n e s s . The above e q u a t i o n g i v e s the i n i t i a l r e l a t i v e advantages of s u b p o p u l a t i o n s w i t h the same mean but d i f f e r e n t v a r i a n c e s . U n l e s s the i n i t i a l r e l a t i v e advantage h o l d s t h e r e a f t e r , i t would be wrong t o use t h i s i n i t i a l assessment t o e v a l u a t e the m e r i t s of d i f f e r e n t v a r i a n c e s over l o n g e r p e r i o d s . Over the l o n g e r term the s u b p o p u l a t i o n means u become f u n c t i o n s of time n ( t ) , and An/At i s an i n c r e a s i n g f u n c t i o n of the g e n e t i c a l l y based v a r i a n c e i n phenotype (the d i r e c t i o n b e i n g toward the n e a r e s t p e a k ) . Thus comparison of d i f f e r e n t v a r i a n c e s ( m a i n t a i n e d by d i f f e r e n c e s i n v a r i a n c e p r o d u c t i o n ) over the l o n g term i s more c o m p l i c a t e d . I t i s noteworthy t h a t over the l o n g term s e l e c t i o n can f a v o r i n c r e a s e d v a r i a n c e even under c u r v e s t h a t a re concave downward. 2 2 T h i s l a s t p o i n t can be i l l u s t r a t e d by computer s i m u l a t i o n ( d e t a i l s of the model a r e d e s c r i b e d i n Appendix I I I ) . Two s u b p o p u l a t i o n s , A aricKB, have d i f f e r e n t r a t e s of p r o d u c t i o n of p h e n o t y p i c v a r i a n c e . B has the h i g h e r r a t e . They e v o l v e under the p a r a b o l i c f i t n e s s f u n c t i o n shown i n F i g u r e 2 . Note t h a t t h i s c u r v e i s concave down so t h a t , g i v e n e q u a l means, the s u b p o p u l a t i o n w i t h g r e a t e r v a r i a n c e i s a t an immediate d i s a d v a n t a g e i n f i t n e s s everywhere under the c u r v e . Here both s u b p o p u l a t i o n s begin w i t h the same s i z e and average phenotype. The s i m u l a t i o n shows t h a t the s u b p o p u l a t i o n w i t h the g r e a t e r v a r i a n c e improves i t s average phenotype a t a g r e a t e r r a t e (see F i g u r e 3 a ) , which over the l o n g e r term l e a d s t o a h i g h e r average f i t n e s s than t h a t of the s u b p o p u l a t i o n w i t h lower v a r i a n c e , which l a g s f a r t h e r away from the a d a p t i v e peak. Short term f i t n e s s causes the s u b p o p u l a t i o n w i t h lower v a r i a n c e t o have g r e a t e r numbers. In g e n e r a t i o n 7 , i n t h i s run (see F i g u r e 3 b ) , the r a n k i n g of s u b p o p u l a t i o n s r e v e r s e s due t o the c u m u l a t i v e e f f e c t of a f i t n e s s advantage g a i n e d by improvement i n average phenotype. T h e r e f o r e , i f we l o o k more than one g e n e r a t i o n ahead we see t h a t s e l e c t i o n can f a v o r g r e a t e r v a r i a n c e p r o d u c t i o n even under a f i t n e s s f u n c t i o n t h a t i s concave down. D i s c u s s i o n Proper e v a l u a t i o n of the r e l a t i v e advantages of d i f f e r e n t r a t e s of v a r i a t i o n p r o d u c t i o n (and t h e r e f o r e , p o p u l a t i o n v a r i a n c e s ) i s dependent on the time s c a l e of comparison. As time s c a l e s l e n g t h e n , a d a p t a b i l i t y g a i n s i n importance r e l a t i v e t o i n i t i a l adaptedness (Appendices I and I I ) . V a r i a t i o n i s 23 F i g u r e 2. An i l l u s t r a t i o n of the i n i t i a l c o n d i t i o n s of the computer s i m u l a t i o n t h a t produced the r e s u l t s i n F i g u r e 3. Two s u b p o p u l a t i o n s , i n i t i a l l y i d e n t i c a l i n s i z e and average phenotype, a r e a l l o w e d t o e v o l v e w i t h r e s p e c t t o q u a n t i t a t i v e t r a i t x under a f i t n e s s f u n c t i o n t h a t i s concave down everywhere. o OJ in in 40 50 6 0 7 0 80 MEASURE OF PHENOTYPE GENERATIONS F i g u r e 3. Output from the computer s i m u l a t i o n model d e s c r i b e d i n Appendix I I I . Two s u b p o p u l a t i o n s are e v o l v i n g towards an a d a p t i v e peak at 75 " p h e n o t y p i c u n i t s " . S u b p o p u l a t i o n B ( d o t t e d l i n e ) has the h i g h e r r a t e of v a r i a t i o n p r o d u c t i o n , (a) Average phenotype over t i m e , (b) Numbers over t i m e . 25 i m p o r t a n t f o r i t s d e t e r m i n a t i o n of the r a t e of p h e n o t y p i c change over t i m e , not j u s t i n i t s c o n t r i b u t i o n t o average p o p u l a t i o n f i t n e s s at any one t i m e . The former e f f e c t must be taken i n t o account i n any r e a l i s t i c a n a l y s i s of the r e l a t i v e advantages of a l l e l e s t h a t c o n f e r d i f f e r e n t r a t e s of v a r i a t i o n p r o d u c t i o n . P o p u l a t i o n g e n e t i c s d e a l s w i t h the s t a t i s t i c a l b e h a v i o r of p o p u l a t i o n s , and we commonly t h i n k of p h e n o t y p i c v a r i a t i o n as a c h a r a c t e r i s t i c of a p o p u l a t i o n . I am a d d r e s s i n g v a r i a t i o n p r o d u c t i o n , which can be t r e a t e d as a l i f e h i s t o r y s t r a t e g y , and above I have shown how these two ' v a r i a t i o n s ' a r e l i n k e d . In t a l k i n g about s e l e c t i o n f o r d i f f e r e n t v a r i a t i o n p r o d u c t i o n , people o f t e n t h i n k of the p o p u l a t i o n c h a r a c t e r i s t i c and deduce t h a t group s e l e c t i o n i s n e c e s s a r y . In the e x p l a n a t i o n above, I have shown how s e l e c t i o n of more i n c l u s i v e c a t e g o r i e s ( i n d i v i d u a l s of many d i f f e r e n t phenotypes w i t h common r a t e s of v a r i a t i o n p r o d u c t i o n ) can take p l a c e v i a t h e i r r e s p e c t i v e subcomponents (by secondary s e l e c t i o n ) , r a t h e r than by p i t t i n g group a g a i n s t group. I t seems obvi o u s t h a t , g i v e n h e r i t a b l e v a r i a t i o n i n v a r i a t i o n p r o d u c t i o n , c e r t a i n p a t t e r n s of v a r i a t i o n w i l l p r e v a i l . But t h i s i s i n t e r e s t i n g because d i f f e r e n t p a t t e r n s a r e f a v o r e d under d i f f e r e n t c o n d i t i o n s — v a r i a t i o n p r o d u c t i o n i s not always m i n i m i z e d . The p o i n t of t h i s s e c t i o n i s t o c o n v i n c e the reader t h a t g i v e n v a r i a t i o n i n v a r i a t i o n p r o d u c t i o n , s e l e c t i o n can produce a d a p t i v e p a t t e r n s of v a r i a t i o n p r o d u c t i o n . In o t h e r words, i t i_s r e a s o n a b l e t o e x p l i c i t l y c o n s i d e r p a t t e r n s of v a r i a t i o n p r o d u c t i o n r a t h e r than t o assume, as has u s u a l l y been done i n the p a s t , t h a t v a r i a t i o n i s random, and l e a v e the 26 e x p l a n a t i o n of e v o l u t i o n a r y p a t t e r n s t o p a t t e r n s i n v a r i a t i o n l o s s , e.g. n a t u r a l s e l e c t i o n and d r i f t . 27 CHAPTER THREE  METAVARIATION The l a s t c h a p t e r p o i n t e d out t h a t many known g e n e t i c f a c t o r s c o u l d be p e r c e i v e d as b e i n g a p a r t of a system f o r r e g u l a t i n g the p r o d u c t i o n of g e n e t i c v a r i a t i o n . I t a l s o e x p l a i n e d how, g i v e n v a r i a t i o n i n these h e r i t a b l e f a c t o r s , n a t u r a l s e l e c t i o n can a c t t o change the p a t t e r n of v a r i a t i o n w i t h i n a p o p u l a t i o n . Chapter One d e s c r i b e d why we c o u l d t h i n k about a system f o r r e g u l a t i n g v a r i a t i o n p r o d u c t i o n . The p r e s e n t c h a p t e r w i l l c o n s i d e r c o n t r o l systems f o r v a r i a t i o n p r o d u c t i o n i n the a b s t r a c t , and take a t h e o r e t i c a l l o o k a t the c o n d i t i o n s under which such a system s h o u l d e x i s t , i f a t a l l . " M e t a v a r i a t i o n " i s my word f o r " v a r i a t i o n i n v a r i a t i o n p r o d u c t i o n " . Given h e r i t a b l e v a r i a t i o n i n phenotype, s e l e c t i o n can mold the g e n e t i c b a s i s of phenotype. G i v e n h e r i t a b l e m e t a v a r i a t i o n , s e l e c t i o n can t a i l o r v a r i a t i o n p r o d u c t i o n . An O p t i m a l Rate of V a r i a t i o n P r o d u c t i o n The ' f u n c t i o n ' of a d d i t i v e v a r i a t i o n i n phenotype i s t o 's e a r c h ' phenotype-space f o r phenotypes b e t t e r f a v o r e d by s e l e c t i o n . In a changing environment t h i s v a r i a t i o n e n a b l e s the g e n e t i c i n f o r m a t i o n of a p o p u l a t i o n t o t r a c k the (changing) o p t i m a l phenotype. I f , i n a ch a n g i n g environment, v a r i a t i o n were produced a t too slow a r a t e , the p o p u l a t i o n would go e x t i n c t once the ch a n g i n g c o n d i t i o n s exceeded the t o l e r a n c e range of a l l the phenotypes. C o m p e t i t i o n w i t h a n o t h e r p o p u l a t i o n of organisms t h a t was b e t t e r a b l e t o t r a c k the changing c o n d i t i o n s c o u l d cause e x t i n c t i o n even i f a l l o t h e r a s p e c t s of the environment 28 c o u l d be t o l e r a t e d . So a g e n e t i c system can produce v a r i a t i o n a t too slow a r a t e . But v a r i a t i o n can be produced a t too g r e a t a r a t e a l s o . U n l e s s the environment changes t o make the o r i g i n a l phenotypes l e s s f i t , p r o d u c i n g e x p e r i m e n t a l phenotypes i s a bad gamble r a t h e r than a n e c e s s i t y . I f the environment has been the same f o r a l o n g t i m e , the p o p u l a t i o n w i l l l i k e l y have e v o l v e d t o be near an a d a p t i v e peak, where the f i t n e s s f u n c t i o n i s concave down. In such a case g r e a t e r v a r i a t i o n p r o d u c t i o n w i l l mean g r e a t e r p r o d u c t i o n of l e s s f i t phenotypes (see Chapter One). I f the environment remains s t a t i c , the best s t r a t e g y would be t o produce no v a r i a t i o n a t a l l . I t appears then t h a t t h e r e i s an o p t i m a l r a t e , or at l e a s t a best range of r a t e s , a t which t o produce v a r i a t i o n g i v e n a p a r t i c u l a r r a t e of change of the environment. In a c c e p t i n g e v o l u t i o n we a r e a c c e p t i n g the i d e a t h a t the w o r l d i s a c h a n g i n g one. But what i f the r a t e of change changes? We have j u s t r e c o g n i z e d t h a t t h e r e i s an o p t i m a l r a t e , or range of r a t e s , a t which t o produce v a r i a t i o n t h a t i s determined by the r a t e of change of the environment. I f we l i v e i n a w o r l d of changes i n e n v i r o n m e n t a l r a t e s of change i t would seem r e a s o n a b l e t h a t g e n e t i c systems be c a p a b l e of t r a c k i n g the moving compromise between adaptedness and a d a p t a b i l i t y . J u s t as v a r i a t i o n i n phenotype i s u s e f u l i n t r a c k i n g an o p t i m a l phenotype, v a r i a t i o n i n v a r i a t i o n p r o d u c t i o n r a t e s p e r m i t s the t r a c k i n g of an o p t i m a l v a r i a t i o n p r o d u c t i o n r a t e . The n o t i o n of an o p t i m a l r a t e a t which t o produce g e n e t i c v a r i a t i o n i s not new. Kimura ( i 9 6 0 ) quotes Auerbach (1956): 29 "Thus each s p e c i e s has t o s t r i k e a b a l a n c e between the s h o r t - t e r m requirement f o r a low f r e q u e n c y of m u t a t i o n and t h e l o n g - t e r m r e q u i r e m e n t f o r an ample s t o r e of mutant genes. A s p e c i e s i n which m u t a t i o n s are t o o f r e q u e n t w i l l d i e out because too many of i t s i n d i v i d u a l s are weak, s h o r t - l i v e d or s t e r i l e . A s p e c i e s i n which m u t a t i o n s a r e t o o r a r e may do w e l l f o r a t i m e , but w i l l not s u r v i v e when a l t e r e d c o n d i t i o n s demand a d a p t a t i o n s f o r which i t does not p o s s e s s the n e c e s s a r y genes." Kimura s t a t e s : "These c o n s i d e r a t i o n s i n e v i t a b l y suggest t h a t t h e r e must be an optimum m u t a t i o n r a t e f o r the s u r v i v a l of a s p e c i e s under a g i v e n r a t e of e n v i r o n m e n t a l change." Kimura (1960) then goes on t o d e s c r i b e what he c a l l s the " P r i n c i p l e of Minimum G e n e t i c Load", by which the e x p e c t e d o p t i m a l m u t a t i o n r a t e can be d e t e r m i n e d . H i s e s s e n t i a l p o i n t s a r e t h e s e : 1. Haldane's (1957) s u b s t i t u t i o n a l l o a d , or c o s t of s u b s t i t u t i n g one a l l e l e of a gene f o r a n o t h e r , i s independent of s e l e c t i o n i n t e n s i t y and depends, i n s t e a d , on the degree of dominance and i n i t i a l f r e q u e n c y of the f a v o r e d mutant. 2. S u b s t i t u t i o n a l l o a d (Le) d e c r e a s e s w i t h g r e a t e r i n i t i a l f r e q u e n c y , and t h e r e f o r e d e c r e a s e s w i t h m u t a t i o n r a t e . 3. M u t a t i o n a l l o a d (Lm) i n c r e a s e s w i t h m u t a t i o n r a t e . 4. The g e n e t i c system s h o u l d modify m u t a t i o n r a t e (and degree of dominance) so t h a t L= Lm + Le i s m i n i m i z e d . I have p r e s e n t e d Kimura's argument o n l y f o r the sake of i n t e r e s t . G i v e n a f a m i l i a r i t y w i t h the concept of g e n e t i c l o a d , Kimura's argument i s s t r a i g h t f o r w a r d t o e x p l a i n . U n f o r t u n a t e l y , h i s argument i n terms of g e n e t i c l o a d i s a group s e l e c t i o n argument, because a g e n e t i c l o a d i s "the p r o p o r t i o n by which the p o p u l a t i o n f i t n e s s i s d e c r e a s e d i n comparison w i t h an optimum 30 genotype" (Crow 1958). The reasons I have d e s c r i b e d f o r the e x i s t e n c e of an o p t i m a l r a t e of v a r i a t i o n p r o d u c t i o n are l e s s c o n c i s e , but they do not i n v o l v e group s e l e c t i o n . I would l i k e t o t r y t o f o r s t a l l some c o n f u s i o n b e f o r e I go on. In Chapter One I p o i n t e d out t h a t the r e l a t i v e importances of adaptedness and a d a p t a b i l i t y depend on the time s c a l e over which the r e s u l t s of s e l e c t i o n a r e c o n s i d e r e d . In the p r e s e n t c h a p t e r I have noted t h a t the o p t i m a l compromise between adaptedness and a d a p t a b i l i t y i s dependent on the r a t e of change of the environment. These a r e s e p a r a t e n o t i o n s . For a g i v e n time h o r i z o n the r a t e of e n v i r o n m e n t a l change w i l l d e t e r m i n e the o p t i m a l compromise. For a g i v e n (changing) environment the time h o r i z o n of an o b s e r v e r ' s comparison w i l l d e t e r m i n e the best s t r a t e g y . To Track or not t o Tra c k ? Whether t r a c k i n g a best phenotype or a be s t v a r i a t i o n p r o d u c t i o n r a t e , the b a s i c problem i s i n d e t e r m i n i n g how r e s p o n s i v e t o be t o 'movement of the t a r g e t ' . How a d a p t a b l e s h o u l d a system be, or when a r e the immediate c o s t s of a d a p t a b i l i t y worth b e a r i n g ? I c o n s i d e r R i c h a r d L e v i n s (1962,1963,1964a,1964b,1965,1967) t o be the p i o n e e r of most of the t r a c k i n g i d e a s . The i s s u e of a d a p t a b i l i t y a r i s e s as soon as the w o r l d i s viewed as one of "changing e n v i r o n m e n t s " . (He d e s c r i b e d L a y z e r ' s mechanism a l g e b r a i c a l l y i n L e v i n s (1964b), p. 638) L e v i n s r e c o g n i z e d t h a t v a r i a t i o n p r o d u c t i o n was an a d a p t i v e system, and t h a t the genome might be tuned t o produce the o p t i m a l r a t e of v a r i a t i o n 31 p r o d u c t i o n by secondary s e l e c t i o n . The immediate c o s t s of v a r i a t i o n p r o d u c t i o n a r e o n l y worth b e a r i n g i f the t a r g e t i s p r e d i c t a b l e 'enough'. " I f the p a t t e r n of e n v i r o n m e n t a l change i s such as t o make pa s t environments poor p r e d i c t o r s of p r e s e n t e n v i r o n m e n t s , p o p u l a t i o n s t h a t have responded a d a p t i v e l y t o p a s t environments w i l l be i l l - a d a p t e d t o p r e s e n t ones" ( L e v i n s 1965). P r e d i c t a b i l i t y , or a u t o c o r r e l a t i o n , i s t h e r e f o r e an . i m p o r t a n t e n v i r o n m e n t a l parameter i n the d e t e r m i n a t i o n of the a d a p t e d n e s s / a d a p t a b i l i t y compromise. The d e t e r m i n a t i o n of what i s p r e d i c t a b l e 'enough' i s beyond the scope of t h i s paper. But L e v i n s e x p l o r e d a u t o c o r r e l a t i o n w i t h a s i m u l a t i o n model i n which p h e n o t y p i c v a r i a n c e was a d j u s t a b l e v i a s e l e c t i o n on a g e n e t i c d e t e r m i n a n t of the average e f f e c t of an a l l e l e on phenotype. H i s a n a l y t i c a l c a l c u l a t i o n s (1964) and Monte C a r l o e x p e r i m e n t s (1965) both suggest t h a t p h e n o t y p i c v a r i a n c e s h o u l d be g r e a t e r than z e r o o n l y i f the e n v i r o n m e n t a l a u t o c o r r e l a t i o n from one g e n e r a t i o n t o the next i s g r e a t e r than about 0.8. M e t a v a r i a t i o n In my d i s c u s s i o n of how g e n e t i c a l l y r e s p o n s i v e a p o p u l a t i o n s h o u l d be t o changes i n the environment I have been u s i n g a s p a t i a l metaphor of t r a c k i n g , or s e a r c h i n g f o r , a moving t a r g e t . L e v i n s ' problem was t o l o o k a t the a d a p t e d n e s s / a d a p t a b i l i t y compromise i n the g e n e t i c d e t e r m i n a t i o n of phenotype. My i n t e r e s t here w i l l be i n examining the analogous problem of g e n e t i c d e t e r m i n a t i o n of p h e n o t y p i c v a r i a t i o n p r o d u c t i o n . P h e n o t y p i c v a r i a t i o n has the f u n c t i o n of t r a c k i n g i n phenotype-32 space; v a r i a t i o n i n v a r i a t i o n p r o d u c t i o n , which I w i l l c a l l ' m e t a v a r i a t i o n ' , has the f u n c t i o n of t r a c k i n g i n v a r i a t i o n -p r o d u c t i o n - s p a c e . The problems are the same except t h a t they a r e on d i f f e r e n t l e v e l s . E a r l i e r work has demonstrated t h a t a u t o c o r r e l a t i o n i n the e n v i r o n m e n t a l l y d e t e r m i n e d o p t i m a l phenotype i s an i m p o r t a n t f a c t o r i n d e t e r m i n i n g how w e l l t o t r a c k , i . e . a t what r a t e t o produce p h e n o t y p i c v a r i a t i o n . By a n a l o g y , a u t o c o r r e l a t i o n i s p r o b a b l y i m p o r t a n t i n d e t e r m i n i n g the r a t e a t which t o produce metavar i a t i o n . Time S c a l e Dependence At t h i s time i t must be emphasized t h a t the s t a t i s t i c ' a u t o c o r r e l a t i o n ' i s time s c a l e dependent. "The a u t o c o r r e l a t i o n f u n c t i o n . . . i s a measure of the degree of c o r r e l a t i o n between a s e r i e s as o b s e r v e d and t h a t same s e r i e s i f i n i t i a t e d a f t e r a s p e c i f i e d time l a g . " ( F i n e r t y 1980) L e v i n s was d e a l i n g w i t h a o n e - g e n e r a t i o n time l a g , i . e . how p r e d i c t a b l e an environmejrt i s from one g e n e r a t i o n t o the n e x t . T h i s i s because one g e n e r a t i o n i s the minimum time over which d i f f e r e n t i a l r e p r o d u c t i o n can i n f l u e n c e gene f r e q u e n c i e s ; i t i s the minimum time s c a l e over which the g e n e t i c system can respond t o a changing environment. Any e n v i r o n m e n t a l change on a s h o r t e r time s c a l e , i . e . w i t h i n a g e n e r a t i o n , must be d e a l t w i t h by a f a s t e r response. F a s t e r responses i n c l u d e d e v e l o p m e n t a l a d j u s t m e n t , a c c l i m a t i z a t i o n , and s h o r t e r term b e h a v i o r a l and p h y s i o l o g i c a l r e s p o n s e s . Given t h i s time s c a l e c o n s i d e r a t i o n , we now make the r e f i n e m e n t t h a t a t r a c k i n g system s h o u l d respond o n l y i f the environment i s 33 p r e d i c t a b l e enough on the time s c a l e over which the system can respond. When i s M e t a v a r i a t i o n Important? The computer model d e s c r i b e d i n Appendix I works w e l l f o r i t s i n t e n d e d purpose of comparing d i f f e r e n t v a r i a t i o n p r o d u c t i o n schemes i n v a r i o u s e n v i r o n m e n t s . The s e l e c t i o n regime i n a one-d i m e n s i o n a l environment i s m o d e l l e d as a f i t n e s s f u n c t i o n i n the form of an a d a p t i v e peak d e f i n i n g the o p t i m a l phenotype. The form and b r e a d t h of the a d a p t i v e peak are m o d i f i a b l e t o change the immediate c o s t of v a r i a t i o n p r o d u c t i o n ( u n f i t v a r i a n t s ) . The e n v i r o n m e n t a l change from g e n e r a t i o n t o g e n e r a t i o n can be a r b i t r a r i l y s p e c i f i e d . Up t o s i x a s e x u a l p o p u l a t i o n s w i t h " a r b i t r a r y " v a r i a t i o n p r o d u c t i o n schemes can be run at the same t i m e , i n d e p e n d e n t l y or i n c o m p e t i t i o n w i t h each o t h e r . The output c o n s i s t s of the f o l l o w i n g s t a t i s t i c s f o r each g e n e r a t i o n : p o p u l a t i o n s i z e , average phenotype and r e l a t i v e average f i t n e s s e s f o r each p o p u l a t i o n , and average r a t e of v a r i a t i o n p r o d u c t i o n f o r a l l p o p u l a t i o n s . The d a t a a r e produced i n t a b u l a r and p l o t form. The above computer model i s not adequate f o r d e t e r m i n i n g the c o n d i t i o n s under which m e t a v a r i a t i o n i s i m p o r t a n t . The q u e s t i o n i s not whether any p a r t i c u l a r v a r i a t i o n scheme i s b e t t e r than a n o t h e r under c e r t a i n c i r c u m s t a n c e s , but whether a d j u s t a b l e v a r i a t i o n , g i v e n i t s c o s t s , i s ever a t an advantage compared w i t h f i x e d v a r i a t i o n p r o d u c t i o n . The computer model c o n f i r m s what has been d i s c u s s e d about d i f f e r e n t o p t i m a l r a t e s of v a r i a t i o n p r o d u c t i o n f o r d i f f e r e n t k i n d s of e n v i r o n m e n t a l 34 change, but i t s c o n s t r a i n t of a s e x u a l r e p r o d u c t i o n r e s t r i c t s g e n e r a l i t y , and i t i s not equipped t o compare a p o p u l a t i o n w i t h a d j u s t a b l e v a r i a t i o n w i t h one w i t h f i x e d v a r i a t i o n . F u rthermore, i t was u n c l e a r t o me how such an e x p l o r a t o r y model c o u l d be used t o c o n f i d e n t l y d e l i m i t a l l of the c o n d i t i o n s under which the c o s t s of a m e t a v a r i a t i o n system would be worth b e a r i n g . The c o s t s of m e t a v a r i a t i o n a r e of two k i n d s : 1. F i r s t , t h e r e i s the a d d i t i o n a l m e t a b o l i c c o s t i n c u r r e d t o the i n d i v i d u a l organism i n the form of DNA i n v o l v e d o n l y i n the r e g u l a t i o n of v a r i a t i o n p r o d u c t i o n . In the s h o r t term a genome co m p r i s e d s o l e l y of DNA i n v o l v e d i n development and maintenance of the i n d i v i d u a l phenotype might be 'cheaper'. I t i s u n c e r t a i n what e f f e c t s " e x t r a " DNA would have on an o r g a n i s m . Some, a u t h o r s a re p r e p a r e d t o assume t h a t a s i g n i f i c a n t p r o p o r t i o n of e u k a r y o t e genomes i s "j u n k " , u s e l e s s t o the i n d i v i d u a l . G i v e n the l a r g e amount of DNA i n e u k a r y o t e s t h a t i s of no demonstrated u s e f u l n e s s , i t might be s a f e t o assume t h a t the amount of DNA r e q u i r e d f o r a m e t a v a r i a t i o n system would have a v e r y s m a l l e f f e c t on immediate f i t n e s s . See Chapter Four f o r f u r t h e r d i s c u s s i o n of the s e c o n c e r n s . 2. A second c a t e g o r y of c o s t s a r i s e s a t the l i n e a g e , or p o p u l a t i o n l e v e l s . I t can be measured by comparing the c o s t s of h a v i n g a f i x e d v a r i a t i o n p r o d u c t i o n scheme, and not r e s p o n d i n g t o change i n e n v i r o n m e n t a l change, w i t h the c o s t s of p o s s i b l y r e s p o n d i n g i n a p p r o p r i a t e l y . As j u s t d i s c u s s e d , such i n a p p r o p r i a t e response can occur i f the environment i s not s u f f i c i e n t l y a u t o c o r r e l a t e d on the time 35 s c a l e over which the r e g u l a t i o n system can respond. A system t h a t responds too q u i c k l y t o immediate c o n d i t i o n s i s d i s a d v a n t a g e o u s i f immediate c o n d i t i o n s a re anomalous, and t h e r e f o r e bad p r e d i c t o r s of f u t u r e c o n d i t i o n s . Given a p r e d i c t a b l e environment, a system may respond too s l o w l y , and thus always be adapted t o the way t h i n g s were. A q u a n t i t a t i v e assessment of the c o n d i t i o n s r e q u i r e d t o f a v o r m e t a v a r i a t i o n over f i x e d v a r i a t i o n r e q u i r e s knowledge o f : 1 . the t o l e r a n c e of i n d i v i d u a l s t o the a m p l i t u d e of e n v i r o n m e n t a l v a r i a b i l i t y . T h i s i s imp o r t a n t i n d e t e r m i n i n g the c o s t of not r e s p o n d i n g , and the b e n e f i t of r e s p o n d i n g . 2. the p o t e n t i a l speed of response of a p a r t i c u l a r m e t a v a r i a t i o n system 3. the p r e d i c t a b i l i t y of e n v i r o n m e n t a l change, from the v i e w p o i n t of the organism, on the time s c a l e of response of i t s assumed m e t a v a r i a t i o n system. I c o n c l u d e d t h a t my o r i g i n a l i n t e n t i o n of q u a n t i t a t i v e l y d e s c r i b i n g a l l the s e t s of c o n d i t i o n s under which a m e t a v a r i a t i o n system would be advantageous was too complex t o manage w i t h i n the scope of t h i s t h e s i s . I t would have i n c l u d e d enough unmeasurable v a r i a b l e s t o be of l i t t l e immediate use. Below I o f f e r a q u a l i t a t i v e assessment of how f a s t a v a r i a t i o n r e g u l a t i o n system might respond, s h o u l d i t e x i s t . But f i r s t , I would l i k e t o emphasize t h a t my i n t e n d e d q u a n t i t a t i v e assessment was t o answer j u s t a p a r t i c u l a r i n s t a n c e of the more g e n e r a l q u e s t i o n "What speeds of i n c o r p o r a t i o n of 36 i n f o r m a t i o n about the environment i n t o the genotype are advantageous t o l i v i n g systems?" I can imagine f o u r d i f f e r e n t models of v a r i a t i o n p r o d u c t i o n and s e l e c t i o n , each w i t h a d i f f e r e n t feedback speed of i n f o r m a t i o n from the environment t o the g e n e t i c m a t e r i a l : 1. t r i a l and e r r o r -- T h i s i s the s t a n d a r d assumption of random ( u n d i r e c t e d ) v a r i a t i o n . M u t a t i o n s happen i n a way u n c o r r e l a t e d w i t h t h e i r p o t e n t i a l u s e f u l n e s s . See Warburton (1967) f o r a model of s e l e c t i o n based on the t h e o r y of g u e s s i n g games. 2. p a t t e r n e d t r i a l and e r r o r -- V a r i a t i o n p r o d u c t i o n can be f o c u s s e d i n p a t t e r n s t h a t a r e more l i k e l y t o be b e n e f i c i a l . S e l e c t i o n on a l pha-genes produces ' h e u r i s t i c s ' s t o r e d i n ( l o n g e r memory) beta-genes. 3. s t r e s s - p r o d u c e d t r i a l s -- L i f e t i m e e x p e r i e n c e s enhance v a r i a t i o n p r o d u c t i o n i n an i n d i v i d u a l ' s germ l i n e w i t h r e s p e c t t o s t r e s s e d t r a i t s (see McDonald 1983). 4. d i r e c t programming (Lamarckian) -- No t r i a l and e r r o r p r o c e s s moderated by n a t u r a l s e l e c t i o n . L i f e t i m e e x p e r i e n c e programs an i n d i v i d u a l ' s gametes. C h a r a c t e r i s t i c s a re a c q u i r e d s t e a d i l y , i f not a l l a t once. V a r i a t i o n p r o d u c t i o n i s always i n the d i r e c t i o n of improvement. Not a l l of these feedback speeds have r e c e i v e d e q u a l a t t e n t i o n . I s t h a t r e a s o n a b l e ? A q u a n t i t a t i v e d e m o n s t r a t i o n t h a t Lamarckian i n h e r i t a n c e would seldom or never be advantageous, even i f i t were p o s s i b l e , would be much more p o w e r f u l than d i s c r e d i t i n g i t on the b a s i s of what we do not know, i . e . l a c k 37 of e v i d e n c e f o r the r e q u i r e d c o n n e c t i o n s between environment and g e n e t i c m a t e r i a l . The q u a n t i t a t i v e t h e o r y n e c e s s a r y t o s p e c i f y the p o t e n t i a l u t i l i t y of any of^^these feedback speeds i s , to my knowledge, l a c k i n g i n the b i o l o g i c a l l i t e r a t u r e . T h i s i s an area r e q u i r i n g a t t e n t i o n . C o n s i d e r F i g u r e 4, which p i c t u r e s a h i e r a r c h y of c o n t r o l systems: the phenotype i n c l u d e s s e v e r a l l e v e l s of c o n t r o l system (see Bateson 1963), the a l p h a genes c o n t r o l the phenotype t h a t i s d e v e l o p e d , and the beta-genes c o n t r o l the g e n e r a t i o n of new ( a l p h a - ) genotypes. (The ' a l p h a ' and 'beta' d i s t i n c t i o n was made by L a y z e r 1980.) A c c o r d i n g t o h i e r a r c h y t h e o r y (see Simon 1973) we expect h i g h e r l e v e l s i n the h i e r a r c h y t o change more s l o w l y and t o det e r m i n e l o n g e r term p a t t e r n s , and lower l e v e l s t o be f a s t e r and i m p o r t a n t i n the s h o r t term. In the h i e r a r c h i c a l o r g a n i z a t i o n of F i g u r e 4, changes i n each l e v e l a r e s e l e c t e d v i a the l e v e l s below. ( T h i s i s not group s e l e c t i o n . ) The ' s e l e c t i o n p r e s s u r e ' each l e v e l f a c e s i s com p r i s e d of the d i f f e r e n t i a l ' f i t n e s s e s ' of the l e v e l j u s t below. The d i f f e r e n t i a l f i t n e s s e s of phenotypes d e t e r m i n e the change i n gene f r e q u e n c i e s of alpha-genes w i t h i n a p o p u l a t i o n . The degree t o which the s t r e n g t h of s e l e c t i o n on the phenotypes i s r e f l e c t e d i n a change i n gene f r e q u e n c i e s depends on the degree of correspondence between phenotype and genotype, i . e . the h e r i t a b i l i t y , h 2 ( 0 < h 2 < l ) . T h i s correspondence i s never p e r f e c t because t h r o u g h dominance and e p i s t a s i s more than one genotype can code f o r a g i v e n phenotype and, s i n c e the development of a phenotype proceeds i n i n t e r a c t i o n w i t h the environment, e n v i r o n m e n t a l v a r i a t i o n can produce d i f f e r e n t R A N D O M PARAMETERS OF THE N O N - R A N D O M STRUCTURAL AND REGULATORY GENES (©< G E N E S ) E P I G E N E S I S 5 PHENOTYPE 7 V A R I A T I O N P R O D U C T I O N GENETIC SYSTEM {J9 G E N E S ) V A R I A T I O N P R O D U C T I O N S M E T A V A R I A T I O N ( S E C O N D A R Y ) S E L E C T I O N G I V E N C O R R E S P O N D E N C E OF G E N O T Y P E S WITH P A R T I C U L A R P A R A M E T E R S G I V E N C O R R E S P O N D E N C E OF P H E N O T Y P E WITH G E N O T Y P E F i g u r e 4. The r e l a t i o n s h i p of alp h a and beta genes, and the l e v e l s of i n d i r e c t i o n i n secondary s e l e c t i o n . CO 39 phenotypes from the same genotype. (response t o ) = h 2 ( s t r e n g t h o f ) ( s e l e c t i o n ) ( s e l e c t i o n ) (Roughgarden 1979) So we can say t h a t (change i n a l p h a ) = h , 2 ( s t r e n g t h of s e l e c t i o n ) (gene f r e q u e n c i e s ) ( on phenotypes ). The d i f f e r e n t i a l ' f i t n e s s e s ' of genotypes ( a l p h a genes) determine the change i n f r e q u e n c i e s of the 'metagenotypes' ( b e t a g e n e s ) . The correspondence between these l e v e l s i s not p e r f e c t e i t h e r ( h 2 2 < l ) . T h i s i s because the beta genes (as d e f i n e d by L a y z e r ( l 9 8 0 ) and i n F i g u r e 4) j u s t t a i l o r the v a r i a b i 1 i t y of each a l p h a l o c u s ( r a t h e r than p r e s c r i b e the p a r t i c u l a r a l l e l e , which would i n v o l v e a Lamarckian mechanism or s e t t i n g v a r i a b i l i t y = 0 ) ; a g i v e n beta a l l e l e may cause the g e n e r a t i o n of any number of d i f f e r e n t a l p h a a l l e l e s , and c o n v e r s e l y , a p a r t i c u l a r a l p h a a l l e l e may-be a s s o c i a t e d w i t h many d i f f e r e n t b eta a l l e l e s . So we have ( change i n beta ) = h 2 2 ( s t r e n g t h of s e l e c t i o n ) (gene f r e q u e n c i e s ) ( on alph a - g e n o t y p e s ) Se x u a l r e c o m b i n a t i o n f u r t h e r d e c r e a s e s the c o r r e l a t i o n , or l i n k a g e d i s e q u i l i b r i u m , between the beta a l l e l e s and the a l p h a a l l e l e s t h a t they produce. The reader i s r e f e r r e d t o K a r l i n and McGregor (1974) f o r e v i d e n c e t h a t the mechanism of secondary s e l e c t i o n can work w i t h i n s e x u a l l y r e p r o d u c i n g p o p u l a t i o n s . They de t e r m i n e d t h a t "Linkage between m o d i f i e r and pri m a r y l o c i appears t o a f f e c t o n l y the speed of f i x a t i o n or approach t o polymorphism but not the q u a l i t a t i v e n a t u r e of the outcome" a t the m o d i f i e r (beta) l o c u s . There are two l e v e l s of i n d i r e c t i o n between s e l e c t i o n on phenotypes and changes i n be t a gene f r e q u e n c i e s (see F i g u r e 4 ) . The s t r e n g t h of s e l e c t i o n on the phenotype i s d i l u t e d by two 40 s u c c e s s i v e ' h e r i t a b i l i t y ' f a c t o r s , so t h a t the response at the beta gene l e v e l , the v a r i a t i o n - p a t t e r n i n g l e v e l , i s ve r y slow. L e v i n s (1965) c a l c u l a t e s t h a t t h i s response would n e v e r t h e l e s s be i m p o r t a n t on a time s c a l e much s h o r t e r than a s p e c i e s l i f e t i m e . But the p o i n t i s t h a t the p a t t e r n s of change i n v o l v i n g adjustment of v a r i a t i o n p r o d u c t i o n a re on an e v o l u t i o n a r y time s c a l e , r a t h e r than the g e n e r a t i o n t o g e n e r a t i o n e c o l o g i c a l time s c a l e u s u a l l y d e a l t w i t h i n c l a s s i c a l p o p u l a t i o n g e n e t i c s . The R e a l World i s M u l t i d i m e n s i o n a l For s i m p l i c i t y I have, u n t i l now, i g n o r e d the f a c t t h a t the w o r l d i s m u l t i d i m e n s i o n a l . In Chapter One I e x p l a i n e d the m o d i f i c a t i o n of v a r i a t i o n p r o d u c t i o n o n l y i n terms of one, a l l -i m p o r t a n t , t r a i t . That s i m p l i f i c a t i o n a v o i d e d the f a c t s t h a t d i f f e r e n t t r a i t s can have d i f f e r e n t v a r i a t i o n p r o d u c t i o n r a t e s , and t h a t t h e r e can be c o v a r i a n c e i n f i t n e s s among those t r a i t s . NOTE: ' T r a i t ' i s an awkward term i n t h a t i t r e f e r s t o a s u b j e c t i v e l y d e f i n e d component of phenotype. Almost any as p e c t of phenotype can be c a l l e d a t r a i t . The term i s u s u a l l y used t o i d e n t i f y components of phenotype p a r t i c u l a r l y r e l e v a n t t o the s e l e c t i o n regime b e i n g d i s c u s s e d i n orde r t o f a c i l i t a t e phenotype-phenotype c o m p a r i s o n s . That i s how i t i s used h e r e . J u s t as phenotype- or t r a i t - s p a c e i s m u l t i d i m e n s i o n a l , so i s v a r i a t i o n - p r o d u c t i o n - s p a c e . A d j u s t i n g r a t e s of v a r i a t i o n p r o d u c t i o n makes sense o n l y i f the r a t e of e n v i r o n m e n t a l change changes. But the environment may not change i n a l l r e s p e c t s a t once," and o n l y a subset of v a r i a n t s may have p o t e n t i a l 41 usefulness. For example, i f the environment only changes in temperature then only temperature variants would be required for adaptability -- variants of any other sort have no potential usefulness. Consider the problem from another perspective. Let us say that variation production i s regulated in populations of a p a r t i c u l a r type of organism by a mechanism a f f e c t i n g a l l t r a i t s , say by d i f f e r e n t a l l e l e s of a genetic repair enzyme, one of which is more e f f e c t i v e than the other. Selection for temperature variants would i n d i r e c t l y favor the less e f f e c t i v e a l l e l e that produced more variants. But this d i r e c t i o n a l selection would be in opposition to the s t a b i l i z i n g selection acting on a l l other phenotypic t r a i t s . The l a t t e r would favor the more e f f e c t i v e repair enzyme, that caused lower variant production. And i f the d i r e c t i o n a l selection were strong enough to select for greater production of variants, because of the general effect of the genetic repair system, variants in a l l t r a i t s would be produced, whereas only temperature variants have a chance of having a higher f i t n e s s . From t h i s kind of argument i t i s clear that the most responsive v a r i a t i o n adjustment system would be one that could independently regulate the production of variants of d i f f e r e n t t r a i t s . In the population genetics l i t e r a t u r e , the interference of selection on one locus with selection on other l o c i that are s t a t i s t i c a l l y correlated (in linkage disequilibrium) with i t i s known as the Hill-Robertson e f f e c t (Felsenstein 1974). The process of recombination destroys linkage disequilibrium among 42 l o c i in a p o p u l a t i o n , and that f u n c t i o n u n d e r l i e s a l l exp l a n a t i o n s of the e v o l u t i o n a r y advantages of recombination ( F e l s e n s t e i n 1974, F e l s e n s t e i n and Yokoyama 1976). V a r i a t i o n Product ion and Genet i c Memory The s p a t i a l metaphor of t a r g e t - t r a c k i n g i s not the only metaphor u s e f u l in d i s c u s s i n g e v o l u t i o n a r y dynamics. I n s i g h t s can a l s o be gained by t h i n k i n g of e v o l u t i o n in terms of a c q u i r i n g and r e j e c t i n g i n f o r m a t i o n . The a r r a y of gene f r e q u e n c i e s i n a p o p u l a t i o n c o n t a i n s i n d i r e c t i n f o r m a t i o n about i t s environment i n the present and, sin c e f i x a t i o n or l o s s takes time, i n the past. Warburton (1967) has, in f a c t , modelled n a t u r a l s e l e c t i o n as a guessing game where mutations are "guesses" and s u c c e s s f u l a l l e l e s are s u f f i c i e n t l y " r i g h t " answers. Lev i n s (1968) p o i n t s out that the gene pool of a p o p u l a t i o n i s a memory, as we l l as a r e c i p e f o r phenotypes capable of s u r v i v a l . A very long memory, in which gene f r e q u e n c i e s depended on a l l the environments of the past, with equal weight, would "know" a l o t about the environment and i t s h i s t o r y , but i t c o u l d not t r a c k recent c o n d i t i o n s . To t r a c k the recent environment, gene f r e q u e n c i e s would have to be p r i m a r i l y determined by the recent environment, r a t h e r than the h i s t o r y of c o n d i t i o n s . Memory i s lengthened or shortened by reducing or enhancing g e n e t i c v a r i a t i o n p r o d u c t i o n , r e s p e c t i v e l y . "The paradox which now emerges i s that only a system with short memory can f o l l o w the environment. But the optimum parameters of the t r a c k i n g system depend on the mean, 43 v a r i a n c e , and a u t o c o r r e l a t i o n of the environment. These can o n l y be e s t i m a t e d a c c u r a t e l y by a system w i t h a l o n g enough memory so t h a t the law of l a r g e numbers o p e r a t e s . S i n c e the s t a t i s t i c s of the environment a re a l s o s u b j e c t t o change, the c a l i b r a t i n g system cannot have i n f i n i t e memory. There i s some optimum l e v e l of memory f o r i t , which can o n l y be e s t a b l i s h e d by systems w i t h l o n g e r memory, e t c . " ( L e v i n s 1968) L e v i n s p e r c e i v e s a problem, or paradox, because he i s t a c i t l y assuming t h a t a p o p u l a t i o n can have o n l y one memory, i . e . one gene p o o l . I f organisms c o n t a i n o n l y a l p h a genes, t h a t i s t r u e . But i f they had beta genes as w e l l , t h a t would mean two memories f o r a p o p u l a t i o n : one s h o r t memory of a l p h a gene f r e q u e n c i e s , and another l o n g e r , more s l o w l y c h a n g i n g memory of beta genes e n c o d i n g the s t r a t e g y f o r the a l p h a genes. So i f we suppose t h a t s u c c e s s f u l organisms are c o n s t r u c t e d i n such a way as t o d e a l w i t h the a d a p t e d n e s s / a d a p t a b i 1 i t y t r a d e o f f a t the g e n e t i c l e v e l , s i n c e the assessment of the e x i s t e n c e of s u f f i c i e n t a u t o c o r r e l a t i o n i n the environment r e q u i r e s a l o n g memory, and r e s p o n s i v e n e s s r e q u i r e s a s h o r t memory, does i t not make sense t o expect a t l e a s t two k i n d s of g e n e t i c memory? 44 CHAPTER FOUR  GENOME SIZE PATTERNS I have been a s s e r t i n g the p o s s i b i l i t y t h a t g e n e t i c c o n t r o l d e t e r m i n e s a p a t t e r n of v a r i a t i o n p r o d u c t i o n s u i t a b l e t o the r a t e and d i r e c t i o n of change of a p o p u l a t i o n ' s e n v i r o n m e n t . S i n c e a g e n e t i c c o n t r o l system has i m p l i c a t i o n s f o r genome s t r u c t u r e , and genome s i z e (the t o t a l amount of DNA per c e l l ) i s a crude i n d i c a t o r of d i f f e r e n c e s i n genome s t r u c t u r e , i t seems r e a s o n a b l e t o examine p a t t e r n s i n genome s i z e among s p e c i e s f o r ev i d e n c e of p a t t e r n s a c r o s s environments d i f f e r i n g i n r a t e s of change. Below I review known p a t t e r n s i n genome s i z e , t a k e a c r i t i c a l l o o k a t the e x i s t i n g e x p l a n a t i o n s f o r them, and propose an e x p l a n a t i o n based on e n v i r o n m e n t a l r a t e s of change and the r e g u l a t i o n of v a r i a t i o n p r o d u c t i o n . The P a t t e r n s and the C-value Paradox There i s e x t e n s i v e v a r i a t i o n i n the amount of DNA per genome a c r o s s a n i m a l and p l a n t t a x a (see F i g u r e 5). The range i n genome s i z e w i t h i n each group a l s o v a r i e s c o n s i d e r a b l y . W h i l e t h e r e i s l i t t l e s p e c i e s t o s p e c i e s v a r i a t i o n among r e p t i l e s , b i r d s , and mammals, DNA amounts i n amphibians span the e n t i r e range of t h e s e groups. DNA amount i n b i r d s v a r i e s by l e s s than a f a c t o r of two, but i t ranges over t h r e e o r d e r s of magnitude i n a l g a e and p r o t o z o a . Genome s i z e has been observed t o v a r y among t a x a a t a l l l e v e l s . But i n t r a s p e c i f i c v a r i a t i o n i n genome s i z e i s s t i l l the e x c e p t i o n ; r e p o r t s of i t a r e p r o b a b l y o v e r - r e p r e s e n t e d i n the 45 - l — I I l m i ; - I — I I M T T T I — T T T T T — I I I 111 ] — c' i i i m i i ~ ~ _^  o" T — I I I I l l l | "1 1—I I M III] 1—I I I r t ; A. ANIMALS 1 ~ M C T A T X R i A I M o w M K l J MAMMAL** , PnOTQTMCRiA (I CCCCNQ I O N A ' C E L L I H A P L O I O J 1 $T *vt5 (B*tfi> ANUftA (Frog* and ToofrU 1 . 1 1 • • i 1 . 1 — — " UROOCL« I S o K m M f i 11 APOOA ( C o v c i U m * —* | f>PNOA (Lung f * h n l . D'<*/G£*OMt ] 3 N A / C M O 0 M 0 $ 0 M C I TOTAL 0N4*IN MULTINUCLEATED CELLS _t . OiN&E FO« W E E N »LCAE ^ ^ • " • " ^ j j j TELtOSTCl I J K X O S T E l | t*ONT riSMCS 1 , J CMONDROSTCi J 1 , 5 A G N A T H A (Lomprtn and Mrjq«*h«v) 1 [ aPMALOCMORDATA ( A ^ c ^ u * ! ' UROCHCAOATA I T ^ c e t r t ) • £ ARTMROPOOA ' MOLLUSCA 11 ANNCLlCA (&«QmrM*<9 Wo"m) 1 , 7 CC«NO0C«VATA 11 KMATOOA (flcvd—*™! 11 C O t L t N T E W T A I 2 POmr fRA <Spo«ont B. PLANTS G » M » * O S P t « ! M t E J J S P E R M t T C V i t T E S | SPHEKO**StOA I H V W I O H I 1 5 LYCOPSlDA (CutJ-MOTt*!) PTEBiOOPMrTES BACTERIA AND VIRUSES \ 56 B A C T E * » i A 32 2 - 5 DNA v i f t u s t s f. * 5 AND - S DNA ViftUSES I t I 11III _ l ' 1 1 1 ' ' I ' NUCLEOTIDES ' i m i l I 1_1_L1 U l l -F i g u r e 5. The ranges of DNA (RNA f o r some v i r u s e s ) c o n t e n t per c e l l and per chromosome i n major c a t e g o r i e s of p r o k a r y o t i c ad e u k a r y o t i c o r g a nisms. The number of s p e c i e s r e p r e s e n t e d i s t o the r i g h t of each e n t r y , (from P r i c e 1976) 46 l i t e r a t u r e , and many of them have not been c o n f i r m e d by subsequent s t u d i e s (Bennett and Smith 1976). C u r r e n t methods cannot r e l i a b l y d e t e c t v a r i a t i o n a t l e v e l s below 3-5% (Bennett and Smith 1976), and i t i s t h e r e f o r e p o s s i b l e t h a t much i n t r a s p e c i f i c v a r i a t i o n goes undemonstrated. The n o t i o n t h a t the r o l e of DNA i s t o program an organism and i t s development l e a d s t o the e x p e c t a t i o n t h a t the amount of DNA s h o u l d v a r y w i t h the i n f o r m a t i o n requirement of organisms. But from what i s known about i n f o r m a t i o n r e q u i r e m e n t s , t h e r e i s no s i g n i f i c a n t c o r r e l a t i o n (Sparrow e t a l . 1972); t h i s problem has become known as the 'C-value paradox'. (Whereas the n-value of a c e l l r e f e r s t o number of chromosomes, e.g. n f o r h a p l o i d and 2n f o r d i p l o i d , c - v a l u e i s a r e l a t i v e measure of amount of DNA by w e i g h t . A b s o l u t e w e i g h t s a r e t y p i c a l l y i n ' p i c o g r a m s . ) Moreover, i t i s d i f f i c u l t t o d e s c r i b e why t h e r e i s so much DNA i n any e u k a r y o t e s p e c i e s . A l t h o u g h t h e r e a r e problems i n e s t i m a t i o n ( B i s h o p 1974), most e s t i m a t e s i n d i c a t e t h a t o n l y a s m a l l p r o p o r t i o n of the e u k a r y o t e genome codes f o r p r o t e i n s ( C r i c k 1971; Ohno 1972). The h y p o t h e s i s t h a t the r e m a i n i n g DNA i s i n v o l v e d i n t r a n s c r i p t i o n a l c o n t r o l and r e g u l a t i o n ( B r i t t e n and Davidson 1969,1971; Z u c k e r k a n d l 1974,1976) seems unable t o e x p l a i n why two c l o s e l y r e l a t e d s p e c i e s would d i f f e r markedly i n t h e i r DNA c o n t e n t s (Walker 1968). A l t h o u g h the e x p e c t e d r u l e of genome s i z e i n c r e a s e w i t h organism c o m p l e x i t y does not h o l d , many p a t t e r n s i n genome s i z e have been o b s e r v e d . I t i s not known what th e s e p a t t e r n s mean. S t u d y i n g them may suggest a f u n c t i o n f o r 'excess' DNA, t u r n out t o be c o n s i s t e n t w i t h the dynamics of 'junk' and/or ' s e l f i s h ' 47 DNA (see b e l o w ) , . or p o i n t t o some o t h e r f a c t o r c a u s i n g p a r t i c u l a r v a l u e s of both DNA q u a n t i t y and the c o r r e l a t e d c h a r a c t e r . At p r e s e n t t h e r e seem to be almost as many ' e x p l a n a t i o n s ' as t h e r e a r e p a t t e r n s . In Ta b l e 2 are l i s t e d p a t t e r n s i n genome s i z e r e p o r t e d i n the l i t e r a t u r e . T h i s l i s t i s not i n t e n d e d t o be e x h a u s t i v e , but to i l l u s t r a t e the apparent non-random d i s t r i b u t i o n of DNA amount. The E x p l a n a t i o n s I t i s o b v i o u s t h a t t h e r e a r e two broad p o s s i b i l i t i e s f o r the mystery DNA. I t c o u l d have a f u n c t i o n , and many a u t h o r s have c a u t i o n e d t h a t i t might n o t . I t c o u l d j u s t be 'junk' and t h a t DNA i s , a f t e r a l l , "... r a t h e r an i g n o r a n t m o l e c u l e t h a t f r e q u e n t l y g e t s out of hand and i s q u i t e c a p a b l e of g e n e r a t i n g a m u l t i t u d e of sequence arrangements" (Dover 1980). The c o n f o u n d i n g of c o r r e l a t i o n and c a u s a t i o n appears i n the c o n t e x t of genome s i z e p a t t e r n s i n the f a c t t h a t even f u n c t i o n -l e s s DNA might have some p h e n o t y p i c e f f e c t . " S i n c e the range of a d a p t i v e s t o r i e s i s as wide as our minds a r e f e r t i l e , new s t o r i e s can always be p o s t u l a t e d " (Gould and Lewontin 1979 i n D o o l i t t l e and Sa p i e n z a 1980). The DNA c o u l d be of a d a p t i v e v a l u e f o r a c e r t a i n s e l e c t i o n regime ( c a u s a t i o n ) , or merely be t o l e r a t e d by i t . I w i l l now c o n s i d e r p u b l i s h e d e x p l a n a t i o n s f o r p a t t e r n s i n genome s i z e . These e x p l a n a t i o n s a r e most e a s i l y t r e a t e d i n groups a c c o r d i n g t o the u n d e r l y i n g assumption about what the r o l e i s of the DNA t h a t i s d i f f e r e n t i a l l y d i s t r i b u t e d a c r o s s s p e c i e s so as t o produce the p a t t e r n s . TABLE 2 P a t t e r n s i n Genome s i z e r a d i o s e n s i t 1 v i t y v a r i e s d i r e c t l y w i th DNA content (Sparrow and Miksche 1961; Bowen 1962; Baetcke et a l . 1967; Underbrink et a l . 1968 ) r a d i a t i o n - i n d u c e d mutation r a t e s vary d i r e c t l y w i th DNA c o n t e n t (Sparrow et a l . 1968; Abrahamson et a l . 1973) p r o p o r t i o n of genome comprised of r e p e t i t i v e DNA i n c r e a s e s with genome s i z e (amphibians: Mizuno and MacGregor 1974; S t r a u s s 1971; c o n i f e r s : Miksche and H o t t a 1973; angiosperms: F l a v e l l et a l . 1974) C o n t r a r y e v i d e n c e : V i c i a :Chooi 1971b ) h i g h DNA c o n t e n t u s u a l l y i m p l i e s much h e t e r o c h r o m a t i n ( S t e b b i n s 1966) DNA/cell v a r i e s d i r e c t l y w i t h chromosome s i z e ( B a e t c k e et a l . 1967; Sparrow et a l . 1972) DNA c o n t e n t may or may not c o r r e l a t e w i th chromosome number (s e e Hinegardner 1976) DNA/cell v a r i e s d i r e c t l y w i t h n u c l e a r volume (Commoner 1964; Baetcke et a l . 1967; Sparrow et a l . 1972) DNA/cell v a r i e s d i r e c t l y w i th c e l l s i z e ( anima 1s:Commoner 1964; seed and pol1 en:Jones and Rees 1968, Bennett 1972. Bennett 1973, Jones and Brown 1976 ) a d u l t body s i z e i n c r e a s e s with DNA c o n t e n t ( m o l l u s c s : Hinegardner 1974a; Drosophi1 a :Endow and G a l l 1975; p o l y p l o i d p l a n t s ) m i t o t i c c y c l e time i n c r e a s e s w i t h DNA c o n t e n t (Van't Hof and Sparrow 1963; Yang and Dodson 1970; Evans and Rees 1971; Evans et a l . 1972) m e i o t i c c y c l e time i n c r e a s e s w i t h DNA c o n t e n t (Bennett 1971; and p o l y p l o i d y : Bennett and Smith 1972) i n b r e e d i n g / o u t b r e e d i n g t r e n d s a r e s i g n i f i c a n t 1n d i f f e r e n t d i r e c t i o n s i n d i f f e r e n t genera (see Rees and H a z a r i k a 1969) minimum g e n e r a t i o n time i n c r e a s e s with DNA content (Bennett 1972; Smith and Bennett 1975) T a b l e 2 (cont'd) 14. a n n u a l s have l e s s DNA than p e r e n n i a l s ( L a t h y r u s : Rees and H a z a r l k a 19G9; V1c1a : Chooi 1971; many p l a n t s : Bennett 1972; Ranunculus : Smith and Bennett 1975) 15. annuals have more DNA than p e r e n n i a l s ( L o l i u m :Jones and Rees 1967; Anthemideae :Nagl 1974; P h a l a r i s :Kadir 1974) 16. temperate p l a n t s have l a r g e r genomes than t r o p i c a l p l a n t s (Avdulov 1931; S t e b b i n s 1966; L e v i n and Funderberg 1979) 17. w i t h i n a group DNA i n c r e a s e s w i t h l a t i t u d e ( P i c e a s i tchens i s :Burley 1965. Miksche 1971; P1nus :Mergen and T h i e l g e s 1967) 18. c o a s t a l p o p u l a t i o n s have more DNA than i n l a n d p o p u l a t i o n s ( Pseudotsuga menziesi i :El-L-akany and S z l k l a i 1971) 19. deep sea f i s h e s have more DNA than t h e i r s h allow water r e l a t i v e s ( E b e l i n g e t a l . 1971) 20. p r i m i t i v e s p e c i e s have more DNA than new s p e c i e s ( S t e b b i n s 1966; Hinegardner 1976; La t h y r u s :Rees and H a z a r i k a 1967; C r e p i s :Jones and Brown 1976; Bachmann et a l . 1972) 21. g e n e r a l 1 s t s have more DNA than s p e c i a l i s t s ( p l a n t s : S t e b b i n s 1966; t e l e o s t s : Hinegardner 1968; amphibians: Bachmann e t a l . 1972; i n s e c t s : B i e r and M u l l e r 1969; mammals: Bachmann 1972; m o l l u s c s : H i n e g a r d n e r 1974a; echlnoderms: Hinegardner 1974b) 22. the d i s t r i b u t i o n of DNA cont e n t w i t h i n major groups 1s u s u a l l y a s y m m e t r i c a l l y d i s t r i b u t e d , skewed toward the h i g h end (Hinegardner 1976, and r e f s . t h e r e ) 23. f i s h f a m i l i e s w i t h s m a l l e r average genome s i z e a l s o have l e s s v a r i a t i o n i n genome s i z e ( Hinegardner and Rosen 1972). 24. average genome s i z e of a taxon 1s i n v e r s e l y r e l a t e d to the number of subtaxa (Bachmann e t a l . 1972; M l r s k y and R1s 1950; Hinegardner 1968; Goin and Goin 1968) 50 E x t r a DNA p l a y s no' r o l e i n phenotype I f 'excess' DNA has no e f f e c t on phenotype, then p a t t e r n s i n DNA amount c o u l d be e x p l a i n e d by p r o c e s s e s a c t i n g i n t e r n a l l y , w i t h i n the genome. S t o c h a s t i c p r o c e s s e s c o u l d generate random p a t t e r n s i n genome s i z e . T h i s would not e x p l a i n the many non-random p a t t e r n s r e p o r t e d . On the o t h e r hand, i t might be t h a t i n c r e a s e s and d e c r e a s e s i n amount of DNA are not e q u a l l y p r o b a b l e , i n which case an o r t h o g e n e t i c t r e n d would r e s u l t . H i n e g a r d n e r (1976), f o r example, l a b e l s groups as c a p a b l e or i n c a p a b l e of DNA i n c r e a s e , thus presuming a d i f f e r e n c e i n genome organ i z a t i o n . Means by which changes i n genome s i z e a r e brought about ( p o l y p l o i d i z a t i o n , unequal c r o s s i n g o v e r , i n s e r t i o n , d e l e t i o n , tandem d u p l i c a t i o n , changes i n chromosome number) are documented i n Ohno (1970). I t i s o b v i o u s t h a t these p r o c e s s e s cannot p r o c e e d w i t h o u t a t l e a s t o c c a s i o n a l l y a f f e c t i n g the v i a b i l i t y of an organism and t h e r e b y b e i n g s u b j e c t t o s e l e c t i o n at one l e v e l ( i n t e r n a l l y ) . So t r e n d s i n genome s i z e a r e a f f e c t e d not o n l y by the p r o b a b l e net d i r e c t i o n of change, but a l s o by p r o b a b l e v i a b i l i t y . I t does not seem u n r e a s o n a b l e , as an example, t h a t i n s e r t i o n s always have a lower p r o b a b i l i t y (than d e l e t i o n s ) of d i s r u p t i n g e s s e n t i a l t r a n s l a t i o n . T h i s would f a v o r genome i n c r e a s e over t i m e . H i n e g a r d n e r and Rosen (1972) c o n s i d e r the 'time h y p o t h e s i s ' t h a t genomes accumulate DNA over e v o l u t i o n a r y t i m e . T h i s c o u l d p o t e n t i a l l y e x p l a i n c e r t a i n p a t t e r n s such as p r i m i t i v e s p e c i e s h a v i n g more DNA than new s p e c i e s (#20) and g e n e r a l i s t s h a v i n g l a r g e r genomes than s p e c i a l i s t s (#21, g i v e n t h a t the d i r e c t i o n 51 of e v o l u t i o n i s toward s p e c i a l i z a t i o n ) but Hin e g a r d n e r and Rosen (1972) found no s i g n i f i c a n t c o r r e l a t i o n between the age of a taxon and i t s genome s i z e . R e g a r d l e s s of the e x i s t e n c e or non-e x i s t e n c e of a c o r r e l a t i o n t h i s h y p o t h e s i s has o t h e r s e r i o u s problems. How i s a genome r e s e t t o ' s m a l l ' at the ' s t a r t ' of a s p e c i e s ? I t i s d i f f i c u l t t o c a s t t h i s h y p o t h e s i s i n terms of mechanism r a t h e r than mere c o r r e l a t i o n . I t i s a v e r y d i f f e r e n t and more l i m i t e d i d e a , as Dover (1980) emphasizes, t h a t a s i g n i f i c a n t p r o p o r t i o n of 'junk' DNA be ' s e l f i s h ' i n t h a t i t s sequences promote the a c c u m u l a t i o n of l i k e sequences, a g a i n w i t h l i t t l e a f f e c t on the phenotype ( D o o l i t t l e and S a p i e n z a 1980; O r g e l and C r i c k 1980). S e l f i s h r e p l i c a t i o n i s another reason why DNA might i n c r e a s e over t i m e . At t h i s p o i n t i t seems i m p o s s i b l e t o proceed w i t h o u t a p p e a l i n g t o n a t u r a l s e l e c t i o n as a f a c t o r i n g e n e r a t i n g genome s i z e p a t t e r n s . S i n c e the p i o n e e r i n g work of M i r s k y and R i s (1951) i t has been a p p a r e n t t h a t genome s i z e has both i n c r e a s e d and d e c r e a s e d d u r i n g the cour s e of e v o l u t i o n . How can one e x p l a i n r e v e r s a l i n an o r t h o g e n e t i c t r e n d ? By a change i n genome o r g a n i z a t i o n ? For what reason? And what d e t e r m i n e s the l i m i t t o the a c c u m u l a t i o n of s e l f i s h DNA i n d i f f e r e n t s p e c i e s ? O b v i o u s l y t h e r e would have t o be l o g i s t i c a l l i m i t s t o the t o t a l amount of DNA a t some p o i n t . The proponents of s e l f i s h DNA invoke " m e t a b o l i c d i s a d v a n t a g e r e l a t i v e t o organisms w i t h l e s s s e l f i s h DNA" ( O r g e l and C r i c k 1980) and " e n e r g e t i c burden" and the d e s t r u c t i o n of needed sequences by s e l f i s h e l e m e n t s ( D o o l i t t l e and S a p i e n z a 1980) they a p p e a l t o s e l e c t i o n f o r c e s on the phenotype. No doubt 52 m e t a b o l i c c o s t s would e x i s t f o r junk as i t would f o r s e l f i s h DNA. In the end the c o n c e p t s of junk or s e l f i s h DNA can o n l y j u s t i f y the e x i s t e n c e of 'excess' DNA i n the genome, and c o n t r i b u t e n o t h i n g t o the e x p l a n a t i o n of p a t t e r n s i n genome s i z e a c r o s s s p e c i e s . The e x p l a n a t i o n of p a t t e r n s i n the p a r t i c u l a r amount of f u n c t i o n l e s s DNA, or the r a t i o of u s e l e s s to u s e f u l DNA ( O r g e l and C r i c k 1980) r e q u i r e s the e x p l a n a t i o n of the r e l a t i v e t o l e r a n c e s of v a r i o u s s e l e c t i o n regimes t o the consequences of i t s p r e s e n c e . "Intragenomic s e l e c t i o n i s c l e a r l y i m p o r t a n t f o r u n d e r s t a n d i n g e v o l u t i o n w i t h i n genomes and f o r u n d e r s t a n d i n g the s i g n i f i c a n c e of c e r t a i n DNA sequences, but i t does not i n i t s e l f c l a r i f y the e v o l u t i o n a r y f o r c e s d e t e r m i n i n g genome s i z e . . . " ( C a v a l i e r - S m i t h 1980b). E x t r a DNA has n u c l e o t y p i c e f f e c t s DNA c o u l d p l a y a r o l e i n t e r m e d i a t e between those of mere junk and of an a l p h a b e t i c code -- i t s b u l k a l o n e c o u l d d e t e r m i n e a s p e c t s of phenotype, independent of sequence. I f t h i s were the c a s e , s e l e c t i o n c o u l d a c t not o n l y i n f a v o u r of s m a l l e r genomes ( a g a i n s t the a c c u m u l a t i o n of junk or s e l f i s h DNA), but i n f a v o u r of l a r g e r genomes under c o n d i t i o n s where a g r e a t e r q u a n t i t y of DNA produces a phenotype w i t h a s e l e c t i v e advantage. Bennett (1971) c a l l e d t h i s a ' n u c l e o t y p i c ' e f f e c t , and the s e t of t r a i t s r e s u l t i n g from such sequence-independent e f f e c t s the ' n u c l e o t y p e ' . "The n u c l e o t y p e i s t h e r e f o r e a g e n o t y p i c , but not a genie c h a r a c t e r " (Bennett 1981). The i d e a of n u c l e o t y p e a p p e a l e d t o C a v a l i e r - S m i t h (1978,1980a, 1980b) who expounds a ' n u c l e o t y p i c t h e o r y ' . He 53 (1978) proposes two f u n c t i o n s of DNA o t h e r than those d i r e c t l y or i n d i r e c t l y i n v o l v e d i n c o d i n g f o r p r o t e i n s : 1. c o n t r o l of c e l l volume, and 2. d e t e r m i n a t i o n of n u c l e a r volume. F u n c t i o n (1) i s d e t e r m i n e d by the number of r e p l i c o n o r i g i n s i n the genome. (A r e p l i c o n i s a u n i t of DNA r e p l i c a t i o n . ) C a v a l i e r - S m i t h (1978) r e f e r s t o models (Sompyrac and Maaloe 1973; Donachie 1974) t h a t p o s t u l a t e the a c c u m u l a t i o n of an i n i t i a t o r , or the d i l u t i o n by c e l l growth of a r e p r e s s o r , s p e c i f i c f o r r e p l i c o n o r i g i n s . When the c o n c e n t r a t i o n of the i n i t i a t o r / r e p r e s s o r a t t a i n s a p a r t i c u l a r c o n c e n t r a t i o n r e p l i c a t i o n i s i n i t i a t e d (or ceased t o be r e p r e s s e d ) and the c e l l d i v i d e s . Thus maximum c e l l s i z e i s d e t e r m i n e d . C a v a l i e r - S m i t h (1978) assumes t h a t the volume of the n u c l e u s i s d e t e r m i n e d by the bulk of i t s c o n t e n t s . He f e e l s t h a t t h i s may be i m p o r t a n t because i t t h e r e b y d e t e r m i n e s n u c l e a r s u r f a c e a r e a (and pore number) w i t h a consequent e f f e c t on n u c l e o c y t o p l a s m i c t r a n s p o r t of RNA and, t h e r e f o r e , 'growth r a t e ' . C a v a l i e r - S m i t h a t t e m p t s t o a p p l y t h e s e non-genic f u n c t i o n s t o the e x p l a n a t i o n of genome s i z e p a t t e r n s (and the r e s o l u t i o n of the C-value paradox) by l i n k i n g up w i t h some i d e a s about r -and K - s e l e c t i o n t h e o r y : " The g r e a t d i v e r s i t y of c e l l volumes and growth r a t e s , and t h e r e f o r e of DNA c o n t e n t s , among e u k a r y o t e s r e s u l t s from a v a r y i n g b a l a n c e i n d i f f e r e n t s p e c i e s between r - s e l e c t i o n , which f a v o u r s s m a l l c e l l s and r a p i d growth r a t e s and t h e r e f o r e low DNA C - v a l u e s , and K - s e l e c t i o n which f a v o u r s 54 l a r g e c e l l s and slow growth r a t e s and t h e r e f o r e h i g h DNA C-v a l u e s . " ( C a v a l i e r - S m i t h 1978). The l i n k between K - s e l e c t i o n and l a r g e c e i l s and slow growth i s never e x p l a i n e d by him. But i n any c a s e , g i v e n s e l e c t i o n f o r l a r g e r c e l l s i z e , "Though t h e r e are undoubtedly s e v e r a l ways of e v o l v i n g l a r g e r c e l l s , a s i m p l e and d i r e c t way would be by i n c r e a s i n g the number of r e p l i c o n o r i g i n s i n v o l v e d i n the volume-dependent c o n t r o l of DNA r e p l i c a t i o n . " ( C a v a l i e r - S m i t h 1980b). But i n the next sentence he p o i n t s out t h a t " T h i s cannot p r o v i d e the fundamental e x p l a n a t i o n of the C-value paradox, s i n c e i t does not n e c e s s i t a t e a l a r g e r genome (as i t i n v o l v e s o n l y a s m a l l f r a c t i o n of the genome)..." So where i s the l i n k between s e l e c t i o n and C-value? "On t h i s t h e o r y i t i s - the e x t r a r e p l i c o n o r i g i n s not the l a r g e r n u c l e u s , or the l a r g e r genome as such, which i n c r e a s e s c e l l s i z e : what the C-value c o n t r o l s more d i r e c t l y i s n u c l e a r volume." ( C a v a l i e r - S m i t h 1980b) So l e t us look a t the c a u s a l c h a i n between s e l e c t i o n and the second proposed f u n c t i o n of DNA, t h a t of d e t e r m i n a t i o n of n u c l e a r volume. "... l a r g e r c e l l s r e q u i r e more rRNA t r a n s p o r t t o the c y t o p l a s m per c e l l c y c l e than do s m a l l e r c e l l s . One would t h e r e f o r e expect s e l e c t i o n t o i n c r e a s e the r a t e of RNA t r a n s p o r t i n l a r g e r c e l l s , l e s t i t become r a t e l i m i t i n g t o c e l l growth and unduly l e n g t h e n the c e l l c y c l e . T h i s c o u l d be done by i n c r e a s i n g the amount of s k e l e t a l DNA (S-DNA) so as t o i n c r e a s e the n u c l e a r s u r f a c e area and the number of n u c l e a r p o r e s . The s u g g e s t i o n i s t h e r e f o r e t h a t the excess DNA i s used, n o t , as has been i n c o r r e c t l y s t a t e d , t o slow 55 development but r a t h e r to p r e v e n t the e x c e s s i v e s l o w i n g of development which would o t h e r w i s e be caused by l a r g e i n c r e a s e s i n c e l l s i z e . " ( C a v a l i e r - S m i t h 1980b) In o t h e r words i t i s s e l e c t i o n f o r s h o r t e r c e l l c y c l e time t h a t f a v o u r s i n c r e a s e d C - v a l u e . At t h i s p o i n t i t i s apparent t h a t "K-s e l e c t i o n f o r l a r g e c e l l s and slow growth" has no e f f e c t on C-v a l u e . C e l l volume can be i n c r e a s e d by i n c r e a s i n g the number of r e p l i c o n o r i g i n s w i t h l i t t l e e f f e c t on C - v a l u e , and l a r g e C-v a l u e s i n l a r g e c e l l s are r e a l l y due t o r - s e l e c t i o n t o p r e v e n t e x c e s s i v e l e n g t h e n i n g of c e l l c y c l e t i m e . "... what s h o u l d never o c c u r on my t h e o r y -- and has not been o b s e r v e d -- i s t h a t h i g h C -value organisms have s m a l l c e l l s and s h o r t l i f e c y c l e s . " Why not? A l a r g e genome (and h i g h r a t e of RNA' t r a n s p o r t ) w i t h few r e p l i c o n o r i g i n s would f u l f i l l the r e q u i r e m e n t s g i v e n the two n o n - p r o t e i n c o d i n g f u n c t i o n s g i v e n a t the o u t s e t . A f i n a l c a u t i o n i s t h a t the DNA f u n c t i o n s proposed by C a v a l i e r - S m i t h are not e n t i r e l y sequence-independent. R e p l i c o n o r i g i n s are presumably p a r t i c u l a r sequences, and one r o l e of s t r u c t u r a l DNA i s t o code f o r s t r u c t u r a l RNA. C a v a l i e r - S m i t h p r e s e n t s us w i t h s e v e r a l new i d e a s b u t , as I have shown, they a r e not s u f f i c i e n t t o form a ' n u c l e o t y p i c t h e o r y ' . At p r e s e n t a l l t h a t e x i s t s i s the s u g g e s t i o n t h a t DNA q u a n t i t y may have a sequence-independent ( n u c l e o t y p i c ) r o l e ( B ennett 1971). 56 DNA d i f f e r e n c e s a r e i n amount of pr imary DNA Another s e l e c t i o n i s t h y p o t h e s i s of g r e a t p o t e n t i a l g e n e r a l i t y i n e x p l a i n i n g genome s i z e p a t t e r n s i s what I s h a l l c a l l the ' l o s s - o f - p a r t s ' h y p o t h e s i s advanced by Hine g a r d n e r (1968,1976; H i n e g a r d n e r and Rosen 1972). The main components of t h i s h y p o t h e s i s a re as f o l l o w s : 1. Some groups of organisms can i n c r e a s e t h e i r genome s i z e , w h i l e o t h e r s c a n n o t , or do n o t . 2. In groups t h a t do not i n c r e a s e t h e i r DNA "The consequence of DNA change and l o s s i s e v o l u t i o n toward s p e c i a l i z a t i o n and e v e n t u a l e x t i n c t i o n . " ( H i n e g a r d n e r 1976) 3. S p e c i a l i z a t i o n i n v o l v e s l o s s of p a r t s and/or f u n c t i o n s . "A s p e c i a l i z e d f i s h would be ex p e c t e d t o have fewer p a r t s , s i n c e the d e r i v a t i v e c o n d i t i o n of s p e c i a l i z a t i o n i s the a d a p t a t i o n t o a r e s t r i c t e d mode of l i f e not r e q u i r i n g the use of a l l s t r u c t u r e s p r e s e n t i n the g e n e r a l i z e d form. Though i t would be p o s s i b l e t o q u a n t i t a t e f i s h p a r t s , i t i s h a r d l y n e c e s s a r y ; even the g r o s s p i c t u r e one g e t s from examining f i s h anatomy shows t h a t the g e n e r a l i z e d f i s h e s have more p a r t s . They tend t o have more s e p a r a t e elements i n the h y o i d a p p a r a t u s and g i l l a r c h e s , more v e r t e b r a e , i n t e r m u s c u l a r bones, s k u l l bones, and f i n r a y s . C e r t a i n l y the t r e n d i s not i n the o p p o s i t e d i r e c t i o n . " (Hinegardner and Rosen 1972) 4. DNA c o d i n g f o r the l o s t t r a i t s can be l o s t , and i s . There a r e s e v e r a l d i f f i c u l t i e s w i t h t h i s e x p l a n a t i o n of genome s i z e p a t t e r n s . One i s the p o s t u l a t i o n of o r t h o g e n e t i c t r e n d s , t h a t some groups can and o t h e r s cannot i n c r e a s e t h e i r 57 DNA. No reason f o r these t r e n d s i s g i v e n . Another d i f f i c u l t y i s the i n t e r e s t i n g q u e s t i o n of whether the d i r e c t i o n of e v o l u t i o n i s toward s p e c i a l i z a t i o n . The d e f i n i t i o n s of g e n e r a l i z e d and s p e c i a l i z e d were as f o l l o w s : " G e n e r a l i z e d w i l l be used t o d e s c r i b e organisms t h a t share numerous f e a t u r e s w i t h o t h e r members of t h e i r t a x o n . In c o n t r a s t , a s p e c i a l i z e d organism shares fewer f e a t u r e s w i t h the members of i t s taxon and w i l l d i f f e r from them i n presence or absence of c e r t a i n f e a t u r e s . " (Hinegardner 1976) These d e f i n i t i o n s imply t h a t e v o l u t i o n w i l l be i n the d i r e c t i o n of s p e c i a l i z a t i o n , making the s t a t e d t r e n d t a u t o l o g i c a l . E v o l u t i o n i s change, and i f change means g a i n or l o s s of c h a r a c t e r i s t i c s i t w i l l imply s p e c i a l i z a t i o n by the above d e f i n i t i o n ( u n l e s s a l l subtaxa change i n the same way so t h a t t h e r e i s no d i v e r s i f i c a t i o n ) . A t h i r d problem i s the c o n n e c t i o n between s p e c i a l i z a t i o n and the l o s s of DNA. Some modes of s p e c i a l i z a t i o n would seem not t o r e q u i r e fewer p a r t s and f u n c t i o n s . V i v i p a r i t y , f o r example, i s viewed (Hinegardner and Rosen 1972) as a p a r t i c u l a r form of s p e c i a l i z a t i o n w i t h i n the Atherinomorpha ( T e l e o s t e i ) , a l t h o u g h i t i s not an o b v i o u s s i m p l i f i c a t i o n of o v i p a r i t y . A l s o , some a u t h o r s (e.g. V a l e n t i n e 1976) assume t h a t the more p r e c i s e m e t a b o l i c r e q u i r e m e n t s of s p e c i a l i s t s r e q u i r e more c o p i e s of an enzyme l o c u s . At any r a t e , the mechanism by which unused DNA i s l o s t i s never e x p l a i n e d . And why a r e DNA i n c r e a s e s not l o s t f o r the same reason t h a t DNA t h a t has f a l l e n i n t o d i s u s e i s l o s t ? H i n e g a r dner(1976) d i s t i n g u i s h e s two t y p e s of DNA i n 58 organisms. "There are the s e l e c t i v e l y c o n s t r a i n e d sequences. These are the ones t h a t a f f e c t e v e n t s i n the o r g a n i s m s , and i n c l u d e genes and t h e i r c o n t r o l . T h i s w i l l be c a l l e d p r i m a r y DNA. Then t h e r e are the much l e s s c o n s t r a i n e d sequences produced by d u p l i c a t i o n ; t h i s i s the secondary DNA. A f u z z y area undoubtedly l i e s between the two; however, the two t y p e s are p r o b a b l y b i g g e r than the o v e r l a p and can be examined as two p o p u l a t i o n s of n u c l e o t i d e sequences." ( H i n e g a r d n e r 1976) Why i s secondary DNA r e t a i n e d i f t h e r e i s s e l e c t i o n c a p a b l e of removing a p i e c e of p r i m a r y DNA f a l l e n i n t o d i s u s e ? The most s e r i o u s problem w i t h the l o s s - o f - p a r t s h y p o t h e s i s i s t h a t i t i s o n l y r e l e v a n t t o p r i m a r y DNA, "the s e l e c t i v e l y c o n s t r a i n e d sequences", and f o r a few reasons i t i s l i k e l y t h a t p r i m a r y DNA i s a r e l a t i v e l y unimportant p a r t of genome s i z e d i f f e r e n c e s . These reasons a r e : 1. P r i m a r y DNA, a c c o r d i n g t o most e s t i m a t e s , c o m p r i s e s o n l y a s m a l l p r o p o r t i o n of the genome. H i n e g a r d n e r (1976) c o n s i d e r s t h i s and c o n c l u d e s t h a t "At the maximum t h e n , i n our average organism p r i m a r y DNA a c c o u n t s f o r 0.6 t o 24 p e r c e n t of the h a p l o i d DNA." I f p r i m a r y DNA i s a s m a l l p r o p o r t i o n then s e l e c t i o n - d e t e r m i n e d changes i n i t are l i k e l y t o be swamped by changes i n the amount of secondary DNA, u n l e s s the q u a n t i t y of secondary DNA i s v e r y s t a b l e . But . i n secondary DNA "Changes or l o s s e s would be more r a p i d than i n the p r i m a r y DNA." ( H i n e g a r d n e r 1976, p.195) 59 Ta b l e 3. The range i n genome s i z e i n t e l e o s t t a x a as a p r o p o r t i o n of the minimum and maximum genome measured i n each t a x o n . The minimum (or maximum) genome s i z e can be viewed as a generous o v e r - e s t i m a t e of the p r i m a r y DNA f o r the group. C a l c u l a t e d from the d a t a of H i n e g a r d n e r and Rosen (1972). DNA (pg) — Range % of % of # of Teleost Taxon min. max. min. max. spp. Osteoglossomorpha .77 1.3 69 41 8 Osteoglossiformes .77 1.3 69 41 4 Osteoglossoidei .77 1.0 30 23 3 Mormyriformes 1.0 1.2 20 17 4 Elopomorpha 1.2 2.5 108 52 4 Anguilliformes 1.4 2.5 79 44 3 Clupeomorpha .77 1.9 147 59 6 Protacanthopterygii 2.7 3.3 22 18 3 Ostariophysi .65 4.4 577 85 75 Cypriniformes .65 2.2 238 70 43 Characoidei .71 2.1 196 66 22 Cyprinoidei .65 2.2 238 70 21 Silu r i f o r m e s .88 4.4 400 80 32 Ca l l i c h t h y i d a e 1.7 4.4 159 61 8 Scolpelomorpha 1.2 1.2 0 0 2 Paracanthopterygii .68 3.0 341 77 12 Gadiformes .68 .98 44 31 5 Batrachoidiformes 1.7 3.0 76 43 4 Lophiiformes .74 1 35 26 3 Acanthopterygii .48 2.1 338 77 168 Atherinomorpha .72 1.6 122 55 19 Exocoetoidei .74 1.2 62 38 5 Cyprinodontoidei .72 1.6 122 55 11 At h e r i n o i d e i 1.1 1.3 18 15 3 Percomorpha .48 2.1 338 77 149 Gasterosteiformes .58 .70 21 17 6 Gasterosteoidae .58 .70 21 17 3 Syngnathoidei .64 .66 3 3 3 Scorpaeniformes .76 1.4 84 46 15 Scorpaenoidei .96 1.4 46 31 4 Hexagrammoidei .79 .99 25 20 5 C o t t o i d e i .76 1.1 45 31 6 Perc iformes .59 . 2.1 256 72 104 Percoidei .72 1.4 94 49 68 Sphyraenoidei .83 1.2 45 31 2 Labroidei .91 2.1 131 57 5 Bl e n n i o i d e i .81 1 23 19 6 Gobioidei 1.2 1.4 17 14 3 Scombroi dei .88 1.1 25 20 7 Stromateoidei .80 .81 1 1 2 Anabantoidei .59 .88 49 33 9 Pleuronectiformes .65 1.1 69 41 12 Pleuronectoidei .65 1 54 35 10 Soleo i d e i .65 1.1 69 41 2 Tetraodontiformes .48 1.1 129 56 10 B a l i s t o i d e i .64 1.1 72 42 5 Tetraodontoidei .48 .90 131 57 5 60 2. I f the d i f f e r e n c e s i n genome s i z e l i e i n p r i m a r y DNA then d i f f e r e n c e s i n genome s i z e between r e l a t e d s p e c i e s must be l e s s than the e n t i r e amount (most l i k e l y a s m a l l f r a c t i o n ) of p r i m a r y DNA i n the g e n e r a l i z e d s p e c i e s . T a b l e 3 i s d e r i v e d from the d a t a of H i n e g a r d n e r and Rosen 1972 and shows the range i n genome s i z e w i t h i n t e l e o s t t a x a as a p e r c e n t a g e of both the minimum and maximum genome w i t h i n a g i v e n t a x o n . The ranges are g e n e r a l l y much g r e a t e r than a f r a c t i o n of a very generous e s t i m a t e of the amount of p r i m a r y DNA (e.g. H i n e g a r d n e r ' s e s t i m a t e was 24% and the range i s o f t e n g r e a t e r than 2 4 % ) . T h i s i s reason to b e l i e v e t h a t at l e a s t some, i f not a l l , of the d i f f e r e n c e s i n genome s i z e a r e due t o v a r y i n g amounts of secondary DNA. The l o s s - o f - p a r t s h y p o t h e s i s seems u n i m p o r t a n t , • i f not i m p l a u s i b l e . DNA v a r i a t i o n i s d i f f e r e n t i a l redundancy f o r gene dosage e f f e c t s I t i s o f t e n s p e c u l a t e d t h a t the c a u s a l f a c t o r i n the p o s i t i v e c o r r e l a t i o n between genome s i z e and l a t i t u d e (#16,#17) i s t e m p e r a t u r e , and t h a t has l e d t o the s u g g e s t i o n t h a t more DNA i s a d a p t i v e i n c o o l e r e n v i r o n m e n t s . "... One way t o i n c r e a s e p r o t e i n p r o d u c t i o n i s t o i n c r e a s e the number of gene c o p i e s . S i n c e enzyme a c t i v i t y has a s t r o n g dependence on temperature ( a p p r o x i m a t e l y d o u b l i n g w i t h each 10°C. r i s e up t o an optimum) i t c o u l d be one l i m i t i n g f a c t o r w i t h r e s p e c t t o e f f i c i e n t growth a t low t e m p e r a t u r e s i n p l a n t s and c o l d - b l o o d e d a n i m a l s . Then, any 61 organisms h a v i n g d u p l i c a t i o n s of r a t e - l i m i t i n g genes would have an immediate s e l e c t i v e advantage..." (Sparrow et a l . 1972) . S t e b b i n s ( 1 9 6 6 ) and o t h e r s have c a u t i o n e d t h a t h i g h DNA c o n t e n t i s p r o b a b l y not d i r e c t l y a d a p t i v e t o low te m p e r a t u r e s s i n c e a few s t r i c t l y t r o p i c a l ( p l a n t ) groups have a h i g h DNA c o n t e n t . S t e b b i n s suggested t h a t gene redundancy governs the r a t e of development, which g e n e r a l l y has t o be sl o w e r a t c o o l e r l a t i t u d e s . He (1966) proposed a model i n which gene m u l t i p l e s a r e o r g a n i z e d i n a t i m e - c h a i n , one copy a c t i v e a t a t i m e , so t h a t the d u r a t i o n of a stage i n development i s s e t by the l e n g t h of the c h a i n of c o p i e s . Grime and Mowforth (1982) proposed a d i f f e r e n t model t o r e l a t e DNA c o n t e n t and t e m p e r a t u r e . The id e a i s t h a t t h e r e can be a s t r a t e g y of s e p a r a t i o n i n time of c e l l e x p a n s i o n and c e l l d i v i s i o n . They c i t e e v i d e n c e t h a t m i t o s i s i s i n h i b i t e d a t (low) te m p e r a t u r e s t h a t s t i l l p e r m i t h i g h r a t e s of c e l l e x p a n s i o n , and show t h a t shoot e x p a n s i o n a t lower t e m p e r a t u r e s means h i g h e r DNA c o n t e n t ( i n B r i t i s h f l o r a ) . P l a n t s which grow i n c o n t i n u a l l y warm c l i m a t e s , or o n l y i n the warm season of v a r i a b l e c l i m a t e s , have s m a l l genomes. The a s s o c i a t i o n of f a s t c e l l e x p a n s i o n w i t h l a r g e genome c o u l d be due t o dosage r e p e t i t i o n r e q u i r e m e n t s , or t o the need f o r a l a r g e n u c l e a r envelope (see n u c l e o t y p i c e f f e c t s ) . Grime and Mowforth (1982) suggest t h a t t emperature c o u l d i n f l u e n c e genome s i z e i n a n i m a l s , t o o . "As might be e x p e c t e d , s m a l l genomes a r e c h a r a c t e r i s t i c of warm-blooded a n i m a l s and i t i s p a r t i c u l a r l y i n t e r e s t i n g 62 t h a t r e p t i l e s which f l o u r i s h i n dry hot c o n d i t i o n s have u n i f o r m l y s m a l l genomes whereas amphibia i n c l u d e s p e c i e s w i t h e x c e p t i o n a l l y l a r g e genomes and c e l l s . The r e s p i r a t o r y system of amphibians depends on the maintenance of a m oist permeable s k i n , so the e c o l o g y and b e h a v i o r of most s p e c i e s i n v o l v e the a v o i d a n c e of i n s o l a t i o n and maintenance of low body te m p e r a t u r e . " E x t r a DNA i n f l u e n c e s a d a p t a b i 1 i t y A l l of the proposed f u n c t i o n s f o r the ' e x t r a ' DNA up t o t h i s p o i n t have c e n t e r e d around 'adaptedness', or s u i t i n g the p r o p e r t i e s of organisms t o c o n d i t i o n s e x i s t i n g i n t h e i r e n v i r o n m e n t s . I t i s a d i f f e r e n t i d e a t h a t the DNA be i m p o r t a n t f o r ' a d a p t a b i l i t y ' . There are s e v e r a l s u g g e s t i o n s of t h i s type'. Ohno (1970) s t r e s s e s the importance of e x t r a , or redundant DNA as e x p e r i m e n t a l m a t e r i a l i n which to t e s t new genes w i t h o u t s u f f e r i n g the l o s s of p r e v i o u s l y e x i s t i n g , and needed, genes. And t h e r e i s e v i d e n c e to show t h a t s e v e r a l genes have e v o l v e d by gene d u p l i c a t i o n . Whereas Ohno was p r i m a r i l y concerned w i t h s t r u c t u r a l genes, B r i t t e n and Davidson (1971) s t r e s s the importance of h a v i n g redundant DNA i n o r d e r t o e v o l v e new gene r e g u l a t i o n systems, and t r i e d t o e x p l a i n the e x i s t e n c e of r e p e t i t i v e DNA i n t h i s manner. I n t r o n s ( i n t r a g e n i c r e g i o n s ) a r e p o r t i o n s of the genome t h a t are t r a n s c r i b e d , but s p l i c e d out of RNA b e f o r e t r a n s l a t i o n . G i l b e r t (1978) suggested t h a t i n t r o n s serve t o i n c r e a s e the r a t e of e v o l u t i o n : 63 1. l a r g e s c a l e changes c o u l d be caused by a m u t a t i o n t h a t a l t e r e d a s p l i c i n g p a t t e r n 2. they c o u l d i n c r e a s e the frequency of r e c o m b i n a t i o n between p a r t s of a s i n g l e gene. R e p e t i t i v e DNA c o u l d a l s o be i m p o r t a n t through the s p a c i n g out of genes i n complex organisms t o f a c i l i t a t e r e c o m b i n a t i o n . On the o t h e r hand, e x t r a DNA might r e t a r d e v o l u t i o n . "... the f a i l u r e of the p o l y p l o i d s t o e v o l v e new c h a r a c t e r i s t i c s can best be a s c r i b e d t o the r e t a r d a t i o n of e v o l u t i o n a r y p r o g r e s s which r e s u l t s from the presence of many d u p l i c a t e d gene l o c i . " ( S t e b b i n s 1966) DISCUSSION The e x i s t e n c e of the C-value paradox i s e v i d e n c e t h a t much i s t o be l e a r n e d about the s t r u c t u r e and f u n c t i o n of the genome. There i s much more DNA i n c e l l s than i s r e q u i r e d t o code f o r p r o t e i n s , and i f the remainder p l a y s a r o l e i n r e g u l a t i o n , why can c o n g e n e r i c s p e c i e s , w i t h a p p a r e n t l y s i m i l a r r e q u i r e m e n t s , d i f f e r so much i n DNA c o n t e n t ? What e l s e c o u l d the DNA be d o i n g t h e r e ? There a r e many non-random c o r r e l a t i o n s of genome s i z e w i t h p h y s i o l o g i c a l , e c o l o g i c a l , and taxonomic parameters (see Table 2 ) . These a r e c l u e s t o the r o l e of the d i f f e r e n t i a l l y d i s t r i b u t e d DNA. S i n c e many of the p a t t e r n s a r e d i f f i c u l t t o e x p l a i n w i t h e x i s t i n g models of the genome, the d i f f e r e n t i a l l y d i s t r i b u t e d DNA c o u l d be the same as the ' e x t r a ' DNA, l i n k i n g the two a s p e c t s of the paradox. 64 I have reviewed the e x p l a n a t i o n s of p a t t e r n s i n genome s i z e , t r e a t i n g them a c c o r d i n g t o t h e u n d e r l y i n g assumption of what the e x t r a DNA i s . Many of these e x p l a n a t i o n s 'make sense', and t h i s i s at l e a s t a reminder, i f not an i n d i c a t i o n , t h a t t h e r e c o u l d be m u l t i p l e causes u n d e r l y i n g the p a t t e r n s o b s e r v e d . F u r t h e r m o r e , many of the e x p l a n a t i o n s a re not m u t u a l l y e x c l u s i v e . As an i l l u s t r a t i o n c o n s i d e r the number of e x p l a n a t i o n s t h a t can be brought t o bear on the a n n u a l / p e r e n n i a l p a t t e r n (#14, Tab l e 2 ) . Annuals g e n e r a l l y have l e s s DNA than p e r e n n i a l s . One c o u l d assume t h a t the d i f f e r e n c e l i e s i n r e g u l a t o r y DNA, and argue t h a t p e r e n n i a l s have a g r e a t e r r e g u l a t o r y r e q u i r e m e n t because they a r e l o n g e r l i v e d and t h e r e f o r e must cont e n d w i t h a more v a r i a b l e environment d u r i n g t h e i r l i f e c y c l e s . Or one c o u l d assume t h a t the DNA d i f f e r e n c e was due t o 'junk' or ' s e l f i s h ' DNA, and t h a t the m e t a b o l i c c o s t of i t were g r e a t e r i n a s p e c i e s w i t h f a s t development and a s h o r t l i f e c y c l e , so t h e r e i s s t r o n g e r s e l e c t i o n a g a i n s t u s e l e s s DNA i n a n n u a l s p e c i e s . Another a l t e r n a t i v e i s t h a t the DNA e f f e c t s a r e n u c l e o t y p i c (sequence-independent) and a n n u a l s have l e s s DNA because they need a s h o r t e r minimum g e n e r a t i o n time ( f a s t e r m i t o s i s and m e i o s i s ) , or ( f o r some reason) s m a l l e r c e l l s . H i n e g a r d n e r might suggest t h a t a n n u a l s a r e s p e c i a l i z e d , u s u a l l y s i m p l e r and w i t h fewer ' p a r t s ' , and t h e r e f o r e r e q u i r e l e s s DNA. Grime and Mowforth (1982) would l o o k t o see i f the growth p e r i o d f o r a n n u a l s was c o n f i n e d t o the warm p a r t of the season, when e x t r a DNA would not be r e q u i r e d f o r f a s t c e l l e x p a n s i o n t e m p o r a l l y s e p a r a t e d from m i t o s i s . Someone e l s e might p o i n t out t h a t 65 a d a p t a b i l i t y might be more i m p o r t a n t f o r p e r e n n i a l s , and t h a t the a d d i t i o n a l DNA they c o n t a i n c o u l d be to t h a t end. C a r e f u l e x p e r i m e n t s c o u l d d i s t i n g u i s h among some of these a l t e r n a t e h y p o theses, but s e v e r a l would be q u i t e d i f f i c u l t t o f a l s i f y . There a r e two c o n c e i v a b l e ways i n which t h i s paradox might be s o l v e d . One i s t h a t a f u n c t i o n be found f o r the e x t r a DNA, and t h a t t h i s new u n d e r s t a n d i n g make us r e a l i z e why the v a r i o u s t r e n d s e x i s t — what t h e i r 'common denominator' i s . The second i s the p o s s i b i l i t y of n o t i c i n g such a 'common denominator', a grand c o r r e l a t i o n t h a t accommodates a l l of the p a t t e r n s found, and e x p l o r i n g the r e a l i t y of mechanisms ( w i t h assumed r o l e s of DNA) t h a t c o u l d p l a u s i b l y g e n erate the p a t t e r n s . Genome S i z e and Rates of E v o l u t i o n The grand c o r r e l a t i o n 'the f a s t e r the r a t e of e v o l u t i o n , the s m a l l e r the genome s i z e ' c o u l d be argued t o f i t a l l p a t t e r n s . A n c i e n t or ' l i v i n g f o s s i l ' s p e c i e s a re r e c o g n i z e d as such because t h e i r r a t e of change has been very slow f o r a l o n g time -- and they have l a r g e r genomes. Most people would agree t h a t s p e c i a l i s t s a r e i n more of a 'Red Queen' s i t u a t i o n than g e n e r a l i s t s . B i o t i c ( e v o l v i n g ) f a c t o r s p l a y a g r e a t e r r o l e i n d e f i n i n g s p e c i a l i s t s ' s n i c h e s , and they more o f t e n f i n d t hemselves i n c o e v o l u t i o n a r y 'arms r a c e s ' . S p e c i a l i s t s have s m a l l e r genomes than g e n e r a l i s t s (#21). The environment of d i s p e r s i n g a n n u a l s c o u l d g e n e r a l l y d i f f e r more from g e n e r a t i o n t o g e n e r a t i o n than i t does f o r p e r e n n i a l s , e x p o s i n g them more o f t e n t o d i r e c t i o n a l s e l e c t i o n . That the average genome s i z e of a taxon i s i n v e r s e l y r e l a t e d t o the number of subtaxa (#24), 66 temperate genomes be b i g g e r than t r o p i c a l ones (#16), and deep sea f i s h e s have more DNA than t h e i r s h a l l o w water r e l a t i v e s (#19), are a l l f a i r l y e a s i l y c a s t i n ' r a t e of e v o l u t i o n ' terms. A New E x p l a n a t i o n f o r Genome S i z e P a t t e r n s C o r r e l a t i o n does not imply c a u s a t i o n . What mechanism might e x p l a i n t h i s grand c o r r e l a t i o n ? E v o l u t i o n i s change i n the g e n e t i c c o n s t i t u t i o n of a p o p u l a t i o n . From a Neo-Darwinian p e r s p e c t i v e t h i s i m p l i e s the a c t i o n of e i t h e r d i r e c t i o n a l or d i s r u p t i v e s e l e c t i o n . So the problem becomes how these modes of s e l e c t i o n can i n f l u e n c e genome s i z e . I h y p o t h e s i z e t h a t the answer l i e s i n the o b s e r v a t i o n t h a t both of these e v o l u t i o n -c a u s i n g modes of s e l e c t i o n f a v o r p h e n o t y p i c v a r i a n t s i n the p o p u l a t i o n . T h i s means t h a t genome s i z e or any o t h e r c h a r a c t e r i s t i c t h a t i s non-randomly d i s t r i b u t e d among p h e n o t y p i c c o n s e r v a t i v e s and v a r i a n t s i n the p o p u l a t i o n w i l l be i n d i r e c t l y i n f l u e n c e d by d i r e c t i o n a l or d i s r u p t i v e s e l e c t i o n a c t i n g on phenotype. T h i s non-random d i s t r i b u t i o n can come about by a s s o c i a t i o n of the c h a r a c t e r i s t i c w i t h r a t e of p r o d u c t i o n of p h e n o t y p i c v a r i a n t s . I f , f o r example, s m a l l e r genomes produce v a r i a n t s a t a g r e a t e r r a t e , then on average p h e n o t y p i c v a r i a n t s w i l l have s m a l l e r genomes and s e l e c t i o n f o r v a r i a n t s w i l l i n d i r e c t l y s e l e c t f o r s m a l l e r genomes. S t a b i l i z i n g s e l e c t i o n would f a v o r l a r g e r genomes. In t h i s manner r a t e of e v o l u t i o n can be c o r r e l a t e d w i t h genome s i z e . S t a t e d more p r e c i s e l y , my new h y p o t h e s i s i s : 67 1. The f u n c t i o n of the 'mystery' DNA r e s p o n s i b l e f o r most genome s i z e p a t t e r n s i s r e g u l a t i o n of v a r i a t i o n p r o d u c t i o n ; more DNA means sl o w e r p r o d u c t i o n of a d d i t i v e g e n e t i c v a r i a t i o n . 2. Secondary s e l e c t i o n (Chapter Two) can a c t v i a p h e n o t y p i c v a r i a t i o n t o i n f l u e n c e DNA amount, g i v e n ( 1 ) . 3. D i r e c t i o n a l s e l e c t i o n i n d i r e c t l y f a v o r s g r e a t e r p r o d u c t i o n of g e n e t i c v a r i a t i o n , and s m a l l e r genome s i z e . Support f o r t h e Genome S i z e / V a r i a t i o n P r o d u c t i o n H y p o t h e s i s U n f o r t u n a t e l y the h y p o t h e s i z e d l i n k between genome s i z e and r a t e s of a d d i t i v e g e n e t i c v a r i a t i o n p r o d u c t i o n has yet t o be e s t a b l i s h e d . There i s o n l y c i r c u m s t a n t i a l e v i d e n c e i n the l i t e r a t u r e . P i e r c e and M i t t o n (1980) r e p o r t e d a s t r o n g n e g a t i v e r e l a t i o n s h i p , i n the s p e c i e s they examined, between genome s i z e and g e n e t i c v a r i a t i o n as measured by average h e t e r o z y g o s i t y (H) and p e r c e n t of p o l y m o r p h i c l o c i ( P ) . T h e i r work does not c o n s t i t u t e e v i d e n c e s u p p o r t i n g the h y p o t h e s i s f o r thes e r e a s o n s : 1. The s t a t i s t i c s H and P cannot be equated w i t h e i t h e r a d d i t i v e or n o n - a d d i t i v e v a r i a t i o n . Only a d d i t i v e v a r i a t i o n i n f l u e n c e s e v o l u t i o n a r y r e s p o n s i v e n e s s . 2. H and P a r e not measurements of v a r i a t i o n p r o d u c t i o n per se. 3. L a r s o n (1981) s e v e r e l y c r i t i c i z e d P i e r c e and M i t t o n ' s s t a t i s t i c a l a n a l y s e s and c o n c l u d e d t h a t the r e p o r t e d r e l a t i o n s h i p was undemonstrated. There i s , however, c o n s i d e r a b l e l i t e r a t u r e t h a t i s 68 e x p l i c i t l y or i m p l i c i t l y s u g g e s t i v e of a r o l e of DNA i n e i t h e r p r omoting or s u p p r e s s i n g r a t e s of v a r i a t i o n p r o d u c t i o n . The q u e s t i o n t h a t needs t o be answered i s , "Does t h e " ~ ^ i n d of DNA o b s e r v e d t o be d i f f e r e n t i a l l y d i s t r i b u t e d a c r o s s organisms g e n e r a l l y i n c r e a s e or d e c r e a s e g e n e t i c v a r i a t i o n p r o d u c t i o n ? " Some " n u c l e o t y p i c e f f e c t s " of DNA c o u l d i n f l u e n c e v a r i a t i o n p r o d u c t i o n as w e l l as o t h e r p h e n o t y p i c t r a i t s . S e l e c t i o n f o r g r e a t e r e v o l u t i o n a r y r a t e would s e l e c t f o r s h o r t e r g e n e r a t i o n times as w e l l as more a d d i t i v e v a r i a t i o n p r o d u c t i o n . DNA b u l k might cause slow e r c e l l d i v i s i o n s and l o n g e r g e n e r a t i o n s and, t h e r e f o r e , d e c r e a s e d e v o l u t i o n a r y r e s p o n s i v e n e s s . Another n u c l e o t y p i c e f f e c t c o u l d occur i f the speed of c e l l d i v i s i o n s ( p a t t e r n s #10, #11), or of c e r t a i n phases of them (H o t t a and S t e r n 1965), had any i n f l u e n c e on the f i d e l i t y of DNA r e p l i c a t i o n , e i t h e r by f a c i l i t a t i n g e r r o r - c h e c k i n g p r o c e s s e s or by a l l o w i n g more time f o r the p r o p e r o r g a n i z a t i o n and a l i g n m e n t of g e n e t i c m a t e r i a l . The o r g a n i z i n g f u n c t i o n of h e t e r o c h r o m a t i n may l e a d t o h i g h e r r e p l i c a t i o n f i d e l i t y . "... h e t e r o c h r o m a t i n may h e l p m a i n t a i n the p r o p e r s p a t i a l r e l a t i o n s h i p s n e c e s s a r y f o r the e f f i c i e n t o p e r a t i o n of the c e l l t h r o u g h the s t a g e s of m e i o s i s and m i t o s i s " , f o r example i t may a i d i n the i n i t i a l a l i g n m ent of chromosomes p r i o r t o s y n a p s i s ( Y u n i s and Yasmineh 1971). A s y n a p s i s has l o n g been c a u s a l l y l i n k e d t o m u t a b i l i t y (Thompson 1962). But h e t e r o c h r o m a t i n may a l s o i n c r e a s e v a r i a t i o n p r o d u c t i o n , f o r example by a l l o w i n g chromosomal rearrangement ( Y u n i s and Yasmineh 1971). Supernumerary chromosome segments and B chromosomes are b o t h h e t e r o c h r o m a t i c . They have been observed 69 t o both i n c r e a s e and d e c r e a s e r e c o m b i n a t i o n r a t e s ( r e f s . i n Rees 1972; C a r l s o n 1978). I t i s r e l e v a n t t o ask what f r a c t i o n of DNA i s r e s p o n s i b l e f o r the d i f f e r e n c e s i n genome s i z e . On the one hand, t h e r e have been numerous r e p o r t s t h a t genome s i z e d i f f e r e n c e s are l a r g e l y d i f f e r e n c e s i n amount of i n t e r m e d i a t e l y r e p e t i t i v e DNA ( p a t t e r n #3). E vidence suggests ( Y u n i s and Yasmineh 1970) t h a t most i n t e r m e d i a t e l y r e p e t i t i v e DNA r e s i d e s i n h e t e r o c h r o m a t i n , and S t e b b i n s (1966) has noted t h a t p l a n t s w i t h l a r g e r genomes g e n e r a l l y have a g r e a t e r p r o p o r t i o n of h e t e r o c h r o m a t i n . On the o t h e r hand, t h e r e i s some e v i d e n c e of the p r o p o r t i o n of r e p e t i t i v e DNA not c h a n g i n g w i t h genome s i z e (Chooi 1971), and e v i d e n c e t h a t o t h e r f r a c t i o n s , e.g. s i n g l e - c o p y DNA, may vary s i g n i f i c a n t l y w i t h genome s i z e . ( r e f s . i n L a r s o n 1981). P r o b a b l y the best s u p p o r t e d of a l l r e l a t i o n s h i p s between DNA amount and v a r i a t i o n p r o d u c t i o n i s Hsu's (1975) "bodyguard h y p o t h e s i s " . He m a r s h a l l s c o n s i d e r a b l e c i r c u m s t a n t i a l e v i d e n c e i n f a v o r of h i s p r o p o s a l t h a t c o n s t i t u t i v e h e t e r o c h r o m a t i n f u n c t i o n s as a s h i e l d a g a i n s t "Mutagens, c l a s t o g e n s or even v i r u s e s a t t a c k i n g the n u c l e u s . . . " (Hsu 1975). A p r e l i m i n a r y experiment s u p p o r t e d h i s h y p o t h e s i s . I t i s a common i d e a t h a t g e n e t i c redundancy l e a d s t o the r e d u c t i o n of e x p r e s s e d v a r i a t i o n . Bachman et a l . (1972) d e s c r i b e the s u g g e s t i o n of B i e r and M u l l e r (1969) t h a t "... the r e p e t i t i v e n e s s i n h e r e n t i n l a r g e r genomes r e s u l t s i n a g e n e t i c i n e r t i a ; m u t a t i o n s i n s i n g l e c o p i e s of r e p e t i t i v e DNA a r e not q u a n t i t a t i v e l y i m p o r t a n t enough t o provoke n a t u r a l s e l e c t i o n , even i f the genes are 70 f u n c t i o n a l . " S t e b b i n s (1966) a s c r i b e s the r e t a r d e d e v o l u t i o n of p o l y p l o i d p l a n t s t o the presence of d u p l i c a t e d gene l o c i . The i d e a i s t h a t m u t a t i o n s , as l o n g as they a r e not dominant, w i l l have l e s s of an impact on phenotype i f they a r e " c o v e r e d f o r " by redundant c o p i e s . One problem i n a p p l y i n g t h i s c o v e r u p n o t i o n t o s p e c i e s which a re not p o l y p l o i d i s t h a t the assumed e x i s t e n c e of e x t e n s i v e tandem d u p l i c a t i o n has not been s u p p o r t e d ( P r i c e 1976). Some e v i d e n c e a g a i n s t the "coverup" e f f e c t of redundancy i s p r o v i d e d by Paquin and Adams (19 8 3 ) , who found the r a t e of v a r i a t i o n p r o d u c t i o n i n p o p u l a t i o n s of d i p l o i d y e a s t t o be almost t w i c e t h a t of c o i s o g e n i c h a p l o i d s . I t might be a g e n e r a l t r u t h t h a t , a t l e v e l s common i n organisms, v a r i a t i o n s u p p r e s s i o n r e q u i r e s more o r g a n i z a t i o n , and more DNA, than does v a r i a t i o n p r o m o t i o n . The h y p o t h e s i s t h a t amount of DNA and r a t e of v a r i a t i o n p r o d u c t i o n are n e g a t i v e l y c o r r e l a t e d i s t e s t a b l e (Hsu 1975), but the c r i t i c a l e x p e r i m e n t s have yet to be performed. CONCLUSION I have c r i t i c a l l y r e v i e w e d the e x i s t i n g e x p l a n a t i o n s f o r genome s i z e p a t t e r n s . Some are " s p e c i a l - c a s e " and narrow i n scope. The more g e n e r a l e x p l a n a t i o n s a r e i n t e r n a l l y i n c o n s i s t e n t , and u n t e s t a b l e . The c o r r e l a t i o n "the f a s t e r the r a t e of e v o l u t i o n , the s m a l l e r the genome s i z e " i s c o n s i s t e n t w i t h most of the r e p o r t e d p a t t e r n s . I t i s h y p o t h e s i z e d t h a t g r e a t e r amounts of DNA a r e c a u s a l l y c o n n e c t e d w i t h lower r a t e s of a d d i t i v e v a r i a t i o n 71 p r o d u c t i o n . A l t h o u g h i t i s t e s t a b l e , t h e r e i s a t p r e s e n t o n l y c i r c u m s t a n t i a l e v i d e n c e f o r t h i s h y p o t h e s i s . Given the h y p o t h e s i z e d r e l a t i o n s h i p , d i r e c t i o n a l s e l e c t i o n f o r p h e n o t y p i c v a r i a n t s c o u l d i n d i r e c t l y f a v o r s m a l l e r genomes, thus p r o d u c i n g the observed c o r r e l a t i o n . T e s t i n g t h i s e x p l a n a t i o n would r e q u i r e the q u a n t i f i c a t i o n of " r a t e of e v o l u t i o n " f o r many groups of organisms. T h i s problem i s a k i n t o t h a t of comparing " n i c h e s " . I t w i l l p r o b a b l y o n l y be p o s s i b l e t o make r e l a t i v e s t a t e m e n t s about r a t e s of e v o l u t i o n , under s p e c i a l l y c o n t r o l l e d c i r c u m s t a n c e s . 72 CHAPTER FIVE  TESTING THE IDEAS I have suggested (Chapter Four) t h a t a s i g n i f i c a n t p r o p o r t i o n of the genome can be c o n s i d e r e d a g e n e t i c memory f o r v a r i a t i o n p r o d u c t i o n p a t t e r n s , and I have d e s c r i b e d a s e l e c t i o n mechanism (Chapter One) by which i t can be m o d i f i e d . How does one go about t e s t i n g the h y p o t h e s i z e d e x i s t e n c e of a r e g u l a t i o n system f o r v a r i a t i o n p r o d u c t i o n ? The a v a i l a b l e o p t i o n s are to seek: 1. g e n e t i c e v i d e n c e of the system i t s e l f , and/or 2. e v i d e n c e of the a c t i o n of such a system. Each s o r t of e v i d e n c e c o u l d be sought i n a " n a t u r a l e x p e r i m e n t " , or a p u r p o s e f u l l y c r e a t e d e x p e r i m e n t . A f t e r b r i e f l y n o t i n g which organisms are most l i k e l y t o have m e t a v a r i a t i o n systems, I w i l l s p e c u l a t e on the s t r u c t u r e of a m e t a v a r i a t i o n system. An ex p e c t e d s t r u c t u r e i s a requ i r e m e n t f o r s e e k i n g e v i d e n c e of the system i t s e l f . I w i l l then d i s c u s s problems i n measuring the ex p e c t e d p a t t e r n s i n g e n e t i c v a r i a t i o n . A s u g g e s t e d experiment i s o u t l i n e d , and the outcomes of some r e l a t e d p r e v i o u s e x p e r i m e n t s a r e d i s c u s s e d . Throughout t h i s c h a p t e r I e x e r c i s e the " m e t a v a r i a t i o n p e r s p e c t i v e " by g e n e r a t i n g q u e s t i o n s . The c h a p t e r ends w i t h a d i s c u s s i o n of the r e l e v a n c e of the i d e a s t o two "bandwagon" t o p i c s . 73 Where t o Look Organisms most l i k e l y t o have a m e t a v a r i a t i o n system would l i v e i n an environment 1. which changed over t i m e , over a g r e a t e r range than t h a t which c o u l d be accommodated by p h e n o t y p i c f l e x i b i l i t y , n e c e s s i t a t i n g a g e n e t i c r e s ponse. 2. where the change i n r a t e s and/or d i r e c t i o n of change of the e n v i r o n m e n t a l change has t o be p r e d i c t a b l e "enough" t o make m o d i f i c a t i o n of v a r i a t i o n p r o d u c t i o n p a t t e r n s w o r t h w h i l e . The d i f f i c u l t i e s of c h o o s i n g a l i k e l y organism a re those of d e t e r m i n i n g " e n v i r o n m e n t a l g r a i n " ( i . e . how the environment i s p e r c e i v e d by the organism) and the l a c k of a q u a n t i t a t i v e t h e o r y t o p r o p e r l y d e s c r i b e "enough". Could i t be more e s s e n t i a l t h a t complex o r g a n i s m s , of lower f e c u n d i t y , f i n d a way of r e d u c i n g t h e i r l o s s e s ( u n f i t v a r i a n t s ) i n v a r i a n t p r o d u c t i o n ? Making the assumption t h a t the d i f f e r e n t i a l l y d i s t r i b u t e d DNA among t a x a has i t s f u n c t i o n i n the r e g u l a t i o n of v a r i a t i o n p r o d u c t i o n , i t would be i n t e r e s t i n g t o see i f t h e r e i s a s i g n i f i c a n t l y b e t t e r c o r r e l a t i o n of DNA c o n t e n t w i t h e s t i m a t e d i n f o r m a t i o n r e q u i r e m e n t f o r s i m p l e r organisms as compared w i t h complex ones. S p e c u l a t i o n on M e t a v a r i a t i o n System S t r u c t u r e In the l a s t c h a p t e r I c o n s i d e r e d known p a t t e r n s i n genome s i z e . I noted a t the o u t s e t t h a t d i f f e r e n c e s i n genome s i z e c o u l d be i n t e r p r e t e d as rough i n d i c a t o r s of d i f f e r e n c e s i n genome s t r u c t u r e . A l t h o u g h , as p r e d i c t e d from the m e t a v a r i a t i o n 7 4 model, the p a t t e r n s seemed t o v a r y a c c o r d i n g t o the " r a t e of e v o l u t i o n " of a group, the l i n k i n g of g r e a t e r amount of DNA w i t h l e s s v a r i a t i o n p r o d u c t i o n was s t r i c t l y post hoc. There was no p r i o r e x p e c t a t i o n about how such v a r i a t i o n r e g u l a t i o n might be o r g a n i z e d . I t would be u s e f u l t o s p e c u l a t e about the g e n e t i c s t r u c t u r e of a system f o r v a r i a t i o n p r o d u c t i o n a d j u s t m e n t . A h y p o t h e t i c a l model system c o u l d y i e l d new i n s i g h t i n t o p r e s e n t knowledge. I f some n e c e s s a r y c h a r a c t e r i s t i c s c o u l d be e s t a b l i s h e d , the way would be open t o f a l s i f i c a t i o n of the i d e a t h a t v a r i a t i o n c o n t r o l e x i s t s i n an o r g a n i z e d system. We know t h a t : 1. To maximize the e f f e c t i v e n e s s of secondary s e l e c t i o n on a s e t of v a r i a t i o n p r o d u c t i o n schemes, the v a r i a t i o n p r o d u c t i o n m o d i f i e r s s h o u l d be c l o s e l y l i n k e d to the genes t h a t i n f l u e n c e the phenotype upon which ( p r i m a r y ) s e l e c t i o n a c t s . In t h a t way the ' h e r i t a b i l i t y ' or c o r r e l a t i o n between genotypes c r e a t e d from a c e r t a i n v a r i a t i o n p r o d u c t i o n scheme, and the b e t a genes t h a t program t h a t scheme, i s as h i g h as p o s s i b l e . I i n t e n t i o n a l l y used a s e x u a l p o p u l a t i o n s t o d e s c r i b e the a c t i o n of secondary s e l e c t i o n (Chapter One). In a p a n m i c t i c s e x u a l p o p u l a t i o n , i f beta and a l p h a gene were not l i n k e d , then they would remain a s s o c i a t e d f o r an average of o n l y two g e n e r a t i o n s ( L e i g h 1970). In t h a t s i t u a t i o n t h e r e i s l i t t l e a s s o c i a t i o n between phenotype and the h y p o t h e t i c a l v a r i a t i o n c o n t r o l genes r e s p o n s i b l e f o r p r o d u c i n g i t , and secondary s e l e c t i o n i s l e a s t ef f e c t i v e . 75 2. S i n c e e v o l u t i o n a r y r e s p o n s i v e n e s s w i l l not n e c e s s a r i l y be r e q u i r e d of a l l t r a i t s a t the same t i m e , the independent " c o n t r o l of v a r i a t i o n f o r d i f f e r e n t t r a i t s i s advantageous. 3. There must be a c e r t a i n amount of r e c o m b i n a t i o n between the genes i n v o l v e d i n p r o d u c i n g the t r a i t s u n d e r g o i n g s e l e c t e d change, and those genes of t r a i t s under d i f f e r e n t s e l e c t i o n regimes, i n o r d e r t o a v o i d the H i l l - R o b e r t s o n e f f e c t ( F e l s e n s t e i n 1974). One way t o have independent c o n t r o l of t r a i t s would be t o have s e p a r a t e m o d i f i e r s c o n t r o l l i n g each l o c u s i n the genome ( c l o s e l y l i n k e d t o the l o c u s f o r reason (1) ). But s e l e c t i o n i s more e f f e c t i v e on m o d i f i e r s i f one m o d i f i e r a f f e c t s many l o c i ( K a r l i n and McGregor 1974). So the most r e s p o n s i v e v a r i a t i o n r e g u l a t i o n system would have o n l y one m o d i f i e r f o r each independent t r a i t . I t appears t h a t the ways t o s a t i s f y the d u a l r e q u i r e m e n t s of t i g h t l i n k a g e t o each l o c u s , and one m o d i f i e r f o r s e v e r a l l o c i , a r e : 1. combine a l l l o c i f o r a t r a i t , and the m o d i f i e r , i n one l i n k a g e group 2. have a r e g u l a t o r - c o n t r o l l e r system i s o m o r p h i c t o the gene r e g u l a t i o n system proposed by B r i t t e n and Davidson (1969) f o r gene r e g u l a t i o n . The p l e i o t r o p i c r e l a t i o n s h i p t h a t can e x i s t between genes and t r a i t s makes s o l u t i o n (1) l e s s e f f e c t i v e than ( 2 ) . In a r e g u l a t o r - c o n t r o l l e r system ( 2 ) , one or more ' c o n t r o l l e r s ' ( ' r e c e p t o r s ' ) would be l i n k e d t o each p r i m a r y l o c u s , and they would r e c e i v e s i g n a l s from p a r t i c u l a r monomorphic ' r e g u l a t o r * l o c i ( the m o d i f i e r genes) t o , f o r example, a l l o w or d i s a l l o w 76 e r r o r - c h e c k i n g by a c e r t a i n enzyme. The f a c t t h a t the s t r u c t u r a l p r e d i c t i o n s of the i d e a l gene r e g u l a t i o n system and the i d e a l v a r i a t i o n r e g u l a t i o n system c o i n c i d e i s i m p o r t a n t i n i t s e l f , s i n c e i t g i v e s two d i f f e r e n t i n t e r p r e t a t i o n s t o the same s t r u c t u r a l e v i d e n c e . I t might a f f e c t c o n f i d e n c e i n the h y p o t h e s i z e d gene r e g u l a t i o n system. M c C l i n t o c k (1965) has d e s c r i b e d a r e g u l a t o r - c o n t r o l l e r system f o r m u t a t i o n i n maize. And s e v e r a l a u t h o r s , i n c l u d i n g Nagl (1979), have v o i c e d s u s p i c i o n t h a t v a r i a t i o n p r o d u c t i o n and d i f f e r e n t i a t i o n may be r e l a t e d p r o c e s s e s . Two i m p o r t a n t p o i n t s a r e : 1. The most r e s p o n s i v e system i s not a l w a y s the most a p p r o p r i a t e one, the l a t t e r being d e t e r m i n e d by the p r e d i c t a b i l i t y of the r a t e of change of e n v i r o n m e n t a l change. I t s h o u l d be apparent t h a t r e s p o n s i v e n e s s would be slowed by the i n c r e a s e of r e c o m b i n a t i o n r a t e s between l o c i and t h e i r v a r i a t i o n ' c o n t r o l l e r s ' , and the decrease of r e c o m b i n a t i o n between l o c i i n v o l v e d i n d i f f e r e n t t r a i t s , t o produce the H i l l - R o b e r t s o n e f f e c t . 2. I t may r e q u i r e a l e s s h i g h l y f o r m a l i z e d v a r i a t i o n r e g u l a t i o n system than the one j u s t s u g g e s t e d t o p a t t e r n v a r i a t i o n t o a s i g n i f i c a n t e x t e n t . Gene d u p l i c a t i o n , or changes i n the b u l k of DNA p r e s e n t (see o t h e r i n f l u e n c e s i n p r e v i o u s c h a p t e r ) , f o r example, may be enough. 77 E p i g e n e s i s and C a n a l i z a t i o n So f a r I have been making the s t a n d a r d Neo-Darwinian s i m p l i f i c a t i o n of i g n o r i n g the p r o c e s s of e p i g e n e s i s . The p r o c e s s of e p i g e n e s i s l i e s between the g e n e t i c mechanisms I have been d i s c u s s i n g , and the phenotype (and p h e n o t y p i c v a r i a t i o n ) . I t i.s the r e l a t i o n s h i p s of genes and t r a i t s (one-to-one, e p i s t a t i c , p l e i o t r o p i c ) , an e p i g e n e t i c c o n s i d e r a t i o n , t h a t d e termine the " a d d i t i v i t y " of g e n e t i c v a r i a t i o n . > GENOTYPE > PHENOTYPE mu t a t i o n e p i g e n e s i s E a r l i e r I mentioned a p o s s i b l e r e l a t e d n e s s between d i f f e r e n t i a t i o n and v a r i a t i o n p r o d u c t i o n i n the c o n t e x t of the s i m i l a r i t y of the g e n e t i c o r g a n i z a t i o n t h a t each r e q u i r e . Now I would l i k e t o note the g r e a t s i m i l a r i t y of the changing p a t t e r n s of v a r i a t i o n p r o d u c t i o n expected from a m e t a v a r i a t i o n system, and the phenomenon of " c a n a l i z a t i o n " c a u s a l l y a t t r i b u t e d t o the e p i g e n e t i c system. C a n a l i z a t i o n i s the "deepening" of a d e v e l o p m e n t a l response so t h a t the same norm i s produced d e s p i t e c o n s i d e r a b l e v a r i a t i o n i n the environment (Waddington 1957,1975). I t r e f e r s , not t o the d e c r e a s e i n p h e n o t y p i c v a r i a t i o n per se, but t o the d e c r e a s i n g s e n s i t i v i t y of the d e v e l o p m e n t a l pathway t o v a r i a t i o n i n the environment. At the p h e n o t y p i c l e v e l t h i s i m p l i e s l e s s v a r i a t i o n i n the t r a i t , a change t h a t c o u l d be mimicked by s t a b i l i z i n g s e l e c t i o n on m e t a v a r i a t i o n . M o d i f i e r f r e q u e n c i e s change s l o w l y . C a n a l i z a t i o n "...has been observed i n s i t u a t i o n s i n which s e l e c t i o n p r e s s u r e c o n t i n u e s f o r many g e n e r a t i o n s . " (Waddington 78 1974) S t a b l e environments and s t a b i l i z i n g s e l e c t i o n f a v o r c a n a l i z a t i o n , whereas c h a n g i n g environments and d i s r u p t i v e s e l e c t i o n f a v o r i t s breakdown (Waddington and Ro b e r t s o n 1966, and r e f e r e n c e s t h e r e i n ) . Waddington g i v e s c r e d i t t o the e p i g e n e t i c system, r a t h e r than t o a c a t e g o r y of (b e t a ) genes, f o r f o c u s s i n g v a r i a t i o n p r o d u c t i o n . On Measur i n q Genet i c Var i a t i o n P r o d u c t i o n One p r e d i c t i o n based on the assumed e x i s t e n c e of a m e t a v a r i a t i o n system i s t h a t g e n e t i c v a r i a t i o n i n p o p u l a t i o n s be a d a p t i v e l y p a t t e r n e d t o s u i t the environment. ( T h i s i s the "n i c h e v a r i a t i o n h y p o t h e s i s " about g e n e t i c v a r i a t i o n . ) T h i s i s a weak p r e d i c t i o n , because f i n d i n g such p a t t e r n s would not imply the e x i s t e n c e of the h y p o t h e s i z e d m e t a v a r i a t i o n system. S t r o n g e r p r e d i c t i o n s would be i n terms of changes i n v a r i a t i o n p r o d u c t i o n p a t t e r n s . In e i t h e r case a t e s t i n v o l v e s the measurement of g e n e t i c v a r i a t i o n p r o d u c t i o n . G e n e t i c v a r i a t i o n ( g e n e r a l l y measured v i a phenotype) i s u s u a l l y q u a n t i f i e d i n terms of average h e t e r o z y g o s i t y (H) and p e r c e n t of p o l y m o r p h i c l o c i ( P ) . These c o n v e n i e n t s t a t i s t i c s bear no c l e a r r e l a t i o n s h i p t o the c a t e g o r i e s " a d d i t i v e " and " n o n - a d d i t i v e " g e n e t i c v a r i a t i o n . L e v i n s (1964a) was c l e a r i n h i s e x p l a n a t i o n t h a t a d d i t i v e and n o n - a d d i t i v e v a r i a t i o n have d i f f e r e n t f u n c t i o n s i n a d a p t a t i o n , and are f a v o r e d by n a t u r a l s e l e c t i o n under d i f f e r e n t c i r c u m s t a n c e s . For example, an environment c o n s t a n t i n time would not f a v o r the maintenance of a d d i t i v e v a r i a t i o n . But t h a t same s t a b i l i t y c o u l d e n able p o p u l a t i o n s t o p e r c e i v e the environment as s p a t i a l l y p a t c h y , a 79 s i t u a t i o n f a v o r i n g the maintenance of n o n - a d d i t i v e v a r i a t i o n i n the p o p u l a t i o n . A l l p r e d i c t i o n s of the m e t a v a r i a t i o n model are i n terms of a d d i t i v e v a r i a t i o n o n l y . Any p a t t e r n comparing g e n e t i c v a r i a t i o n measured by H and P w i t h some o t h e r f a c t o r i s p o t e n t i a l l y i n f l u e n c e d by d i f f e r i n g amounts of n o n - a d d i t i v e v a r i a t i o n . The r e s t of the problem i s i n how t o e s t i m a t e v a r i a t i o n p r o d u c t i o n . V a r i a t i o n i n a p o p u l a t i o n i s i n f l u e n c e d by s e v e r a l f a c t o r s such as p o p u l a t i o n s i z e , p o p u l a t i o n s t r u c t u r e , and h i s t o r y ( t i m e s i n c e l a s t b o t t l e n e c k i n g ) . And, s h o u l d the v a r i a t i o n be i n t e r p r e t e d as p r e - s e l e c t i o n , or p o s t - s e l e c t i o n ? I s low v a r i a t i o n i n d i c a t i v e of low v a r i a t i o n p r o d u c t i o n , or h i g h s e l e c t i o n ? Perhaps the best way t o measure t h e a d d i t i v e v a r i a t i o n r e l e v a n t t o t h e s e hypotheses would be i n d i r e c t l y v i a measurements of e v o l u t i o n a r y r e s p o n s i v e n e s s . T h i s would b e s t be done t h r o u g h s e l e c t i o n e x p e r i m e n t s u s i n g the methods of a n a l y s i s of q u a n t i t a t i v e g e n e t i c s . Suggested Experiment A y a l a (1966,1967,1969) performed experiments i n which he compared the e v o l u t i o n a r y response of i r r a d i a t e d f r u i t f l i e s w i t h t h a t of unexposed f l i e s . The i n c r e a s i n g p o p u l a t i o n d e n s i t i e s i n h i s cages p r o v i d e d the d i r e c t i o n a l s e l e c t i o n p r e s s u r e . A d a p t a t i o n was a s s e s s e d i n terms of p o p u l a t i o n s i z e , and p r o d u c t i v i t y . A f t e r an i n i t i a l d e l a y , the i r r a d i a t e d p o p u l a t i o n s i n c r e a s e d i n f i t n e s s and became b e t t e r adapted than the c o n t r o l s . 80 I propose a s i m i l a r experiment i n which d i r e c t i o n a l s e l e c t i o n , i n s t e a d of i o n i z i n g r a d i a t i o n , i s used t o t r i g g e r i n c r e a s e d v a r i a t i o n p r o d u c t i o n . The h y p o t h e s i s i s t h a t a m e t a v a r i a t i o n system e x i s t s . T h i s i m p l i e s t h a t s t a b i l i z i n g s e l e c t i o n w i l l cause v a r i a t i o n p r o d u c t i o n t o d e c r ease i n a p o p u l a t i o n , and d i r e c t i o n a l s e l e c t i o n w i l l cause i t t o i n c r e a s e . The r a t e of v a r i a t i o n p r o d u c t i o n w i l l be compared i n two groups of p o p u l a t i o n s by comparing t h e i r e v o l u t i o n a r y r e s p o n s i v e n e s s . The l a t t e r w i l l be measured as a b i l i t y t o m a i n t a i n p r o d u c t i v i t y i n a c h a n g i n g environment. The e x p e r i m e n t a l t r i c k i s t o s t i m u l a t e v a r i a t i o n p r o d u c t i o n i n one group by d i r e c t i o n a l s e l e c t i o n i n a way t h a t does not c o n f e r i t w i t h an advantage i n a p p r o p r i a t e s t o r e d v a r i a t i o n . T h i s i s t o be a c c o m p l i s h e d as f o l l o w s : 1. Choose a v a r i a b l e t h a t can be c o n v e n i e n t l y m a n i p u l a t e d t o produce d i r e c t i o n a l s e l e c t i o n i n two ( o p p o s i t e ) d i r e c t i o n s , and s t r o n g s t a b i l i z i n g s e l e c t i o n . A v a r i a b l e such as d e v e l o p m e n t a l t i m e , t h a t p e r m i t s c a t a s t r o p h i c c u t o f f beyond a p r e d e t e r m i n e d range, i s s u p e r i o r t o a v a r i a b l e l i k e temperature t o l e r a n c e . 2. S t a r t two groups of p o p u l a t i o n s from the same s t o c k . Each p o p u l a t i o n s h o u l d be l a r g e enough t o m i n i m i z e the importance of d r i f t , yet s m a l l r e l a t i v e t o the c a r r y i n g c a p a c i t y of i t s c o n t a i n e r . 3. L e t us c a l l the s t a r t i n g v a l u e of the s e l e c t i o n v a r i a b l e " r e l a t i v e z e r o " . R e l a t i v e z e r o s h o u l d be as c l o s e as p o s s i b l e t o the c o n d i t i o n s under which the founder s t o c k has been m a i n t a i n e d f o r a l o n g t i m e , so t h a t " s t a b i l i z i n g " 81 s e l e c t i o n around r e l a t i v e z e r o does not amount t o d i r e c t i o n a l s e l e c t i o n . S u b j e c t group A t o s t a b i l i z i n g s e l e c t i o n a t r e l a t i v e z e r o . 4. S u b j e c t group B t o d i r e c t i o n a l s e l e c t i o n i n the " n e g a t i v e " d i r e c t i o n ( a r b i t r a r y ) . For l a c k of a q u a n t i t a t i v e t h e o r y I cannot s p e c i f y the d u r a t i o n and i n t e n s i t y of d i r e c t i o n a l s e l e c t i o n r e q u i r e d t o s i g n i f i c a n t l y change t h e f r e q u e n c i e s of m o d i f i e r a l l e l e s . (Remember t h a t the speeds of s e l e c t i o n a t m o d i f i e r l o c i w i l l be much slowe r than the speed of s e l e c t i o n on a l l e l e s d e t e r m i n i n g phenotype.) Group B i s t o be d i r e c t i o n a l l y s e l e c t e d t o h a l f t h a t undetermined e x t e n t i n the n e g a t i v e d i r e c t i o n , and then back a g a i n t o r e l a t i v e z e r o . T h i s t r e a t m e n t i s i n t e n d e d t o " t u r n on" v a r i a t i o n p r o d u c t i o n w i t h o u t s t o r i n g a l l e l e s i n the p o p u l a t i o n a p p r o p r i a t e f o r the next g e n e t i c r e s p o n s e . The i m p o r t a n t e n v i r o n m e n t a l change f o r p r o d u c i n g d i r e c t i o n a l s e l e c t i o n i s between g e n e r a t i o n s , not w i t h i n g e n e r a t i o n s . The c l a s s i c a l e x p e r i m e n t s t e s t i n g the e f f e c t i v e n e s s of heterogeneous environments i n m a i n t a i n i n g polymorphisms ( P o w e l l 1971; A y a l a and McDonald 1974) used w i t h i n - g e n e r a t i o n t e m p o r a l h e t e r o g e n e i t y , which would not be e x p e c t e d t o f a v o r the maintenance of a d d i t i v e v a r i a t i o n . 5. The p r o d u c t i v i t y of groups A and B i s t o be measured a t the same t i m e s , over r e g u l a r i n t e r v a l s . P r o d u c t i v i t y i s t o be measured i n terms of the " s u r p l u s " over a p o p u l a t i o n s i z e " q u ota". The q u o t a i s s e t l a r g e enough t o a v o i d the 82 i n f l u e n c e of g e n e t i c d r i f t . The p o p u l a t i o n s a re r e s e t t o t h i s quota at each census. The r a t e of change of the s e l e c t i o n v a r i a b l e , which d e t e r m i n e s the i n t e n s i t y of d i r e c t i o n a l s e l e c t i o n , i s t o be c o n t r o l l e d so t h a t the a d u l t p o p u l a t i o n s i z e never f a l l s below the q u o t a . 6. As group B i s r e t u r n e d t o c o n d i t i o n s a t r e l a t i v e z e r o , b e g i n d i r e c t i o n a l s e l e c t i o n of both groups, t o g e t h e r , i n the " p o s i t i v e " d i r e c t i o n . M o n i t o r t h e i r r e l a t i v e p r o d u c t i v i t i e s . My p r e d i c t i o n i s t h a t group A w i l l i n i t i a l l y be more r e s p o n s i v e t o the s e l e c t i o n because i t s s t o r e d v a r i a t i o n i s l i k e l y t o be g r e a t e r , and more a p p r o p r i a t e t o c o n d i t i o n s s l i g h t l y " p o s i t i v e " . Group B, i f i t d i d inde e d produce v a r i a t i o n a t a g r e a t e r r a t e by t h i s t i m e , s h o u l d g a i n and s u r p a s s group A i n adaptedness as the l a t t e r ' s s t o r e d v a r i a t i o n i s d e p l e t e d . A p o s s i b l e c r i t i c i s m of t h i s experiment i s t h a t the a l t e r e d e n v i r o n m e n t a l parameter i t s e l f ( e .g. t e m p e r a t u r e ) , r a t h e r than d i r e c t i o n a l s e l e c t i o n , may be r e s p o n s i b l e f o r changing v a r i a t i o n p r o d u c t i o n . The r e l a t i v e m e r i t s of s t o r e d v e r s u s produced v a r i a t i o n a r e an i m p o r t a n t c o n s i d e r a t i o n . Slow v a r i a t i o n p r o d u c t i o n might r e q u i r e t h a t v e r y l a r g e p o p u l a t i o n s be used i n o r d e r t o o b t a i n a p p r e c i a b l e g e n e t i c response. And i f p h e n o t y p i c v a r i a t i o n p r o d u c t i o n were moderated a t the e p i g e n e t i c l e v e l , then group A, under s t a b i l i z i n g s e l e c t i o n , c o u l d m a i n t a i n a s i z a b l e s t o r e of p o t e n t i a l l y u s e f u l a l l e l e s w h i l e p r o d u c i n g l i t t l e p h e n o t y p i c v a r i a t i o n . 83 P r e v i o u s E x p e r i m e n t s S e v e r a l e x periments have been done comparing the c o m p e t i t i v e a b i l i t y of s t r a i n s d i f f e r i n g i n r a t e s of v a r i a t i o n p r o d u c t i o n . These have compared, f o r example, mutator and w i l d -type s t r a i n s of E s c h e r i c h i a c o l i (Gibson et a l . 1970; Cox and Gibson 1974; Chao and Cox 1983), and i s o g e n i c haploi.d and d i p l o i d s t r a i n s of the y e a s t Saccharomyces c e r e v i s i a e (Paquin and Adams 1983). In both of t h e s e cases the competing s t r a i n s were a s e x u a l , and c o n s i d e r e d t o be f a c i n g the problem of a d a p t a t i o n t o a new environment. The mutator E. c o l i and the d i p l o i d S. c e r e v i s i a e proved t o be c o m p e t i t i v e l y s u p e r i o r by reason of a f a s t e r r a t e of f i x a t i o n of advantageous new m u t a t i o n s -- they e v o l v e d f a s t e r . The mutator E. c o l i had a h i g h e r m u t a t i o n .rate. The d i p l o i d y e a s t was assumed t o have the same p e r - l o c u s m u t a t i o n r a t e as the i s o g e n i c h a p l o i d , and t h e r e f o r e t w i c e the o v e r a l l m u t a t i o n r a t e of the h a p l o i d . Chao and Cox (1983) c o n c l u d e d t h a t " . . . i t i s s u r p r i s i n g t h a t mutator genes are r a r e l y found i n n a t u r e . " E v o l u t i o n d i d not s t o p over the c o u r s e of t h e i r experiment -- an e q u i l i b r i u m , or " a d a p t i v e peak", was never reached. I would expect t h a t s t a b i l i z i n g s e l e c t i o n , i f i t c o u l d be produced i n t h e i r system, would be to the advantage of the non-mutator. These a r e comparisons of the s u i t a b i l i t y of d i f f e r e n t v a r i a t i o n schemes t o a g i v e n environment, r a t h e r than a t e s t f o r the e x i s t e n c e of m e t a v a r i a t i o n , i . e . the a b i l i t y of a s t r a i n t o change i t s v a r i a t i o n p r o d u c t i o n scheme. 84 M e t a v a r i a t i o n as E x p l a n a t i o n in Two Bandwagon T o p i c s SEX. Sex p e r m i t s a m y r i a d of d i f f e r e n t ways i n which gene f l o w , and c o n s e q u e n t l y g e n e t i c v a r i a t i o n p r o d u c t i o n , can be r e g u l a t e d . (See the f a c t o r s i n T a b l e 1.) The concept and c o s t of a d a p t a b i l i t y have been d i s c u s s e d more i n the l i t e r a t u r e on the v a l u e of sex than anywhere e l s e . I t h i n k i t i s i m p o r t a n t to r e a l i z e t h a t , i n b e i n g a b e t w e e n - i n d i v i d u a l phenomenon, sex opens the way f o r u s i n g s p a t i a l (between i n d i v i d u a l ) h e t e r o g e n e i t y f o r temporal cues, damping g e n e t i c response to l o c a l , s h o r t - t e r m f l u c t u a t i o n s . ( T h i s k i n d of response i s w a s t e f u l . See L e v i n s (1964) on the a d a p t i v e s i g n i f i c a n c e of gene f l o w . ) More than j u s t r e c o m b i n a t i o n , a p r o c e s s of g e n e t i c v a r i a t i o n p r o d u c t i o n , sex i s a mechanism by which v a r i a t i o n p r o d u c t i o n can be a d j u s t e d and r e g u l a t e d i n many ways, r a n g i n g from a s s o r t a t i v e n e s s of m a t i n g s , t o d i s p e r s a l r a t e s , t o the extreme of r e p r o d u c t i v e i s o l a t i o n . I p r e f e r t o view sex as a v e r y f l e x i b l e system f o r p r o d u c i n g m e t a v a r i a t i o n . HYBRID DYSGENESIS. From the s t a n d p o i n t of m e t a v a r i a t i o n , the phenomenon of h y b r i d d y s g e n e s i s i s v e r y i n t e r e s t i n g : " H y b r i d d y s g e n e s i s a r i s e s i n one of the two r e c i p r o c a l male-female c r o s s e s , u s u a l l y males from r e c e n t l y w i l d -caught s t r a i n s c r o s s e d w i t h females from l o n g - e s t a b l i s h e d l a b o r a t o r y s t r a i n s ... I t i s c h a r a c t e r i z e d by v a r i o u s a s s o c i a t e d germ l i n e d y s f u n c t i o n s i n c l u d i n g h i g h m u t a b i l i t y , f r e q u e n t chromosomal rearrangements, male r e c o m b i n a t i o n ( n o r m a l l y absent i n D r o s o p h i l a ) , f a i l u r e of e a r l y embryonic development, and s t e r i l i t y due t o germ l i n e e x t i n c t i o n i n both males and f e m a l e s . . . The o n l y p u z z l e i s 85 the o s t e n s i b l e n o r m a l i t y of the somatic t i s s u e . " (Rose and D o o l i t t l e 1983) So f a r two i n t e r a c t i o n systems (P-M and I-R) have been found t o u n d e r l y h y b r i d d y s g e n e s i s , and they have been shown t o i n v o l v e t r a n s p o s a b l e P and I elements (Rose and D o o l i t t l e 1983). The d i s t r i b u t i o n s of P and I s t r a i n s show s t r i k i n g t e m p o r a l t r e n d s : l a b o r a t o r y age i s i n v e r s e l y c o r r e l a t e d w i t h the presence of a c t i v e P and I elements. Two hypotheses have been advanced t o e x p l a i n why o l d e r l a b o r a t o r y p o p u l a t i o n s of D r o s o p h i l a have fewer P and I elements ( B r e g l i a n o and K i d w e l l 1983): 1. The " s t o c h a s t i c l o s s h y p o t h e s i s " (Bucheton et a l . 1976; E n g e l s 1981) s u g g e s t s t h a t R and M p o p u l a t i o n s r e s u l t from the l o s s of I and P f a c t o r s i n s m a l l i s o l a t e s , m a i n l y those kept under l a b o r a t o r y c o n d i t i o n s . 2. The " r e c e n t i n v a s i o n h y p o t h e s i s " ( K i d w e l l 1979,1982) s u g g e s t s t h a t t h e r e has r e c e n t l y been a r a p i d spread of I and P f a c t o r s t h rough n a t u r a l p o p u l a t i o n s . O l d l a b o r a t o r y s t r a i n s r e c o r d the o r i g i n a l s t a t e of w i l d p o p u l a t i o n s . A g a i n , t h e r e i s a m i s s i n g h y p o t h e s i s d e a l i n g w i t h the c o n s t a n c y , or r a t e of change, r a t h e r than the p a r t i c u l a r s t a t e , of the l a b environment. Maybe the P and I elements a r e r e l a t e d t o v a r i a t i o n p r o d u c t i o n and a r e l e s s b e n e f i c i a l i n the c o n s t a n t l a b environment than they a r e i n a perhaps more t e m p o r a l l y heterogeneous n a t u r a l environment. From my p e r s p e c t i v e , p a r t i c u l a r l y g i v e n the " p u z z l i n g " n o r m a l i t y of the soma, the phenomenon of h y b r i d d y s g e n e s i s l o o k s l i k e a runaway v a r i a t i o n p r o d u c t i o n system — too much, or u n c o n t r o l l e d , v a r i a t i o n i s produced i n the germ l i n e 86 ( o f f s p r i n g ) . N o t i c e t h a t , l i k e sex, i t i s a b e t w e e n - i n d i v i d u a l phenomenon, and c o u l d t h e r e f o r e be p l a y i n g a f u n c t i o n i n u s i n g s p a t i a l h e t e r o g e n e i t y as a means of p r e d i c t i n g and r e g u l a t i n g v a r i a t i o n u s e f u l i n t e m p o r a l r e s p o n s i v e n e s s . B r e g l i a n o and K i d w e l l (1983) note t h a t d a t a on the t i m i n g of appearance of I and P f a c t o r s i n w i l d p o p u l a t i o n s "... r o u g h l y c o i n c i d e s w i t h the appearance of s t r o n g new s e l e c t i v e p r e s s u r e s i n p o p u l a t i o n s of i n s e c t s " . The d a t e s of appearance of I and P s t r a i n s c o r r e s p o n d w i t h i n t e n s i v e use of DDT, and f i r s t use of organophosphates, r e s p e c t i v e l y ( B r e g l i a n o and K i d w e l l 1983). I would l i k e t o emphasize h y b r i d d y s g e n e s i s as an im p o r t a n t p l a c e t o s t a r t l o o k i n g f o r a system i n v o l v e d i n r e g u l a t i n g v a r i a t i o n p r o d u c t i o n . 87 DISCUSSION "There has grown up, w i t h i n the N e o - D a r w i n i s t paradigm of e v o l u t i o n a r y t h e o r y , a dogma t h a t the c h a r a c t e r of any new elements t h a t may appear i n a p o p u l a t i o n as p o t e n t i a l raw m a t e r i a l s f o r e v o l u t i o n are q u i t e unconnected w i t h the n a t u r e of the s e l e c t i o n p r o c e s s t o which they w i l l be s u b j e c t e d . . . T h i s seems t o be not o n l y t e n a c i o u s l y b e l i e v e d , but d e e p l y f e l t . . . " ( C H . Waddington 1974). P o p u l a t i o n - l e v e l Genet i c Memory Waddington and h i s f o l l o w e r s have s t r e s s e d the importance of the " e p i g e n e t i c system", a phe n o m e n o l o g i c a l model, i n a d a p t i v e l y f o c u s s i n g the p r o d u c t i o n of p h e n o t y p i c v a r i a t i o n . The e p i g e n e t i c system i s presumably the r e s u l t of a l o n g p e r i o d of e v o l u t i o n . In the c o u r s e of t h i s t h e s i s I have d e s c r i b e d not a phen o m e n o l o g i c a l model, d e r i v e d from e x p e r i m e n t a l o b s e r v a t i o n s , but r a t h e r a mechanism t h a t might be c o n s i d e r e d a f i r s t a p p r o x i m a t i o n t o an e p i g e n e t i c system. I t i s premised on a c o n c e p t u a l d i v i s i o n of the genome i n t o two, not n e c e s s a r i l y m u t u a l l y e x c l u s i v e , s e t s of genes ( L a y z e r 1980): 88 1. those ( a l p h a genes) which govern the development and maintenance of the i n d i v i d u a l organism, and 2. those Cf/eta genes) which govern g e n e t i c a d a p t a b i l i t y , i . e . g e n e t i c v a r i a t i o n p r o d u c t i o n . To use L e v i n s ' (1968, and see end of my Chapter Three) memory a n a l o g y , the a l p h a memory s t o r e s what s e l e c t i o n has f a v o r e d i n developmental programs, and the beta memory s t o r e s what s e l e c t i o n has f a v o r e d i n g e n o t y p i c v a r i a t i o n p r o d u c t i o n . Each memory' has a c h a r a c t e r i s t i c l a g time due t o the time i t t a k e s t o f i x new i n f o r m a t i o n . For example, the " a l p h a memory" i s l a s t i n f l u e n c e d by the environment of the p a s t g e n e r a t i o n . U n l e s s the l a s t g e n e r a t i o n was a good p r e d i c t o r of the p r e s e n t g e n e r a t i o n , i t would not have been an advantage t o respond g e n e t i c a l l y , i . e . t o update a l p h a "memory,.at a l l . The same r a t i o n a l e h o l d s f o r beta memory, o n l y i t s l a g time i s much l o n g e r because i t i s more s l o w l y changed (by secondary s e l e c t i o n ) v i a changes i n a l p h a memory. Because a d a p t a b i l i t y ( b e t a memory) changes more s l o w l y than a daptedness, t h i s means t h a t e v o l u t i o n a r y p a t t e r n s d e t e r m i n e d by the way a d a p t a b i l i t y changes a r e n e c e s s a r i l y of a l o n g e r time s c a l e t h a n those p a t t e r n s based on changes i n adaptedness. I t i s i n t e r e s t i n g t o r e a l i z e t h a t the be t a genes, s t o r i n g f a v o r a b l e p a t t e r n s of g e n e t i c v a r i a t i o n p r o d u c t i o n , a r e r e a l l y a p o p u l a t i o n - l e v e l memory. Edstrom (1975) has d e s c r i b e d an i n g e n i o u s model of e v o l u t i o n i n which he, t o o , p o s t u l a t e s the e x i s t e n c e of a p o p u l a t i o n - l e v e l memory i n the genome. In h i s model the , second g e n e t i c memory i s a sample of a l l e l e f r e q u e n c i e s i n the p o p u l a t i o n , o b t a i n e d by a c e n s u s i n g p r o c e s s 89 made p o s s i b l e by s e x u a l r e p r o d u c t i o n (see Edstrom 1975). T h i s memory i s used i n a d i f f e r e n t way: through gene c o n v e r s i o n , s e g r e g a t i o n r a t i o s are d i s t o r t e d s l i g h t l y i n f a v o r of r a r e a l l e l e s . T h i s would cause r a r e a l l e l e s t o i n c r e a s e much f a s t e r , and a t much lower c o s t , than would be p o s s i b l e by n a t u r a l s e l e c t i o n . Edstrom (1975) c a l c u l a t e s t h a t i t would take 9240 g e n e r a t i o n s , a t a p o s i t i v e s e l e c t i o n c o e f f i c i e n t of 0.01, t o i n c r e a s e the f r e q u e n c y of a r e c e s s i v e m u t a t i o n from 0.01 t o 0.1. A s e g r e g a t i o n r a t i o of 1.01 i n f a v o r of the r e c e s s i v e c o u l d produce the same r e s u l t i n o n l y 233 g e n e r a t i o n s , w i t h o u t the r e p r o d u c t i v e e x c e s s r e q u i r e d by n a t u r a l s e l e c t i o n . V a r i a t i o n P r o d u c t i o n and E v o l u t i o n a r y P a t t e r n s D e s p i t e e x p l i c i t r e c o g n i t i o n , . b y people such as L e v i n s and L a y z e r , of v a r i a t i o n p r o d u c t i o n as an a d a p t i v e system s u b j e c t t o s e l e c t i o n , t h e r e s t i l l seems t o be a r e l u c t a n c e t o o p e n l y d i s c u s s the i d e a i n the l i t e r a t u r e . I have ye t to see a d i s c u s s i o n about L a y z e r ' s a d j u s t a b l e v a r i a t i o n i d e a s , a l t h o u g h he made them c l e a r . Templeton (1981) c r i t i c i z e d L a y z e r ' s s e l e c t i o n mechanism and made no comment on the c e n t r a l d r i v e of L a y z e r ' s (1980) paper. A l t h o u g h c o n s i d e r a b l e a t t e n t i o n i s now b e i n g p a i d t o a d a p t a b i l i t y and adjustment of v a r i a t i o n i n t h e l i f e h i s t o r y and o p t i m a l f o r a g i n g l i t e r a t u r e ( K a plan and Cooper 1984; Lacey et a l . 1983; C r a n d a l l and S t e a r n s 1982; C a r a c o 1980), the importance of p a t t e r n s of v a r i a t i o n p r o d u c t i o n i n e v o l u t i o n has r e c e i v e d d i r e c t a t t e n t i o n o n l y by the e p i g e n e t i c i s t s (eg. Waddington 1957; Ho and Saunders 1979). But p r o c e s s e s of 90 v a r i a t i o n p r o d u c t i o n are s t a r t i n g t o come under g r e a t e r s c r u t i n y f o r t h e i r p o t e n t i a l r o l e i n d e t e r m i n i n g e v o l u t i o n a r y p a t t e r n s . The ' e f f e c t h y p o t h e s i s ' of Vrba (1980,1983) i s one e x p l a n a t i o n f o r ' t r e n d s ' , which are l o n g - t e r m d i r e c t i o n a l t e n d e n c i e s i n e v o l u t i o n (Vrba 1983).. I t s t a t e s t h a t t r e n d s may be u n s e l e c t e d ' e f f e c t s ' of c h a r a c t e r s and p r o c e s s e s w i t h i n s p e c i e s , r a t h e r than the r e s u l t of s e l e c t i o n and a d a p t a t i o n . T h i s i s based on a n o t i o n of secondary s e l e c t i o n , t h a t a d a p t a t i o n s d r i v e n by i n d i v i d u a l s e l e c t i o n may have i n c i d e n t a l e f f e c t s , and t h a t t h e s e e f f e c t s might i n f l u e n c e net s p e c i a t i o n r a t e (R) i n a m o n o p h y l e t i c group. My s t a n c e i s i n t e r m e d i a t e between the e f f e c t h y p o t h e s i s and s p e c i e s s e l e c t i o n (see S t a n l e y 1975,1979). A l t h o u g h Vrba r e f e r s t o second o r d e r s e l e c t i o n , she i s emphatic i n a l l o w i n g a d a p t a t i o n o n l y a t the ' i n d i v i d u a l ' l e v e l , and does not i n c l u d e the p o s s i b i l i t y of a more i n c l u s i v e a d a p t i v e system. My p o i n t i s p r e c i s e l y t h a t such an a d a p t i v e system might e x i s t . On the o t h e r hand, S t a n l e y ' s s p e c i e s s e l e c t i o n i s a form of group s e l e c t i o n , r a t h e r than a p r o c e s s of d i r e c t upward c a u s a t i o n by s e l e c t i o n on i n d i v i d u a l s , as I a d v o c a t e . Dover's (1982) concept of " m o l e c u l a r d r i v e " i s u n u s u a l i n t h a t i t s u g g e s t s p a t t e r n s based on v a r i a t i o n p r o d u c t i o n r a t h e r than on v a r i a t i o n l o s s , eg. s e l e c t i o n and d r i f t . " M o l e c u l a r d r i v e " r e f e r s t o the a c t i o n of a s e t of p r o c e s s e s i n c l u d i n g unequal c r o s s i n g o v e r , t r a n s p o s i t i o n , and gene c o n v e r s i o n , t h a t a r e c a p a b l e of moving a v a r i a n t repeat sequence i n t r a c h r o m o s o m a l l y , t o homologous chromosomes, and t o nonhomologous chromosomes (Lewin 1982). In a p a n m i c t i c s e x u a l 91 p o p u l a t i o n t h i s d i f f u s i o n of a v a r i a n t throughout the gene p o o l i s f a s t e r than the f i x a t i o n of a v a r i a n t w i t h i n a f a m i l y of •repeats. T h i s i m p l i e s t h a t " t h e r e i s i n each i n d i v i d u a l the same average r a t i o of o l d and new v a r i a n t s f o r a p a r t i c u l a r f a m i l y " (Dover 1982), and t h a t s e l e c t i o n w i l l not d i s c r i m i n a t e among i n d i v i d u a l s because they a r e a l l more or l e s s s i m i l a r . T h i s i s an e x p l a n a t i o n of the o b s e r v a t i o n t h a t v a r i a t i o n i n members of a repeat f a m i l y i s mo s t l y between s p e c i e s , and not w i t h i n s p e c i e s . I t a l s o l e d Dover to s p e c u l a t e on the p o s s i b i l i t y of " a c c i d e n t a l s p e c i a t i o n " due-to the c o h e s i v e d i v e r g e n c e of s u b p o p u l a t i o n s t o the p o i n t where the v i a b i l i t y of h y b r i d s might be a f f e c t e d . M o l e c u l a r d r i v e i s independent of s e l e c t i o n and d r i f t , and seems t o o p e r a t e on a l o n g e r time s c a l e than those two p r o c e s s e s . O l d Ideas The c o n c e p t u a l d i v i s i o n between t y p e s of genes i s not a r e c e n t i d e a . Dobzhansky (1970) w r i t e s "Lamprecht argued i n a s e r i e s of papers (summary i n Lamprecht 1964) t h a t t h e r e a re two c a t e g o r i e s of genes and m u t a t i o n s , some d i s t i n g u i s h i n g s p e c i e s and o t h e r s o n l y v a r i e t i e s . Bocher (1951) b e l i e v e d t h a t t h e r e a re two k i n d s of m u t a t i o n s , some r e s p o n s i b l e f o r a d a p t a t i o n t o the environment and o t h e r s f o r p r o g r e s s i v e e v o l u t i o n . " Bocher's dichotomy, i n p a r t i c u l a r , i s remarkably s i m i l a r t o t h a t of a l p h a and b e t a genes ( L a y z e r 1980), which I d e s c r i b e d . Dobzhansky c o n t i n u e s , "These views have very.few a d h e r e n t s a t p r e s e n t . " Perhaps these i d e a s s h o u l d be r e c o n s i d e r e d ! 92 SUMMARY 1. U n d i r e c t e d v a r i a t i o n p r o d u c t i o n by d e f i n i t i o n has no c o n n e c t i o n w i t h the s e l e c t i o n f o r c e s t o which the new v a r i a n t s w i l l be s u b j e c t e d , and u s u a l l y l o w e r s the immediate f i t n e s s of p a r e n t s . 2. G e n e t i c a d a p t a b i l i t y i s im p o r t a n t f o r m a i n t a i n i n g immediate f i t n e s s i n a cha n g i n g w o r l d , and i t r e q u i r e s the p r o d u c t i o n of g e n e t i c v a r i a n t s , so t h e r e i s an " a d a p t e d n e s s / a d a p t a b i 1 i t y " t r a d e o f f. 3. The b e s t a d a p t e d n e s s / a d a p t a b i 1 i t y compromise depends on a. e n v i r o n m e n t a l p a r a m e t e r s , i n c l u d i n g r a t e s of change and p r e d i c t a b i l i t y , and b. the time s c a l e over which the compromise s t r a t e g y i s o b s e r v e d . A l o n g time s c a l e of o b s e r v a t i o n f a v o r s more inves t m e n t i n a d a p t a b i l i t y . 4. Given the e x i s t e n c e , i n a p o p u l a t i o n , of h e r i t a b l e " v a r i a t i o n i n v a r i a t i o n p r o d u c t i o n p a t t e r n s " ( i . e . " m e t a v a r i a t i o n " ) , s e l e c t i o n can t a i l o r g e n e t i c a d a p t a b i l i t y . Many g e n e t i c elements a r e known t h a t modify p r o c e s s e s of g e n e t i c v a r i a t i o n p r o d u c t i o n . Random v a r i a t i o n i n the s e elements produces m e t a v a r i a t i o n . Secondary s e l e c t i o n , i n p a r t i c u l a r , can a c t on the s e m o d i f i e r s . Thus v a r i a t i o n p r o d u c t i o n a t the l e v e l of the genotype i s not n e c e s s a r i l y u n d i r e c t e d , or random. The q u e s t i o n i s r a i s e d of whether genomes might be o r g a n i z e d t o f a c i l i t a t e m o d i f i c a t i o n of g e n e t i c v a r i a t i o n p r o d u c t i o n . 93 5. We can expect e v o l u t i o n a r y p a t t e r n s t o be caused by p a t t e r n s i n v a r i a t i o n p r o d u c t i o n , as w e l l as the t r a d i t i o n a l l y emphasized p a t t e r n s i n v a r i a n t l o s s (e.g. s e l e c t i o n and d r i f t ) . Hypotheses can be f o r m u l a t e d on the b a s i s of a d a p t a b i l i t y and change, as w e l l as adaptedness and s t a t e of the environment. 6. The mechanism of secondary s e l e c t i o n , and the n o t i o n t h a t a p a r t of the genome i s i n v o l v e d i n r e g u l a t i n g g e n e t i c v a r i a t i o n p r o d u c t i o n , a re used t o b u i l d a p o s s i b l e e x p l a n a t i o n f o r the observed p a t t e r n s i n genome s i z e . 7. S e l e c t i o n changes a l l e l e f r e q u e n c i e s at m o d i f i e r l o c i much more s l o w l y than a t p r i m a r y l o c i . So changes i n a d a p t a b i l i t y occur more s l o w l y than changes i n adaptedness. Slow processes, might e x p l a i n , l o n g term e v o l u t i o n a r y p a t t e r n s b e t t e r than f a s t p r o c e s s e s and s p e c i a l c o n t i n g e n c i e s . 93a P a t t e r n e d p r o d u c t i o n of g e n e t i c v a r i a t i o n : c o n s i d e r i t , " . ..the main weakness of modern e v o l u t i o n a r y t h e o r y i s i t s l a c k of a f u l l y worked out t h e o r y of v a r i a t i o n , t h a t i s , of c a n d i t u r e f o r e v o l u t i o n . . . " (Medawar 1967) or d i s m i s s i t . " M u t a t i o n s . . . a r i s e r e g a r d l e s s of t h e i r a c t u a l or p o t e n t i a l u s e f u l n e s s . 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Gene c o n t r o l in eukaryotes and the c-value paradox: "excess" DNA as an impediment to t r a n s c r i p t i o n of coding sequences. J.MoLec.Evol. 9:73-104. 104 APPENDIX I. FITNESS, PERSISTENCE, AND TIME SCALES I am c o n v i n c e d t h a t not enough a t t e n t i o n has been p a i d t o the time s c a l e dependence of the r e s u l t s of s e l e c t i o n , and t h a t t h i s o v e r s i g h t i s the s o u r c e of an enormous amount of c o n f u s i o n . I w i l l t r y t o i l l u s t r a t e the q u a l i t a t i v e change i n the r e s u l t s of s e l e c t i o n w i t h time s c a l e , and f o l l o w i t w i t h an example of c o n f u s i o n a r i s i n g out of f a i l u r e t o d i s t i n g u i s h among d i f f e r e n t time s c a l e s . F i t n e s s i s d e f i n e d t o mean " t h a t or t h o s e p r o p e r t i e s r e l e v a n t t o s e l e c t i o n " , t o d e l i b e r a t e l y make " n a t u r a l s e l e c t i o n f a v o r s the f i t t e s t " a t r u i s m (Dawkins 1982). L o o k i n g at a p o p u l a t i o n i n the s h o r t term, say from one g e n e r a t i o n t o the n e x t , the o n l y phenomena we see a r e r e l a t i v e changes i n p r o p o r t i o n s of v a r i o u s c h a r a c t e r i s t i c s , and f i t n e s s g e t s d e f i n e d as the r e l a t i v e e f f e c t i v e r a t e of r e p r o d u c t i o n . I f one assumes t h a t i n our w o r l d the p a s s i n g of time i m p l i e s change, then over the l o n g e r term the a b i l i t y t o cope w i t h change, i . e . a d a p t a b i l i t y , becomes more i m p o r t a n t compared w i t h adaptedness t o the s t a t e of the environment at any one time ( e . g . r e l a t i v e r a t e of i n c r e a s e ) . U n l e s s a n y t h i n g t h a t c o n t r i b u t e s t o adaptedness i n c r e a s e s a d a p t a b i l i t y i n the same p r o p o r t i o n ( p l a i n l y not so, e.g. sex and no sex ) we w i l l need a d i f f e r e n t d e f i n i t i o n of f i t n e s s t o s a t i s f y the t r u i s m . D i f f e r e n t time s c a l e s produce d i f f e r e n t r e s u l t s of s e l e c t i o n , r e q u i r i n g a d i f f e r e n t d e f i n i t i o n of f i t n e s s . I n s t e a d of h a v i n g the word " f i t n e s s " be so m a l l e a b l e , and 1 0 5 t h e r e f o r e vague, as t o take on the meaning of whatever p r o p e r t i e s a re c o n v e n i e n t , i t i s p r o b a b l y b e t t e r t o l e a v e i t as the s h o r t time s c a l e n o t i o n of d i f f e r e n t i a l r e p r o d u c t i o n and adaptedness. Dawkins (1982) shows t h a t even w i t h t h i s c o n s t r a i n t the word " f i t n e s s " has a t l e a s t f i v e d i f f e r e n t d e f i n i t i o n s . For p r o p e r t i e s r e l e v a n t t o s e l e c t i o n on l o n g e r time s c a l e s the words " p e r s i s t e n c e " or " p e r s i s t a b i l i t y " c o u l d perhaps be used. C r a n d a l l , S t e a r n s and Dudman ( i n prep) r e c e n t l y c o n s t r u c t e d two computer models, and t e s t e d the worth of v a r i o u s d e f i n i t i o n s of f i t n e s s as p r e d i c t o r s of the outcome. The two models d i f f e r e d i n the s p a t i a l s c a l e i n which the w o r l d was viewed. The m i c r o s c o p i c model viewed the w o r l d as c o n s i s t i n g of a f i n i t e number of p a t c h e s , whereas the m a c r o s c o p i c w o r l d view was one of an i n f i n i t e number of p a t c h e s . In the l a t t e r model " p r o d u c t i v i t y " was the best p r e d i c t o r , whereas i n the m i c r o s c o p i c model the best p r e d i c t o r was "something l i k e a p e r s i s t e n c e " -- and the two measures were found not t o be the same even as the number of f i n i t e p a t c h e s was i n c r e a s e d w i t h o u t bound. T h i s i n d i c a t e d a q u a l i t a t i v e d i f f e r e n c e i n the two models, which t o my mind was embodied i n the p o s s i b i l i t y of e x t i n c t i o n i n the f i n i t e model. And, j u s t as a s p a t i a l s c a l e t h a t made e x t i n c t i o n a f a c t o r made " f i t n e s s " a " p e r s i s t e n c e " , I am c l a i m i n g t h a t a tempor a l s c a l e t h a t makes e x t i n c t i o n a f a c t o r w i l l make " f i t n e s s " a " p e r s i s t e n c e " . The r e s u l t s of n a t u r a l s e l e c t i o n and, i n consequence, the a p p r o p r i a t e p r o p e r t i e s t o be embodied i n " f i t n e s s " , are dependent on the time s c a l e over which the r e s u l t s a r e viewed. As an example of the c o n f u s i o n p o s s i b l e i f time s c a l e i s 106 not taken i n t o a c c o u n t , c o n s i d e r Lewontin's (1965) statement: " . . . t h e c o u r s e of e v o l u t i o n i s determined by a s i m i l a r m a x i m i z i n g p r i n c i p l e both w i t h i n and between p o p u l a t i o n s . W i t h i n p o p u l a t i o n s the r e s u l t of n a t u r a l s e l e c t i o n , by and l a r g e , i s t o change the f r e q u e n c y of genotypes t o maximize the i n t r a p o p u l a t i o n f i t n e s s . Between p o p u l a t i o n s i t i s the p r o b a b i l i t y of s u r v i v a l t h a t i s maximized and the net r e s u l t i s a compromise between these f o r c e s , the degree to which one or the o t h e r i s important depending upon the a u t e c o l o g y of the s p e c i e s . " The d i f f e r e n t " m a ximizing p r i n c i p l e s " t h a t Lewontin p e r c e i v e s a t d i f f e r e n t l e v e l s of o r g a n i z a t i o n a r e due not t o d i f f e r e n t g o a l s of n a t u r a l s e l e c t i o n , but t o the f a c t t h a t i n s w i t c h i n g from one l e v e l t o a n other Lewontin has changed the time s c a l e over which he views the r e s u l t s of n a t u r a l s e l e c t i o n . The two m a x i m i z i n g p r i n c i p l e s a r e r e a l l y j u s t the two s i d e s of the compromise on any l e v e l of s e l e c t i o n : " s h o r t term g a i n v e r s u s l o n g term p e r s i s t e n c e " . The " g a i n " i n the s h o r t term f o r a whole p o p u l a t i o n can be i n terms of average f i t n e s s (W), a b s o l u t e s i z e , or s i z e r e l a t i v e t o o t h e r p o p u l a t i o n s . But over a l o n g e r term what m a t t e r s i s not the h i s t o r y of the p o p u l a t i o n , i t s r e c o r d of s h o r t term g a i n s ( W , s i z e ) , but t h a t i t manages t o p e r s i s t . S i m i l a r l y , on a lower l e v e l , the s h o r t term g a i n s of a l i n e a g e w i t h i n a p o p u l a t i o n a r e i n a b s o l u t e numbers or p r o p o r t i o n of the p o p u l a t i o n . But i n the l o n g run what m a t t e r s i s not the number or r e l a t i v e number of o f f s p r i n g , but t h a t the number of o f f s p r i n g exceeds the number of d e a t h s -- t h a t the l i n e a g e p e r s i s t s . When l o o k i n g a t s e l e c t i o n w i t h i n p o p u l a t i o n s Lewontin c o n s i d e r e d o n l y s h o r t term g a i n , embodied i n the n o t i o n of f i t n e s s . He o v e r l o o k e d the f a c t t h a t i n the l o n g term the 1 07 genotypes and t r a i t s favored by selection within a population are those enhancing persistence or p r o b a b i l i t y of s u r v i v a l . On the population l e v e l Lewontin saw only the long term "maximization" of p r o b a b i l i t y of survival and not the short term population increases and other features that would be important in a population-level d e f i n i t i o n of " f i t n e s s " analogous to the " i n d i v i d u a l " , or within-population concept (W) . The results of natural selection d i f f e r depending on the time scale over which they are examined. They do not depend on the l e v e l of organization at which selection is being considered. "Fitness" belongs on a shorter time scale, "persistence" on the evolutionary one. . 1 0 8 APPENDIX II_ THE FUNCTIONAL HIERARCHY The word ' f i t n e s s ' i s i n t e n d e d t o r e f l e c t the p r o p e r t y ( i e s ) of phenotypes t h a t n a t u r a l s e l e c t i o n f a v o r s (Dawkins 1982). N a t u r a l s e l e c t i o n i s the net r e s u l t of many p r o c e s s e s at work i n a p o p u l a t i o n . Some p r o c e s s e s a r e slowe r than o t h e r s . A q u a l i t y advantageous w i t h r e s p e c t t o a slow p r o c e s s becomes im p o r t a n t over the l o n g e r term as t h a t p r o c e s s becomes an im p o r t a n t cause of change. Thus, time s c a l e d e t e r m i n e s what p r o c e s s e s can be i m p o r t a n t , and what p r o p e r t i e s w i l l be f a v o r e d by n a t u r a l s e l e c t i o n , so ' f i t n e s s ' s h o u l d be d e f i n e d time s c a l e d e p e n d e n t l y (see Appendix I ) . What are a l l the p r o p e r t i e s t h a t f i t n e s s p o t e n t i a l l y c o u l d embody? Can we somehow make a l i s t of p r o p e r t i e s i n o r d e r of t h e i r importance over l o n g e r and l o n g e r time s c a l e s ? Or, e q u i v a l e n t l y , can we d e s c r i b e how the r e s u l t s of n a t u r a l s e l e c t i o n change w i t h time s c a l e ? T h i s w i l l i n v o l v e b r e a k i n g out of the t r a d i t i o n a l h a b i t of c o n f i n i n g n a t u r a l s e l e c t i o n t o a time s c a l e of one g e n e r a t i o n , when the most i m p o r t a n t q u a l i t y i s r e l a t i v e e f f e c t i v e r e p r o d u c t i v e r a t e ( t h e u s u a l d e f i n i t i o n of f i t n e s s ) . The S e l f i s h I n d i v i d u a l L e t us f i r s t c o n s i d e r a time s c a l e s h o r t e r than one g e n e r a t i o n . An organism has c e r t a i n q u a l i t i e s t h a t e n able i t t o s u r v i v e t o m a t u r i t y as i t must do t o r e p r o d u c e . Note t h a t a phenotype c o u l d a r i s e t h a t i n v e s t s h i g h l y i n t h e s e q u a l i t i e s , 109 spending a l l of i t s e n e r g i e s on s e l f - m a i n t e n a n c e and l e a v i n g n o t h i n g f o r r e p r o d u c t i v e i n v e s t m e n t . R e p r o d u c t i o n always c o s t s an i n d i v i d u a l organism i n energy or r i s k , p r o b a b l y l o w e r i n g i t s i n d i v i d u a l s u r v i v a l r a t e . We g e n e r a l l y r e c o g n i z e t h a t such a s t r a t e g y would not be f a v o r e d by n a t u r a l s e l e c t i o n on the g e n e r a t i o n t o g e n e r a t i o n time s c a l e -- we expect a b a l a n c e i n investment between s e l f -maintenance and r e p r o d u c t i o n such t h a t a zygote c o n t r i b u t e s the g r e a t e s t number of z y g o t e s t o the next g e n e r a t i o n . Note t h a t i f we c o n s i d e r i n c r e a s i n g p r o p o r t i o n a l r e p r e s e n t a t i o n i n a p o p u l a t i o n t o be ' s u c c e s s ' , i . e . t o i n d i c a t e b e i n g ' s e l e c t e d ' , then on a wi t h i n - g e n e r a t i o n time s c a l e , the s t r a t e g y of p u t t i n g a l l e n e r g i e s i n t o s e l f - p r e s e r v a t i o n would appear to be f a v o r e d , s i n c e t h e s e s t r a t e g i s t s would comprise a g r e a t e r p r o p o r t i o n of the a d u l t p o p u l a t i o n than of the zygote p o p u l a t i o n . ' I n d i v i d u a l ' s e l e c t i o n i s a misnomer. I t i s not i n d i v i d u a l s t h a t are b e i n g s e l e c t e d , or s o r t e d o u t , but the genes they c,ar.ry from one g e n e r a t i o n t o the next ( c o n s i d e r H a m i l t o n ' s i n c l u s i v e f i t n e s s ) . The i n d i v i d u a l organisms do not even p e r s i s t , so how can they be s a i d t o be s e l e c t e d ? The e n t i t y t h a t p e r s i s t s , and can be viewed as b e i n g s e l e c t e d on t h a t time s c a l e i s the genotype, or s emi-conserved genotype. That i s Dawkins' (1976, 1982) b a s i c p o i n t . I f the i n d i v i d u a l i s a l l - i m p o r t a n t , why s h o u l d i t t a k e the r i s k and spend the energy t o reproduce? S e l e c t i o n of i n d i v i d u a l s i s w i t h i n a g e n e r a t i o n , and f a v o r s s t r a t e g i e s ( e . g . s e l f - m a i n t e n a n c e w i t h no r e p r o d u c t i o n ) t h a t a r e not f i t a c c o r d i n g t o our u s u a l t r a n s - g e n e r a t i o n view of 1 1 0 n a t u r a l s e l e c t i o n and d e f i n i t i o n of f i t n e s s . I c o u l d be c r i t i c i z e d f o r p l a y i n g a semantic game h e r e , or p a y i n g too much a t t e n t i o n t o words. L e t me emphasize t h a t the problem j_s one of s e m a n t i c s . I f we a r e g o i n g t o t a l k about the q u a l i t i e s t h a t make some phenotypes more or l e s s s u c c e s s f u l , then our d e f i n i t i o n of s u c c e s s i s c r i t i c a l . The S e l f i s h L i n e a g e On a l o n g e r - t h a n - u s u a l time s c a l e , i n a c h a n g i n g w o r l d , n a t u r a l s e l e c t i o n w i l l f a v o r p r o p e r t i e s i n v o l v e d i n m a i n t a i n i n g ( o n e - g e n e r a t i o n ) f i t n e s s . G e n e t i c a d a p t a b i l i t y becomes i m p o r t a n t , and i t r e q u i r e s the p r o d u c t i o n and maintenance of g e n e t i c v a r i a t i o n i n a p o p u l a t i o n . U n d i r e c t e d p r o d u c t i o n of g e n e t i c v a r i a n t s ' i m p l i e s the p r o d u c t i o n of l e s s f i t genotypes, and genotypes t h a t may be f i t t e r i n the f u t u r e ( i m p o r t a n t f o r a d a p t a b i l i t y ) may be l e s s f i t a t p r e s e n t . So a d a p t a b i l i t y i s a t odds w i t h immediate f i t n e s s , or "adaptedness", and by c h a n g i n g the time s c a l e over which we view the r e s u l t s of n a t u r a l s e l e c t i o n we have changed the q u a l i t i e s t h a t n a t u r a l s e l e c t i o n " f a v o r s " . A d a p t a b i l i t y i s now w o r t h some c o s t i n terms of immediate f i t n e s s . Note the c o n c u r r e n t change i n ' s e l e c t e d u n i t ' w i t h time s c a l e . W i t h i n a g e n e r a t i o n i t i s the i n d i v i d u a l . From g e n e r a t i o n t o g e n e r a t i o n i t i s the genotype. Over many g e n e r a t i o n s g e n e t i c v a r i a t i o n p r o d u c t i o n becomes a v i r t u e , and the s e l e c t e d u n i t i s something more i n c l u s i v e than the genotype -- the l a t t e r i s s a c r i f i c e d f o r v a r i a t i o n p r o d u c t i o n . I have c a l l e d t h i s u n i t the l i n e a g e , and over the l o n g term r t l o o k s s e l f i s h -- not the 111 genotype, and not the i n d i v i d u a l . Another S e l f i s h L e v e l ? We now have t h r e e d i f f e r e n t p r o p e r t i e s t h a t a d e f i n i t i o n of f i t n e s s c o u l d embody. In o r d e r of i n c r e a s i n g importance w i t h l o n g e r time s c a l e they a r e : s e l f - m a i n t e n a n c e , e f f e c t i v e r e p r o d u c t i o n r a t e , and v a r i a t i o n p r o d u c t i o n . The e f f e c t of i n c r e a s i n g time s c a l e i n cha n g i n g the p r o p e r t i e s t h a t n a t u r a l s e l e c t i o n f a v o r s i s not due t o time i t s e l f . I t i s the change i n an environment t h a t can tak e p l a c e over a l o n g e r time p e r i o d t h a t e x e r t s the s e l e c t i o n p r e s s u r e f a v o r i n g the a b i l i t y t o cope w i t h change ( a d a p t a b i l i t y ) , t h a t r e q u i r e s v a r i a t i o n p r o d u c t i o n . The ' f u n c t i o n ' of v a r i a t i o n p r o d u c t i o n i s t o p e r m i t g e n e t i c a d a p t a t i o n i n a changing environment. There i s one l a s t s t r a t e g y t h a t I would l i k e t o c o n s i d e r . I f the environment i s one of v a r y i n g r a t e s and/or d i r e c t i o n of change, i t might be " u s e f u l " t o v a r y the fr e q u e n c y and k i n d of v a r i a n t p r o d u c t i o n ( i . e . t o produce m e t a v a r i a t i o n ) . That way, i f the v a r i a n t s produced by one l i n e a g e were r a r e l y s u i t e d t o the way the environment was c h a n g i n g , a l i n e a g e w i t h a more s u c c e s s f u l scheme would b e g i n t o predominate. The more i n c l u s i v e u n i t c o n s i s t i n g of the s e l i n e a g e s would t h e r e b y become more a d a p t a b l e t o the c u r r e n t p a t t e r n of e n v i r o n m e n t a l change. I t h i n k t h a t the s p e c i e s c o r r e s p o n d s t o t h i s more i n c l u s i v e u n i t , s i n c e the member p o p u l a t i o n s and l i n e a g e s of a s p e c i e s are g e n e r a l l y c o n s i d e r e d t o share the many mechanisms by which v a r i a n t p r o d u c t i o n can be m o d i f i e d . These i n c l u d e b r e e d i n g s t r u c t u r e , a s s o r t a t i v e n e s s of m a t i n g , and d i s p e r s a l t e n d e n c i e s . Table 4. Properties required for persistence under various environmental conditions. Environmental Persistence-related P e r s i s t i n g Conditions Properties E n t i t y Comment CONSTANT over time and space d u r a b i l i t y and self-maintenance (phenotypic f l e x i b i l i t y ) i n d i v i d u a l The i n d i v i d u a l i s vulnerable to c e r t a i n destructive forces and lack of supplies for metabolism. CONSTANT over time and heterogenous i n space reproduction genotype Since i n d i v i d u a l s occupy d i f f e r e n t locations i n space, reproduction creates " s p a t i a l refuges" for the genotype. CHANGING over time and homogeneous in space v a r i a t i o n lineage Without s p a t i a l refuges, a genotype w i l l go ex t i n c t . Within a lineage, only the variant genotypes that are t o l e r a n t to the change w i l l p e r s i s t . CHANGING i n rate and/or d i r e c t i o n of change metavariation species Metavariation i n e f f e c t explores d i f f e r e n t v a r i a t i o n production schemes f o r the one best suited to the p a r t i c u l a r kind of environmental change. 113 The environments and s t r a t e g i e s d e s c r i b e d above are summarized i n Table 4. Note t h a t h i g h e r l e v e l s t r a t e g i e s are r e q u i r e d f o r p e r s i s t e n c e i n s u c c e s s i v e l y more c o m p l i c a t e d e n v i r o n m e n t s , which r o u g h l y c o r r e s p o n d to l o n g e r and l o n g e r time s c a l e s . In more c o m p l i c a t e d e n v i r o n m e n t s , where the p e r s i s t e n c e of u n i t s a t one l e v e l of o r g a n i z a t i o n becomes i m p o s s i b l e , a k i n d of p e r s i s t e n c e i s o n l y p o s s i b l e by moving one l e v e l of o r g a n i z a t i o n h i g h e r , to the system t h a t g e n e r a t e s the ephemeral u n i t s a t the l e v e l below. The Ex i s t e n t i a l Game I f i n d i t c o n c e p t u a l l y u s e f u l t o look a t e v o l u t i o n as a problem of o b s e r v a t i o n . We observe changes i n the l i v i n g forms e x i s t e n t from one p o i n t i n time t o a n o t h e r . Some p r e v i o u s l y e x i s t i n g forms might be a b s e n t , or changed. Some might be new. (Note t h a t these c a t e g o r i e s are h i g h l y dependent on our d e f i n i t i o n s of these "forms".) The t h i n g s we see a t any time 1. c o u l d be c o n s t a n t l y r e - c r e a t e d by the a b i o t i c e nvironment, or 2. c o u l d have come i n t o b e i n g i n the more d i s t a n t past and have some q u a l i t y p e r m i t t i n g PERSISTENCE. In the case of l i v i n g t h i n g s , because of t h e i r c o m p l e x i t y and h i g h degree of o r g a n i z a t i o n , we can r u l e out ( 1 ) . P e r s i s t e n c e -o r i e n t e d p r o p e r t i e s imbue l i v i n g systems w i t h i n t e r n a l t e l e o l o g y (see A y a l a 1968). We do not see those forms w i t h l e s s or no ' p e r s i s t a b i l i t y ' . Of the t h i n g s we do see, t h e i r purpose seems t o be t o p e r s i s t . T h i s j u s t i f i e s S l o b o d k i n ' s m e t a p h o r i c a l d e s c r i p t i o n of e v o l u t i o n as an e x i s t e n t i a l game among " p l a y e r s " 1 1 4 w i t h v a r i o u s p e r s i s t e n c e - o r i e n t e d p r o p e r t i e s , or " s t r a t e g i e s " . U n f o r t u n a t e l y , S l o b o d k i n was not c l e a r about who the p l a y e r s a r e , and he mixed examples of i n d i v i d u a l and p o p u l a t i o n l e v e l c o n s i d e r a t i o n s . The p r e s e n t approach makes i t c l e a r t h a t who the p l a y e r s a r e i s determined by what s t r a t e g i e s a re a l l o w e d , i . e . what the r u l e s of the e x i s t e n t i a l game a r e . Each l e v e l of s t r a t e g y i s a way of keeping a more i n c l u s i v e , l o n g e r - l i v e d " p l a y e r " i n the " e x i s t e n t i a l game". T a b l e 4 g i v e s the " p l a y e r s " c o r r e s p o n d i n g t o v a r i o u s b a s i c s t r a t e g i e s . The F u n c t i o n a l H i e r a r c h y I t i s c l e a r t h a t the p e r s i s t e n c e - o r i e n t e d s t r a t e g i e s of Table 4 a r e 'n e s t e d ' . E f f e c t i v e r e p r o d u c t i o n r a t e i s dependent on the 'lower' s t r a t e g y , s e l f - m a i n t e n a n c e ( s u r v i v a l of the i n d i v i d u a l ) as w e l l as f e c u n d i t y . But s e l f - m a i n t e n a n c e does not r e q u i r e r e p r o d u c t i o n . L i k e w i s e , v a r i a t i o n p r o d u c t i o n and a d a p t a b i l i t y a r e s u p e r f l u o u s i f they c o s t e x t i n c t i o n i n the s h o r t term. The p e r s i s t e n c e - o r i e n t e d s t r a t e g i e s of T a b l e 4 can be r e a r r a n g e d i n t o the h i e r a r c h i c a l c o n t r o l system or f u n c t i o n a l  h i e r a r c h y p o r t r a y e d i n F i g u r e 6. A l t h o u g h i t i s common t o r e c o g n i z e a h i e r a r c h i c a l o r g a n i z a t i o n of b i o l o g y , i t i s u s u a l l y a s t r u c t u r a l h i e r a r c h y t h a t i s d e s c r i b e d ( m o l e c u l e s , c e l l s , t i s s u e s , o r g a n s , organisms, p o p u l a t i o n s , e c o s y s t e m s ) , not a f u n c t i o n a l one. T h i s i s awkward i n view of the f a c t t h a t e v o l u t i o n a r y e x p l a n a t i o n s a r e i n terms of f u n c t i o n . O t h e r s have suggested r e o r g a n i z i n g b i o l o g y around c a t e g o r i e s based on f u n c t i o n r a t h e r than s t r u c t u r e . Dawkins (1978) s u g g e s t e d " r e p l i c a t o r " as a g e n e r a l term f o r a " u n i t of <D c O C L (/) <D s-S-<D s o VARIATION REPRODUCTION METAVARIATION NEXT TIME P e r s i s t i n g ' U n i t ' S P E C I E S VARIATION NEXT TIME LINEAGE REPRODUCTION NEXT TIME GENOTYPE NUMBERS' PHENOTYPES NUMBERS NEXT TIME I N D I V I DUAL ^ M a i n t e n a n c e o f numbers ( s h o r t t e r m ) r e q u i r e s m a i n t e n a n c e o f r e p r o d u c t i v e f i t n e s s ( l o n g e r t e r m ) , F i g u r e 6. A h i e r a r c h i c a l c o n t r o l s y s t e m o f b i o l o g i c a l p e r s i s t e n c e - o r i e n t e d s t r a t e g i e s . 1 1 6 s e l e c t i o n " . H u l l (1980) t h i n k s t h a t the p a i r of terms " r e p l i c a t o r " and " i n t e r a c t o r " a re more a p p r o p r i a t e . These terms stem d i r e c t l y from the u s u a l '""one-generation time s c a l e d e s c r i p t i o n of the mechanism of n a t u r a l s e l e c t i o n . They o v e r -emphasize r e p r o d u c t i o n , and v a r i a b i l i t y i s c o n s i d e r e d l i t t l e more than s l o p from l e s s - t h a n - p e r f e c t r e p l i c a t i o n . G h i s e l i n (1974) a l s o s u g g e s t s t h a t b i o l o g i c a l c a t e g o r i e s be 'define d i n terms of the causes of e v o l u t i o n , and s u g g e s t s t h a t " T h i s i s one of the main reasons why the u s u a l f o r m u l a t i o n of the b i o l o g i c a l s p e c i e s d e f i n i t i o n i s so a t t r a c t i v e . Gene f l o w and r e p r o d u c t i v e i s o l a t i o n o b v i o u s l y p r o f o u n d l y i n f l u e n c e the p r o p e r t i e s of organ i sms." A h i e r a r c h y of p h y s i o l o g i c a l response systems was d e s c r i b e d by Bateson (1963), and extended i n t o the e c o l o g i c a l realm of p o p u l a t i o n s and s p e c i e s by S l o b o d k i n (1964, 1968). I have added m e t a v a r i a t i o n as a l o g i c a l e x t e n s i o n . Thoday (1953) d e f i n e d f i t n e s s as s u r v i v a l ( p e r s i s t e n c e ) p r o b a b i l i t y , and i n h i s d i s c u s s i o n of the "components of f i t n e s s " he made s e v e r a l of the same p o i n t s I have made. To my knowledge, F i g u r e 6 i s the f i r s t g r a p h i c a l p o r t r a y a l of such a f u n c t i o n a l h i e r a r c h y . F i g u r e 6 p u t s the p r o c e s s of r e p r o d u c t i o n i n p e r s p e c t i v e . I t a l s o shows us a s c a l e of p r o c e s s e s of d e c r e a s i n g speeds as one moves up the h i e r a r c h y . H i e r a r c h y t h e o r y (Simon 1962, P a t t e e 1973) t e l l s us t o expect the f a s t e r p r o c e s s e s a t the bottom t o be more i m p o r t a n t i n s h o r t term p a t t e r n s , and the sl o w e r p r o c e s s e s a t the t o p t o be more i m p o r t a n t i n the l o n g term, e v o l u t i o n a r y p a t t e r n s . What t h i s i m p l i e s i s t h a t the l o g i c a l p l a c e t o l o o k f o r e x p l a n a t i o n of v e r y l o n g term p a t t e r n s l i k e 1 1 7 the mode of e v o l u t i o n (e.g. p u n c t u a t e d v s . g r a d u a l ) i s a t the m e t a v a r i a t i o n l e v e l . I n s t e a d , most c u r r e n t e x p l a n a t i o n s c o n s t r u e s p e c i a l s i t u a t i o n s i n which the f a s t p r o c e s s e s of d r i f t and s e l e c t i o n can be more or l e s s e f f e c t i v e . F i g u r e 6 a l s o i l l u s t r a t e s a d u a l i t y : the s l o w e r p r o c e s s e s i m p o r t a n t i n the l o n g e r terms c o r r e s p o n d to s u c c e s s i v e l y more i n c l u s i v e " u n i t s of s e l e c t i o n " . So t a l k i n g about e v o l u t i o n , over l o n g e r time s c a l e s i s the same as t a l k i n g about " s e l e c t i o n " of more i n c l u s i v e " u n i t s " , and v i c e - v e r s a . (See my d i s c u s s i o n of L ewontin's statement i n Appendix I.) F i t n e s s I t h i n k i t i s c o r r e c t t o assume t h a t i n e v o l u t i o n a r y b i o l o g y the d e s i r e d meaning of f i t n e s s i s "those q u a l i t i e s f a v o r e d by n a t u r a l s e l e c t i o n " . I t i s when t h i s n o t i o n i s t r a n s l a t e d i n t o something more e m p i r i c a l l y t r a c t a b l e , e.g. p h y s i o l o g i c a l v i g o r or e f f e c t i v e r e p r o d u c t i v e r a t e , t h a t the problems and a m b i g u i t i e s a r i s e . In my o p i n i o n at l e a s t some of t h i s c o n f u s i o n i s e x p l a i n e d by the f a c t t h a t d i f f e r e n t i n v e s t i g a t o r s have d i f f e r e n t p e r s p e c t i v e s and u n c o n s c i o u s l y adopt d i f f e r e n t time s c a l e s . That f a c t would a s s u r e t h a t the same concept " f i t n e s s " g i v e r i s e t o d i f f e r e n t e m p i r i c a l d e f i n i t i o n s . The d e f i n i t i o n s of f i t n e s s a r e so numerous t h a t i n any work i t must be s p e c i f i e d which d e f i n i t i o n p e r t a i n s . I recommend a g r e a t e r c o n c i o u s n e s s of the time s c a l e b e i n g c o n s i d e r e d . I have shown above how the " f a v o r i t i s m " of n a t u r a l s e l e c t i o n changes w i t h the time s c a l e of o b s e r v a t i o n , and have g i v e n a range of 1 18 s t r a t e g i e s or p r o p e r t i e s that are d i f f e r e n t i a l l y emphasized by d i f f e r e n t time s c a l e s . On the longest of time s c a l e s , metavariation becomes a valuable s t r a t e g y . 1 19 APPENDIX I I I A COMPUTER MODEL FOR COMPARING  VARIATION PRODUCTION STRATEGIES IN VARIOUS ENVIRONMENTS T h i s computer program i s w r i t t e n as an e x p l o r a t o r y e v o l u t i o n a r y "game". The " p l a y e r s " a r e a s e x u a l l y r e p r o d u c i n g p o p u l a t i o n s w i t h d i f f e r e n t v a r i a t i o n p r o d u c t i o n " s t r a t e g i e s " , l i v i n g i n a r b i t r a r i l y s p e c i f i e d , o n e - d i m e n s i o n a l e n v i r o n m e n t s . The s t r a t e g y of each p l a y e r i s f i x e d f o r a g i v e n run -- t h i s program cannot compare the v i r t u e s and c o s t s of a d j u s t a b l e and f i x e d v a r i a t i o n . I t can compare the c o s t s and b e n e f i t s of d i f f e r e n t f i x e d v a r i a t i o n p r o d u c t i o n s t r a t e g i e s . I n the f o l l o w i n g d e s c r i p t i o n , v a r i a b l e names are p r i n t e d i n c a p i t a l l e t t e r s . ( I n the a c t u a l program code they a re lower case.) Var i a t i o n P r o d u c t i o n There a r e two p o s s i b l e components t o a v a r i a t i o n p r o d u c t i o n s t r a t e g y . One i s the p r o p o r t i o n of o f f s p r i n g t h a t a r e v a r i a n t . The o t h e r i s the d i s t r i b u t i o n of v a r i a n t o f f s p r i n g phenotypes. I t was d e c i d e d t o f i x the p r o p o r t i o n of v a r i a n t o f f s p r i n g a r b i t r a r i l y ( at two t h i r d s ) and v a r y o n l y the o f f s p r i n g d i s t r i b u t i o n s . The l a t t e r a r e s y m m e t r i c a l ( u n d i r e c t e d ) , b i m o d a l , and v a r y o n l y i n the d e v i a t i o n of the v a r i a n t o f f s p r i n g from the p a r e n t a l phenotype. The p a r t i c u l a r d e v i a t i o n c h a r a c t e r i s t i c of a g i v e n p l a y e r w i l l be r e f e r r e d t o as i t s " s t e p - s i z e " . F i g u r e 8 shows a segment of a p o p u l a t i o n b e f o r e ( a ) , and a f t e r (b) 120 P H E N O T Y P E ( p ) F i g u r e 7. R e p r o d u c t i o n of the p o r t i o n of the p o p u l a t i o n t h a t has a phenotype of '25'. T h i s p o p u l a t i o n has a s t e p - s i z e of 6. The o f f s p r i n g w i t h phenotype '31' w i l l d i e w i t h o u t r e p r o d u c i n g i f the environment remains the same. 121 r e p r o d u c t i o n . V a r i a t i o n p r o d u c t i o n s t r a t e g i e s were m o d e l l e d i n t h i s manner because of the p o t e n t i a l f o r s t u d y i n g what the i d e a l o f f s p r i n g d i s t r i b u t i o n s h o u l d be. I t s h o u l d be a composite of s e v e r a l s t e p - s i z e s dependent on the p r o b a b i l i t i e s of o c c u r r e n c e of the e n v i r o n m e n t a l c o n d i t i o n s f o r which each i s o p t i m a l . The work of James (1959) and o t h e r s showed t h a t the d i s t r i b u t i o n of l e t h a l i t y of e f f e c t s of m u t a t i o n s i s b i m o d a l . One mode i s t h a t of s l i g h t l y d e l e t e r i o u s , n e u t r a l , and b e n e f i c i a l m u t a t i o n s . The o t h e r mode i s of v e r y d e l e t e r i o u s and l e t h a l m u t a t i o n s . The m o d e l l e d v a r i a t i o n p r o d u c t i o n s t r a t e g y g i v e s a r e a s o n a b l e a p p r o x i m a t i o n t o t h i s d i s t r i b u t i o n . The Environment The environment was m o d e l l e d as a s y m m e t r i c a l f i t n e s s f u n c t i o n . The form of the a d a p t i v e peak (PFORM) can be s e t as t r i a n g u l a r (LINEAR) or PARABOLIC. The b r e a d t h of the peak i s d e t e r m i n e d by the v a r i a b l e TOLRAD ( " t o l e r a n c e r a d i u s " ) , which i s the d i s t a n c e i n " p h e n o t y p i c u n i t s " from the o p t i m a l phenotype t o the n e a r e s t phenotype w i t h z e r o f i t n e s s . N arrowing the b r e a d t h of the peak by d i m i n i s h i n g TOLRAD i n c r e a s e s the immediate c o s t s of v a r i a t i o n p r o d u c t i o n . The a d a p t i v e PEAK can be moved anywhere over the p e r m i s s i b l e range of 0 t o 100 p h e n o t y p i c u n i t s . Any r e l a t i o n s h i p between PEAK and TIME can be s p e c i f i e d . The environment has a c a r r y i n g c a p a c i t y (KK) which may (ONEPOP:=1) or may not be shared by the p o p u l a t i o n s i n a g i v e n r u n . Dynamics Any i n i t i a l f r e q u e n c y d i s t r i b u t i o n may be s p e c i f i e d f o r a 122 p o p u l a t i o n , e i t h e r by e n t e r i n g i t anew, or by r e f e r r i n g t o a p r e v i o u s l y s t o r e d d i s t r i b u t i o n . R e p r o d u c t i o n o c c u r s a t the s t a r t of e v e r y ( d i s c r e t e ) g e n e r a t i o n . As the a d a p t i v e peak moves, i n d i v i d u a l s of a g i v e n phenotype may e x p e r i e n c e a v a r i e t y of d i f f e r e n t f i t n e s s e s d u r i n g a g e n e r a t i o n . For s i m p l i c i t y , these c u m u l a t i v e e f f e c t s were i g n o r e d . The c o n t r i b u t i o n of a phenotype t o the next g e n e r a t i o n ( s u r v i v a l * f e c u n d i t y ) was determined o n l y by the v a l u e of the f i t n e s s f u n c t i o n a t the time of r e p r o d u c t i o n . F i t n e s s i s a f u n c t i o n o n l y of phenotype, and not of v a r i a t i o n p r o d u c t i o n scheme. Phenotypes o u t s i d e the a d a p t i v e peak d i e w i t h o u t l e a v i n g progeny. Phenotypes underneath the peak reproduce as p r e s c r i b e d by the f i t n e s s f u n c t i o n and the s i z e of the p o p u l a t i o n ( s ) r e l a t i v e t o the c a r r y i n g c a p a c i t y . The number of g e n e r a t i o n s t o be run can be s p e c i f i e d . Output The program r e q u e s t s a run d e s c r i p t i o n which becomes p a r t of the run summary p r i n t e d w i t h the o u t p u t . The a v a i l a b l e output d a t a a r e : 1. p o p u l a t i o n s i z e s over t i m e , 2. mean phenotypes of the p o p u l a t i o n s , and the o p t i m a l phenotype, over t i m e , 3. r e l a t i v e average f i t n e s s e s ( i . e . r e l a t i v e r a t e s of i n c r e a s e ) of the p o p u l a t i o n s over t i m e , and 4. mean s t e p - s i z e f o r a l l p o p u l a t i o n s over t i m e . The output f a c i l i t i e s a r e m o d u l a r i z e d so t h a t each of the four k i n d s of d a t a may be r e q u e s t e d s e p a r a t e l y . F u r t h e r m o r e , the model i s c o n s t r u c t e d f o r easy e x t e n s i o n of runs through 123 a d d i t i o n a l g e n e r a t i o n s . A f t e r such a c o n t i n u a t i o n has been run, the o r i g i n a l output and the a d d i t i o n a l o u t p u t can be re q u e s t e d s e p a r a t e l y , or t o g e t h e r . A l l output c o n s i s t s of a p a i r e d data t a b l e and p l o t . Program Language T h i s model i s a system of programs r u n n i n g on a PDP 11/45 a t the B i o s c i e n c e s Data C e n t r e , U n i v e r s i t y of B r i t i s h Columbia, under the B e r k e l e y UNIX V7 o p e r a t i n g system. I t i s w r i t t e n i n B e r k e l e y P a s c a l , the Bourne s h e l l , and Awk. See F i g u r e 13 f o r the program l i s t i n g s . Example Run Figu r e . 8 shows an example run of the computer model. L i n e s e n t e r e d by the user a re p r e f i x e d w i t h an a n g l e b r a c k e t ">". PEAKGAME was c a l l e d i n o r d e r t o a l t e r t he s p e c i f i c a t i o n s f o r PEAK, PFORM, TOLRAD or ONEPOP. O t h e r w i s e , the model c o u l d have been s t a r t e d by c a l l i n g GAME. The example run mo d e l l e d the e f f e c t s of t h r e e d i f f e r e n t v a r i a t i o n p r o d u c t i o n s t r a t e g i e s i n a c o n s t a n t l y c hanging environment. A l l p o p u l a t i o n s were s t a r t e d w i t h the same s i z e and phenotype d i s t r i b u t i o n . The output of the run i s p i c t u r e d i n F i g u r e s 9 through 12. At t h i s r a t e of e n v i r o n m e n t a l change, a g r e a t e r p r o p o r t i o n of the o f f s p r i n g of p o p u l a t i o n s w i t h g r e a t e r v a r i a t i o n p r o d u c t i o n l a n d o u t s i d e the a d a p t i v e peak. For t h e f i r s t f o u r g e n e r a t i o n s ( F i g u r e 11) r e l a t i v e f i t n e s s was n e g a t i v e l y c o r r e l a t e d w i t h v a r i a t i o n p r o d u c t i o n . The p o p u l a t i o n s w i t h g r e a t e r v a r i a t i o n p r o d u c t i o n t r a c k e d the environment more 124 c l o s e l y ( F i g u r e 10). A f t e r the f o u r t h g e n e r a t i o n , p o p u l a t i o n "X" f a r e d worse, as measured by p o p u l a t i o n s i z e ( F i g u r e 9) and r e l a t i v e mean f i t n e s s ( F i g u r e 11), than the p o p u l a t i o n s w i t h g r e a t e r v a r i a t i o n p r o d u c t i o n . By the end of the run i t i s apparent t h a t p o p u l a t i o n "+", w i t h an i n t e r m e d i a t e r a t e of v a r i a t i o n p r o d u c t i o n , has the best " a d a p t e d n e s s / a d a p t a b i l i t y " compromise f o r t h i s environment. >peakgame e n t e r PEAK f u n c t i o n of TIME, t o l r a d , {pform, onepop) i n P a s c a l : >peak:=30+2*time; to1rad:=10: onepop:=1; o f f to work... (The peak dynamics are now w r i t t e n i n t o the program, and the program i s c o m p i l e d and run. The program b e g i n s : ) T h i s run i s a new run i s a c o n t i n u a t i o n of the l a s t ( d a t a i n f i l e pd) i s a c o n t i n u a t i o n of some o t h e r run ( d a t a i n f i l e o t h e r than pd) uses a s t o r e d p l a y e r d i s t r i b u t i o n E n t e r 1,2,3 or 4: >4 Which f i l e has the s t o r e d p l a y e r d i s t r i b u t i o n ? >di s t 7 E n t e r number of p l a y e r s (< = 6) >3 E n t e r the s t e p - s i z e of p i a y e r h 1 : >2 p l a y e r #2: >4 p l a y e r #3: >7 Magic L i n e : peak:=30+2*time; tolrad:=10; onepop:=1; W r i t e d e s c r i p t i o n of t h i s run: >constant r a t e of change Number of g e n e r a t i o n s to be run? >20 p l a y e r s s t e p - s i z e 1 2 2 4 3 7 g e n e r a t i o n s : 0 to 20 = 20 d e s c r i p t i o n : c o n s t a n t r a t e of change Magic L i n e : peak:?30+2*time; tolrad:=10; onepop:=1; Does e v e r y t h i n g look O.K.? (y/n) >y ro ( p o p u l a t i o n s i z e s a r e p r i n t e d at the end of each g e n e r a t i o n ) > s t e p l o t 1 2 ( p r o d u c e s F i g u r e s 9 and 10, r e s p e c t i v e l y ) > f 1 t n e s s e s (produces F i g u r e 11) >meanstep (produces F i g u r e 12) END OF EXAMPLE RUN ro Ch p i a y e r s 1 2 3 genera t1ons : d e s c r i pt1 on: Mag i c L i ne: peak:=30+2*t1me po i nt s t e p - s i z e 2 4 7 0 to 20 c o n s t a n t 20 r a t e of change po 1 nt ECH0== > x : s t e p -s1zeof2 1 . 50.98 2 . 170.469 3 . 351.718 4 . 407.523 5 . 396.209 6 . 363.758 7 . 318.968 8 . 270.765 9 . 222.921 10. 177.914 1 1 . 136.999 12 . 101.896 13 . 72.994 14 . 50.594 15 . 33.968 16 . 22.209 17 . 14.128 18 . 8.802 19. 5. 369 20. 3 . 222 +:step -s1zeof4 1. 50.98 2 . 153.557 3 . 290.326 4 . 315.935 5 . 296.898 6 . 289.886 7 . 298.499 8 . 326.026 9 . 365.152 10. 4 14.908 1 1 . 463.65 12 . 513.459 13 . 552.504 14 . 588.925 15 . 614.211 16 . 639.855 17 . 653.794 18 . 670.905 19 . 679.037 20. 692.164 tolrad:=10; onepop:=1; p o i n t r t : s t e p - s i z e o f 7 700- ^ B 3 0 - .. 1. 50.98 2. 1 19. 126 3 . 181 . 851 5E0 4 . 169 . 067 5 . 141 . 474 6 . 126 . 307 490 7 . 1 19 . 704 8 . 120. 448 9 . 125. 323 10. 131 . 2 CD 450 1 1 . 134 .552 111 12. 136 .963 Ld 13. 136 .863 CD 3 SO 14 . 133 .451 •> 15 . 128 . 77 ZD 16 . 124 . 233 17 . 1 18 . 47 EBO 18. 1 1 1 .934 19. 105 .85 20. 100 .546 210 p o i n t x:20 xy p a i r s : s t e p - s i z e o f 2 p o i n t +:20 xy pa 1 r s : s t e p - s i z e o f 4 p o i n t r t : 2 0 xy p a i r s : s t e p - s i z e o f 7 140-70 > B- 10> IE • 14- IE-GENERATIONS IB-F i g u r e 9. S i m u l a t i o n model o u t p u t : p o p u l a t i o n s i z e s o v e r t i m e . Command: s t e p l o t 1. p l a y e r s s t e p - s i z e 1 2 2 4 3 7 g e n e r a t i o n s : 0 to 20 = 20 d e s c r i p t i o n : c o n s t a n t r a t e of change Magic L i n e : peak:=30+2*time: tolrad:=10; onepop:=1; EO-:DATA ECH0= p o i n t np: p o i n t + : s t e p - s i z e o f 4 po i nt x 30 1 . 30 1 32 2 . 31 064 2 . 34 3 . 32 396 3 . 36 4 . 33 702 4 . 38 5 . 35 339 5. 40 6. 37 216 6 . 42 7 . 39 224 7 . 44 8 . 41 233 8 . 46 9. 43 276 9. 48 10. 45 263 10. 50 1 1 . 47 27 1 1 . 52 12 . 49 228 12 . 54 13 . 51 219 13 . 56 14 . 53 169 14 . 58 15. 55 166 15 . 60 16. 57 126 16 . 62 17 . 59 129 17 . 64 18 . 61 094 18 . 66 19. 63 106 19 . 68 20. 65 078 20. step-sizeo£2 p o i n t r t : s t e p - s t z e o f 7 30 1 . 30 1 30 796 2 . 31 626 2 . 31 687 3. 33 44 1 3 . 32 345 4 . 35 244 4 . 33 268 5. 37 14 5. 34 603 6. 39 086 6 . 36 205 7. 41 128 7 . 37 961 8. 43 192 8 . 39 792 9. 45 21 1 9. 4 1 659 10. 47 186 10. 43 535 11. 49 201 1 1 . 45 421 12. 51 201 12 . 47 308 13. 53 149 13 . 49 205 14. 55 158 14 . 51 109 15. 57 186 15 . 53 026 16. 59 182 16. 54 948 17. 61 14 17 . 56 883 18. 63 156 18 . 58 823 19. 65 16 19. 60 773 20. 67 1 16 20. D -< U J L L J L D 18-1G-14 • la-ic-p o i n t np:20 xy p a i r s : p o i n t x:20 xy p a i r s : s t e p - s 1 z e o f 2 p o i n t + : 20 xy p a i r s : s t e p - s i z e o f 4 p o i n t r t : 2 0 xy p a i r s : s t e p - s i z e o f 7 Figure 10. Simulation model output: average phenotypes over time. Command: steplot 2. ro CO DATA ECHO==> p o i n t x p o i n t 1. 1 . po i nt r t : 1 . .698813 2 . 1 . 2 . .739878 3 . 1 . 3 . .80239 4 . 1 . 4 . .860688 5 . .940304 5 . .914389 6 . .851567 6 . .920377 7 . .777206 7 . .921259 8 . .735084 8 . .928987 9 . .702394 9 . .921351 10. .689079 10. .917736 1 1 . .671621 1 1 . .919174 12 . .665733 12 . .928652 13 . .65026 13. .914769 14 . .643744 14 . .925199 15 . .6276 18 15 . .926101 16 . .622576 16 . .93328 17 . .607 128 17 . .920733 18 . ..60267 18 . .934322 19 . .588731 19. .931877 1 . .900791 2 . .916362 3 . .939192 4 . .966579 5 . 1 . 6 . 1 . 7 . 1 . 8 . 1 . 9 . 1 . 10. 1 . 1 1 . 1 . 12 . 1 . 13. 1 . 14 . 1 . 15 . 1 . 16 . 1 . 17 . 1 . 18 . 1 . 19 . 1 . p o i n t x:19 xy p a l r s : p o i n t +:19 xy p a i r s : p o i n t r t : 1 9 xy p a i r s : LO CO Ld L i J LJJ LxJ i - o 0 - 9 0-B 0-7 0-B 0.3 .. 0 - 4 o-a D-l 0-1 0-0 B- IO- IE- 14- IB- IB" c!0. GENERATIONS F i g u r e 11. S i m u l a t i o n model o u t p u t : r e l a t i v e a v e r a g e f i t n e s s e s o v e r t i m e . Command: f i t n e s s e s . 5-0 DATA ECH0==> p o i n t x: 1 . 2 . 3 . 4 . 5 . 6 . 7 . 8 . 9 . 10. 1 1 . 12 . 13 . 14 . 15 . 16 . 17 . 18 . 19 . 20. 33333 0371 80837 65509 55906 55306 62176 74878 90206 05217 17636 27528 34708 38703 40977 4 175 4 1602 40195 38824 37088 p o i n t x:20 xy p a i r s : M 1—1 cn I CL U J I— LO 4-5 .. 4-0 .. 3-5 3-0 .. 2-5 -. 5-0 -. 1-5 1-0 . 0-5 .. \ M x x x x x-.x B • 10 • IE- 14- IB- IB. tlD-GENERATIONS F i g u r e 1 2 . S i m u l a t i o n model o u t p u t : a v e r a g e " s t e p - s i z e s " £ o v e r t i m e . Command: m e a n s t e p . ° F i g u r e 13. The s imu1 at ion model program 1i s t i ngs. PEAKGAME v7=yes echo e n t e r PEAK f u n c t i o n of TIME, t o l r a d , {pform, onepop) i n P a s c a l : ' >&2 r e a d mli ne echo o f f to work. . . ' >&2 c a t <<+ >sgame.p (* end of S h e l l , s t a r t of P a s c a l *) program stepgame ( 1 n p u t , o u t p u t , d a t a , s t o r e , r 1 , r 2 ) ; l a b e l 13; c o n s t f u z z = 1.Oe-10: minp= 0; maxp= 100: p l a y e r s = 6; (* c o n s t r a i n e d by p l o t symbols *) 11nelen= 128; b1ank= ' ' ; maxr= 0.5; kk = 1000; type s t r i n g = a r r a y t 1 • 1 i n e l e n ] of char; fname = a r r a y [ 1 . . 1 4 ] of char; var f l a g 1 , f l a g 2 : boolean; cho1ce,i,j,k,maxtIme,new,old,p,s,ss,maxss,playin,t1nc,t1me: i nteger; pform,1i n e a r , p a r a b o l i c,onepop,1owp,hi ghp,prevlow,prevh i gh: i n teger; k i ds,pav,peak,prop,r,1ambda,tolrad,totnum: rea 1 ; l e t t e r : c h a r ; s t e p : a r r a y [ 1 . . p i a y e r s ] of i n t e g e r ; 1 astnum.num,sum: a r r a y [ 1 . . p i a y e r s ] of r e a l ; pop: a r r a y [ 1 . .2 , 1 . . piayers,m1np..maxp] of r e a l ; l a b : a r r a y [ 1 . . p i a y e r s ] of char; e x t i n c t : a r r a y [ 1 . . p i a y e r s ] of boolean; b l u r b , f 1 : s t r i ng; d a t a , s t o r e , r 1 ,r2 : t e x t ; f n : fname; ttinclude " s t r i n g s . ! " (* ========== *) p r o c e d u r e s e t u p ( f : f n a m e ) ; v a r d o i t . i : i n t e g e r ; s p e c i a l : a r r a y ! 1 . . 6 ] of char; beg i n spec i a l [ 1 ] : = 'o';spec i a 1 [ 2 ] : = 'u';spec i a 1 [ 3] : = ' t' s p e c 1 a l [ 4 ] : = ' p ' ; s p e c i a l [ 5 ] : = 'u';spec i a l [ 6 ] : = ' t' doi t:= 0; t o f o r i : = 1 to 6 do If s p e c i a l [ i ] < > f [ 1 ] then d o i t : = do1t+ 1; i f d o i t > 0 then r e w r i t e ( o u t p u t , f ) ; wr i t e l n ( o u t p u t ) ; w r i t e l n ( o u t p u t , ' p l a y e r s s t e p - s i z e ' ) ; f o r 1: = 1 to p l a y i n do w r i t e l n ( o u t p u t , 1 . s t e p [ i ] ) ; wr 1 t e l n f o u t p u t , ' g e n e r a t i o n s : ',time:1,' to ',maxtime: 1, = ',maxt1 me-1ime: 1); w r 1 t e ( o u t p u t , ' d e s c r i p t i o n : ' ) ; p u t s t r ( o u t p u t , b l u r b , ' 1 ' ) ; w r 1 t e 1 n ( o u t p u t , ' M a g i c L i n e : ' ) ; w r 1 t e l n ( o u t p u t , ' $ml1ne ' ) ; w r i t e l n ( o u t p u t ) ; rewr i t e ( o u t p u t , ' / d e v / t t y ' ) ; end; (* ========== *) p r o c e d u r e s a v e p r o p ( s f n : f n a m e ) ; v a r s , p : i n t e g e r ; b e g i n rewrit°(store,5fn); w r 1 t e l n ( s t o r e , t i m e , p l a y 1 n ) ; f o r s:=1 to p l a y i n do w r 1 t e ( s t o r e , s t e p [ s ] ) ; w r 1 t e l n ( s t o r e ) ; f o r s:=1 to p l a y i n do beg i n f o r p:=minp to maxp do w r i t e 1 n ( s t o r e , p o p [ o l d , s , p ] : 1 : 5 ) : wr i t e l n ( s t o r e , 1 a s t n u m f s ] : 2 0 ) ; end; end; (* saveprop *) (* ========== *) p r o c e d u r e r e a d p r o p ( f n : f n a m e ; s w i t c h : 1 n t e g e r ) ; (* s w i t c h : 0 r e a d o n l y the p l a y e r d i s t r i b u t i o n *) (* 1 read p l a y e r d i s t r i b u t i o n and time and a p l a y e r s *) var t e m p : r e a l ; begi n r e s e t ( d a t a , f n ) ; i f not e o f ( d a t a ) then i f s w i t c h <>0 then b e g i n r e a d l n ( d a t a , t i m e , p l a y 1 n ) ; f o r s:=1 to p l a y i n do r e a d ( d a t a , s t e p [ s ] ) ; r e a d l n ( d a t a ) ; end e l s e b e g i n r e a d l n ( d a t a ) ; r e a d l n ( d a t a ) ; end e l s e wr1teln('Dummy The f i l e temp:= 0; f o r s:=1 to p l a y i n do beg i n i s empty. ' ) ; 00 ro f o r p:= m i np to If not r e a d l n ( d a t a , i f abs(temp-maxp do e o f ( d a t a ) then b e g i n r e a d l n ( d a t a , p o p [ o l d , s , p ] ) ; temp:= temp+ p o p [ o l d , s , p ] ; end e l s e wr 1 t e l n ( ' E r r o r . F i l e ran out at 1astnum[s]); 1 a s t n u m [ s ] ) > f u z z P= ' ,p): then temp:= 0; end; end; (* readprop beg i n w r 1 t e l n ( w r 1teln( wr1teln( end; E r r o r . P l a y e r temp= ',temp) lastnum[s]= t o t a l read i n does not match t h a t s t o r e d . ' ) ; 1astnumt s ] ) ; beg i n ( *'. i n i t i a l i z a t i ons *) time: = 0; pform:= 0; 1Inear:= O; onepop:= ( * m1i ne $mli ne old:= 1; new:= 2 ; totnum:= maxss:= 0; prevlow:= m i np; prevhigh:= maxp; p a r a b o l i c : 1 1; (* dummies, would p r o p e r l y make a TYPE * 0; (* 0 means they a r e independent subpopu1 a t i o n s *) a s s i g n s peak f u n c t i o n , form, and t o l e r a n c e r a d i u s , and det 0: whether p l a y e r s share c a r r y i n g c a p a c i t y kk *) f lag1 f lag2 f o r i = f a l s e ; = f a l s e ; =1 to 14 do f n [ 1 ] : blank; w r i t e l n ; w r 1 t e l n ( wr i t e l n ( wr i t e l n ( w r 1 t e l n ( w r 1 t e l n ( wr i te1n( wr i t e l n ; Th i s r u n ' ) ; 1 s a new run -- 1' ) i s a c o n t i n u a t i o n of the l a s t ( d ata i n f i l e pd) -- 2') i s a c o n t i n u a t i o n of some other run (data i n f i l e o t h e r than pd) -- 3 ) uses a s t o r e d p l a y e r d i s t r i b u t i o n -- 4 ) E n t e r 1,2,3 or 4: ' ) ; r e a d ( c h o i ce ) ; c a s e c h o i c e of 1: f l a g 2 : = t r u e ; LO CO 2: b e g i n f 1 [ 1 ] : = p'; f1 [ 2 ] : = ' c f ; f.lagl : = t r u e ; end; 3: b e g i n w r i t e l n ( ' E n t e r name of f i l e g e t s t r ( i n p u t , f 1 , 'w'); f l a g 1 : = t r u e ; end ; 4: b e g i n w r i t e l n ( ' W h i c h f i l e has the g e t s t r ( i nput, f 1 , ' w' );-f l a g 1 : = t r u e ; f1ag2:= t r u e ; end; end; where d a t a i s s t o r e d : ' ) ; s t o r e d p l a y e r d i s t r i b u t i o n ? (* f l a g l => i s not a new run, s t o r e d p l a y e r d i s t r i b u t i o n * (* f l a g 2 => need prompting f o r p l a y e r s and s t e p - s i z e * i f f l a g 2 then b e g i n w r i t e l n ( ' E n t e r number of p l a y e r s (<=6) ' ) : r e a d l n ; read(p1 a y i n ) ; w r i t e l n ( ' E n t e r the s t e p - s i z e o f ' ) ; f o r 1:=1 to p l a y i n do be g i n w r 1 t e l n ( ' p i a y e r #',1:1,':'); r e a d l n ; r e a d ( s t e p [ i ] ) ; end; end; o f o r j:=1 to p l a y i n do begi n l a s t n u m [ j ] : = 0; num[j ] := 0; sum[j]:= 0; f o r i:=1 t o 2 do f o r k:=minp to maxp do p o p [ i , j . k ] : = 0; end; 1 : = 1 ; w h i l e (f1[1]<>blank)and(f1[1]<>'"')and(1<=14) do beg i n f n [ i ] : = f 1 [ 1 ] ; i : = i + 1 ; end; 1f f l a g l then b e g i n i f f l a g 2 then readprop(fn,0) e l s e b e g i n r e a d p r o p ( f n , 1 ) ; „ r e w r i t e ( r 1 , ' r e s 1'); r e w r i t e ( r 2 , ' r e s 2 ' ) end; f o r s:=1 to p l a y i n do totnum:= totnum+ l a s t n u m [ s ] ; end e l s e b e g i n wr i t e l n ; w r 1 t e l n ( ' T h e i n i t i a l t o l e r a n c e range 1s between phenotypes wr i te1n; wr i t e l n( ' Enter : p l a y e r ft, phenotype, numbers ' ) ; w r i t e l n ( ' ( 0 f o r p l a y e r H when done)'): r e a d l n ; r e a d ( s , p , p r o p ); whi1e s<>0 do beg 1 n pop[o l d , s , p ] : = prop; (* i f any s,p i s used more totnum:= totnum+ prop; 1astnum[s]:= lastnum[s]+ prop; sum[s]:= sum[s]+ prop*p; r e a d l n ; r e a d ( s , p , p r o p ) ; end; end; 1f f l a g 2 then b e g i n r e w r i t e ( r 1 , ' r e s u l t s 1 ' ) ; r e w r 1 t e ( r 2 , ' r e s u l t s 2 ' ) ; end; w r 1 t e l n ; w r i t e l n ( Magic L i n e : ' ) ; w r 1 t e l n ( ' $mline ' ) ; w r 1 t e l n ( ' W r i t e d e s c r i p t i o n of t h i s r u n : ' ) ; r e a d l n : g e t s t r ( i n p u t . b l u r b . ' l ) ; write1n('Number of g e n e r a t i o n s to be r u n ? ' ) ; r e a d l n ; r e a d ( t i n c ) ; (* might not need the r e a d l n here *) maxtime:= t i m e + t i n c ; s e t u p ( ' / d e v / t t y ' ) ; w r i t e l n ( ' D o e s e v e r y t h i n g look O.K.? ( y / n ) ' ) ; r e a d l n ; r e a d ( 1 e t t e r ) ; i f l e t t e r = ' n ' then goto 13; s e t u p ( ' s e t u p ' ) ; l a b [ 1 ] : = x lab[4]:='1 wr1te1n(r1 wr i t e 1 n ( r 1 wr i t e l n ( r 1 w r 1 t e l n ( r 2 lab[2]:='+'; 1ab[3] lab[5]:='u'; l a b [ 6 ] i?l abel =on' ); ®>x 1 ab= "generat i o n s " @ylab="numbers" ' ) ; <al abel =on' ); , p e a k - t o l r a d : 1 , ' and ',peak+tolrad:1); an once, t o t a l s w i l l be wrong *) co cn wr 1 t e l n( r2 , '<s>xl ab= "phenotype" ' ); wr 1 t e l n( r2, '<»y 1 ab = "generat 1 ons" ' ) ; w r 1 t e l n ( r 2 . '@ysort' ); f o r i : = 1 to p l a y i n do (* u s e f u l f o r data echo o n l y -- doesn't appear on p l o t s *) begi n i f l a s t n u m [ i ] > 0 then e x t i n c t [ i ] : = f a l s e e l s e e x t i n c t [ 1 ] : = t r u e ; i f s t e p f i ] > m a x s s then tnaxss : = s t e p [ i ] ; wr i t e l n ( r 1 , @ p t 1 1 1 e = ' , 1 a b [ 1 ] , ' : s t e p - s i z e _ o f _ ' , s t e p f i]:1); w r i t e l n ( r 2 , ' @>pt i 11 e = ' , l a b [ 1 ] , ' : s t e p - s i z e _ o f _ ' , s t e p f i ] : 1 ) ; i f not f l a g l then begi n wri t e l n ( r 1 , l a b f 1 ] , t ime,' ',lastnumf1]:1:3); w r i t e l n ( r 2 , l a b f i ] , ( s u m f i ] / l a s t n u m [ i ] ) : 1 : 3 , ' ' ,t i m e ) : sumt1]:= 0; end; end; (* the p e r - g e n e r a t i o n s t u f f ================================================ *) w h i l e time<maxtime do beg i n $m1ine (* peak as a f u n c t i o n of time *) lowp:= round(peak-tolrad+O.5); highp:= round(peak+tolrad-O.5); i f lowp<minp then lowp:= minp; (* a l l o w s peak to s t a r t w i th p a r t of i t s *) i f highp>maxp then highp:= maxp; (* e n t i r e t o l e r a n c e range o u t s i d e minp-maxp *) i f prev1ow<lowp then lowp:= prevlow; i f p r e v h i g h > h i g h p then highp:= p r e v h i g h ; f o r s:=1 to p l a y i n do i f not e x t 1 n c t ( s ] then f o r p:= lowp t o highp do begi n i f p f o r m = p a r a b o l i c then lambda:= 1 - s q r ( ( p - p e a k ) / t o l r a d ) (* p a r a b o l i c f n of d i s t to peak *) e l s e lambda:= 1-abs(p-peak ) / t o l r a d ; (* f u n c t i o n of d i s t a n c e from peak *) i f lambda<0 then lambda:= 0; i f onepop=0 (* e f f e c t s of *) then kids:= p o p f o l d , s , p ] * 1ambda*(1+maxr*(1- 1 a s t n u m f s ] / k k ) ) / 3 (* independent crowding *) e l s e kids:= p o p f o l d , s , p ] * 1ambda*(1+maxr*(1 - totnum/kk))/3; (* j o i n t crowding *) ss:= s t e p [ s ] ; popfnew,s,p]:= poptnew,s.p]+ k i d s ; num[s]:= num[s]+ k i d s ; sum[s]:= sum[s]+ k i d s * p ; i f (p+ss)<=maxp then b e g i n pop[new,s,p+ss]:= poptnew,s,p+ss]+ k i d s ; num[s]:= num[s]+ k i d s ; sum[s]:= sum[s]+ k i d s * ( p + s s ) ; end; i f (p-ss)>=minp then begi n popfnew,s,p-ss]:= pop[new,s,p-ss]+ k i d s ; £J num[s]:= num[s]+ k i d s ; o> sum[s]:= sum[s]+ k 1 d s * ( p - s s ) ; end; p o p f o l d , s , p ] : = 0; prevlow:= rou n d ( p e a k - t o l r a d + 0 . 5 ) - maxss; i f prevlow<minp then prev1ow:=minp; prevhigh:= round(peak+tolrad-0.5)+ maxss; i f prevh1gh>maxp then prevhigh:=maxp; end; time:= time+ 1; (* ou t p u t and p l o t g e n e r a t i o n s t u f f . c l e a r sum and num *) w r i t e l n ( r 2 , 'n',peak:1:3,t ime); (* time i s number of g e n e r a t i o n s gone *) (* readout i s s t a t e at the end of time t h g e n e r a t i o n *) w r 1 t e l n ( o u t p u t ) ; w r i t e l n ( o u t p u t , ' *** '.time); totnum:= 0; f o r i:=1 to p l a y i n do beg 1 n w r i t e ( o u t p u t , n u m [ i ] : 1 : 3 , ' ) ; i f (num[i]=0) and (not e x t i n c t [ i ] ) then b e g l n w r i t e l n ( ' P l a y e r ' , i , ' has gone e x t i n c t . Time: '.time); ext i n e t [ i ] : = t r u e ; end; w r i t e l n ( r 1 , l a b [ i ] , t i m e , ' ',num[11:1:3); i f num[i]=0 then pav:=0 e l s e pav:= sum[i]/num[i]; wr 1 t e l n ( r 2 , 1 a b [ i ] , p a v : 1 : 3 , ' '.time); (* e x t i n c t p l a y e r s w i l l have phenotype z e r o *) totnum:= totnum+ num[i]; l a s t n u m [ i ] : = num[i]; num[i]:=0; sum[i ] :=0; end: old:= new; new:= 3 - o l d ; end; (* end whi1e * ) s a v e p r o p ( ' p d ' ) ; 13: end. + : end of P a s c a l , r e s t a r t of S h e l l p i sgame.p mv obj game game co — i AUXILIARY PROGRAMS ********** s t e p l o t par [par2 par3 ...] v7=yes : E x p l a n a t i o n of parameters: 1 p l o t s p o p u l a t i o n s i z e s v e r s u s g e n e r a t i o n s of the o r i g i n a l run 2 p l o t s average phenotypes over g e n e r a t i o n s f o r o r i g i n a l run 3 does 1 f o r c o n t i n u a t i o n run 4 does 2 f o r c o n t i n u a t i o n run 5 does 1 f o r o r i g i n a l and c o n t i n u a t i o n runs t o g e t h e r 6 does 2 f o r o r i g i n a l and c o n t i n u a t i o n runs t o g e t h e r P r i o r to a second c o n t i n u a t i o n run, and each subsequent c o n t i n u a t i o n run, the c o n t i n u a t i o n d a t a must be appended to the o r i g i n a l data by i s s u i n g the command "t a c k " , because o n l y one s e t of c o n t i n u a t i o n data 1s m a i n t a i n e d at any time. c a t r e s u l t s l > r l . p l o t c a t r e s u l t s 2 > r 2 . p l o t f o r do 1 i n c a s e $ i i n 1) 2) 3) 4) 5) ( c a t setup; q p l o t ( c a t s etup; q p l o t ( c a t s etup; q p l o t ( c a t s etup; q p l o t - j o i n r1 . p l o t ) - j o i n r 2 . p l o t ) wrap 42 wrap 42 grep -v <a res1 \ c a t >> r l . p l o t ( c a t s etup; q p l o t - j o i n r l . p l o t ) 6) grep -v @ res2 \ c a t >> r 2 . p l o t ( c a t setup; q p l o t - j o i n r 2 . p l o t ) *) echo $ i i s a wierd parameter e s a c - j o i n res2) | wrap 42 \ pr pr pr pr -3 -3 wrap 42 wrap 42 -3 -3 1 pr; l p r ; 1 pr; ; 1 pr; ; pr -3 pr l p r ; ; l p r ; ; c a t r e s u l t s l > r l . p l o t c a t r e s u l t s 2 > r 2 . p l o t done ********** f i t n e s s e s v7=yes : uses peakgame output f i l e r e s u l t s l to c a l c u l a t e and : p l o t r e l a t i v e f i t n e s s e s over time c a t <<+ > f 1 t . p i o t ipxl ab= "generat i ons" @y1ab="re 1 a t i v e mean f i t n e s s " P1abe1=on c o 00 ©join + awk - f f i t a w k . a r e s u l t s l >> f i t . p l o t q p l o t f i t . p l o t | wrap 42 f pr -3 J Ipr ********** meanstep v7=yes : uses peakgame output f i l e r e s u l t s l to c a l c u l a t e and p l o t the average s t e p s i z e f o r each g e n e r a t i o n . c a t <<+ >mstep.plot @>y 1 ab= "mean s t e p - s i z e " @xlab="generat i o n s " @ j o i n awk - f a v s t e p . a r e s u l t s l >>mstep.plot q p l o t m s t e p . p l o t / wrap 42 / pr -3 / l p r ********** f i t a w k . a BEGIN {last=1. ; sum=0. ; flag=0. ; maxf= 0.) NF==3. && $2 = l a s t { f o r ( i i n num) { p r o p [ i ] = num[1]/sum i f ( f l a g = 0 . && prev[1]=0.) fabs[1]= p r o p [ i ] / p r e v [ 1 } e l s e f a b s [ i ] = 0. i f ( f a b s [ i ] > m a x f ) maxf= f a b s t i ] p r e v f i ] = p r o p [ i ] } i f ( f l a g = 0 . ) f o r ( i i n f a b s ) p r i n t s y m [ i ] , l a s t - 1 . , f a b s [ i ] / m a x f maxf= 0. las t = $2 sum= 0. flag = 1. > NF==3. && $2==1ast {sym[$1]=$1; num[$1]=$3; sum += $3} END { f o r ( i i n num) { p r o p [ i ] = num[i]/sum i f ( f l a g = 0 . p r e v [ l ] = 0 . ) f a b s [ i ] = p r o p [ i ] / p r e v [ i ] e l s e f a b s f i]= 0. i f ( f a b s [ i ] > m a x f ) maxf= f a b s [ i ] p r e v [ i ] =prop[i] ) CO i f ( f l a g = 0 . ) f o r ( i i n f a b s ) p r i n t s y m [ i ] , l a s t - 1 . , f a b s [ i ] / m a x f to } ********** a v s t e p . a BEGIN ( f l a g = 0 . ) NF==1. { i f (1ndex($1,":") = 0.){ s= index($1,"=") s t e p [ s u b s t r ( $ 1 , s + 1 . . 1 . ) ] = s u b s t r ( $ 1 , 1 e n g t h ( $ 1 ) , 1 . ) > NF==3. && flag==0. < flag=1.; last=$2 } NF==3. SS $2 = l a s t { f o r ( i i n prod) sum+ = prod[1] p r i n t 1ast,sum/cnt cnt=0. sum=0. last=$2 } NF==3. &S $2 = = l a s t {sym[$1]=$1; prod[$1J=$3 * s t e p [ $ 1 ] ; cnt + = $3} END {for ( i i n prod) sum+= p r o d f l ] ; p r i n t l a s t , sum/cnt) ********** tack v7=yes :appends c o n t i n u a t i o n d a t a to o r i g i n a l run da t a , f o r a d d i t i o n a l : c o n t i n u a t i o n runs. g r e p -v @ res1 ] c a t >> r e s u l t s l g r e p -v @ res2 \ c a t >> r e s u l t s 2 

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