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The ancestral shape hypothesis: an evolutionary explanation for the occurrence of intervertebral disc… Plomp, Kimberly A; Viðarsdóttir, Una S; Weston, Darlene A; Dobney, Keith; Collard, Mark Apr 27, 2015

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RESEARCH ARTICLE Open AccessThe ancestral shape hypothesis: an evolutionaryexplanation for the occurrence of intervertebralsbringing the tools of evolutionary biology to bear on problems in medicine and public health.Plomp et al. BMC Evolutionary Biology  (2015) 15:68 DOI 10.1186/s12862-015-0336-y5Department of Archaeology, University of Aberdeen, Aberdeen, UKFull list of author information is available at the end of the articleKeywords: Back pain, Disc herniation, Vertebral shape, Bipedalism, Geometric morphometrics, Schmorl’s nodes* Correspondence: mcollard@sfu.ca1Human Evolutionary Studies Program and Department of Archaeology,Simon Fraser University, Burnaby, BC, CanadaKimberly A Plomp1, Una Strand Viðarsdóttir2, Darlene A Weston3,4, Keith Dobney5 and Mark Collard1,5*AbstractBackground: Recent studies suggest there is a relationship between intervertebral disc herniation and vertebral shape.The nature of this relationship is unclear, however. Humans are more commonly afflicted with spinal disease than arenon-human primates and one suggested explanation for this is the stress placed on the spine by bipedalism. With thisin mind, we carried out a study of human, chimpanzee, and orangutan vertebrae to examine the links betweenvertebral shape, locomotion, and Schmorl’s nodes, which are bony indicators of vertical intervertebral discherniation. We tested the hypothesis that vertical disc herniation preferentially affects individuals with vertebrae thatare towards the ancestral end of the range of shape variation within Homo sapiens and therefore are less well adaptedfor bipedalism.Results: The study employed geometric morphometric techniques. Two-dimensional landmarks were used tocapture the shapes of the superior aspect of the body and posterior elements of the last thoracic and first lumbarvertebrae of chimpanzees, orangutans, and humans with and without Schmorl’s nodes. These data weresubjected to multivariate statistical analyses.Canonical Variates Analysis indicated that the last thoracic and first lumbar vertebrae of healthy humans,chimpanzees, and orangutans can be distinguished from each other (p<0.028), but vertebrae of pathologicalhumans and chimpanzees cannot (p>0.4590). The Procrustes distance between pathological humans andchimpanzees was found to be smaller than the one between pathological and healthy humans. This was thecase for both vertebrae. Pair-wise MANOVAs of Principal Component scores for both the thoracic and lumbarvertebrae found significant differences between all pairs of taxa (p<0.029), except pathological humans vschimpanzees (p>0.367). Together, these results suggest that human vertebrae with Schmorl’s nodes are closer inshape to chimpanzee vertebrae than are healthy human vertebrae.Conclusions: The results support the hypothesis that intervertebral disc herniation preferentially affects individualswith vertebrae that are towards the ancestral end of the range of shape variation within H. sapiens and therefore areless well adapted for bipedalism. This finding not only has clinical implications but also illustrates the benefits ofdisc herniation in human© 2015 Plomp et al.; licensee BioMed Central. This is an Open Access article distributed under the terms of the CreativeCommons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, andreproduction in any medium, provided the original work is properly credited. The Creative Commons Public DomainDedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article,unless otherwise stated.Plomp et al. BMC Evolutionary Biology  (2015) 15:68 Page 2 of 10BackgroundBack pain is an important health issue. It has been esti-mated that 22-65% of people will experience back painat some point in their lives [1], making it one of themost common health problems [2]. Back pain is alsoone of the most serious health problems. Recent worksuggests that it is the greatest contributor to disabilityon a global scale [3]. The prevalence of back pain and thefrequency with which it causes disability mean that it canimpose a substantial economic burden on countries [4].For example, the annual cost of back pain in the UK hasbeen estimated to exceed £1.5 billion per year [5]. Giventhe importance of back pain, there is a need for greaterunderstanding of the underlying factors that cause it.Intervertebral disc herniation is a widespread but poorlyunderstood cause of back pain [6]. It is defined as a pro-lapse of the gelatinous substance inside the disc, thenucleus pulposus, either horizontally through the fibrousouter disc layers or vertically into the vertebral endplate[6]. Intervertebral disc herniation is frequent amongadults, with recent studies suggesting that prevalencerates range from 20% to 78%, depending on population[7-9]. Numerous potential causes of intervertebral discherniation have been proposed, including genetic pre-disposition, disc composition, developmental issues,and physical strain or trauma [10-15], but the aetiologyand pathogenesis of the condition remain unclear [16].Recently, a number of studies have suggested that ver-tebral shape may affect the propensity to experienceintervertebral disc herniation. Pfirrmann and Resnick[17] found that Schmorl’s nodes were associated with aflat vertebral endplate as opposed to the more commonconcave endplate in a sample of cadavers. Schmorl’snodes are depressions on the upper and lower surfacesof the vertebral body that result from vertical intervertebraldisc herniation [18]. They can be identified with theuse of medical imaging technology [19,20] or on drybone [21-23]. Harrington et al. [24] obtained similarresults to Pfirrmann and Resnick [23]. They found thatthe size and shape of the vertebral body was associatedwith lower lumbar intervertebral disc herniation in alarge sample of clinical patients. Most recently, Plompet al. [25] found a correlation between lower thoracicvertebral shape and the presence of Schmorl’s nodes inMedieval and Post-Medieval skeletons. They concludedthat the shape of the pedicles and vertebral body mightplay a role in the development of Schmorl’s nodes [25].Given that several studies have suggested a link betweenvertebral shape and the propensity to experience interver-tebral disc herniation, there is reason to investigate pos-sible explanations for why certain vertebral shapes shouldpredispose for this condition. Humans display substan-tially more degenerative and traumatic spinal pathologiesthan non-human primates [26,27]. This has led someresearchers to hypothesize that our unique mode oflocomotion, bipedalism, may influence the develop-ment of these conditions [28-30]. With this theory inmind, we carried out a cross-species study of vertebralshape variation in humans and non-human apes toexamine the links between vertebral shape, locomotorbehaviour and vertical intervertebral disc herniation.Specifically, we tested the hypothesis that intervertebraldisc herniation preferentially affects individuals whose ver-tebral shape are towards the ancestral end of the range ofshape variation within Homo sapiens and therefore are lesswell adapted for bipedalism.This “ancestral shape hypothesis” is derived fromwork on the evolution of bipedalism. It is now gener-ally accepted that humans and other hominins aremore closely related to chimpanzees (Pan troglodytes),and bonobos (Pan paniscus) than they are to any otherliving species [31]. At the moment, the locomotor behaviourof the common ancestor of the hominin and chimpanzee/bonobo lineages is debated. A number of different loco-motor behaviours have been suggested to be antecedent tobipedalism [32-34]. The most frequently cited suggestion isthat the common ancestor was a knuckle-walker likechimpanzees, bonobos, and gorillas (Gorilla gorilla)[35]. However, it has also been argued that the commonancestor of the hominin and chimpanzee/bonobo lineageswas an arboreal quadrumanous climber like orangutans(Pongo pygmaeus) [36]. Depending on which of thesehypotheses is correct, the hominin lineage shifted fromknuckle-walking to bipedalism or from quadrumanousclimbing to bipedalism. In both cases, the demandsplaced on the vertebrae would have changed. Selectionlikely acted to improve the ability of the vertebrae tocope with the new demands, but given that vertebralshape is almost certainly influenced by multiple genesand that the spine is multifunctional, we can also expectthat within a hominin species, some individuals will havevertebrae that are closer in shape to those of the commonancestor than others. Given that the ancestral vertebralshape would not have been adapted for bipedalism, indi-viduals whose vertebrae are towards the ancestral endof the range of shape variation can be expected to suf-fer disproportionately from external load-related spinalpathologies.In our study, we employed geometric morphometrics(GM) to record and analyze vertebral shape. Being basedon coordinate data as opposed to the inter-landmarkdistances of standard morphometrics, GM methods allowpatterns of shape variation to be investigated within a well-understood statistical framework that yields easily inter-preted numerical and visual results [37-40]. To identifyvertebral shapes associated with bipedalism, we adoptedthe approach employed by Russo [41] and comparedhuman vertebrae to the vertebrae of a knuckle-walkerand the presence of Schmorl’s nodes in humans. Thelandmarks capture the outline shape of the pedicles, theneural foramen, and the superior aspect of the vertebralbody [25]. Eight are Type II landmarks; the remainderare semi-landmarks [46]. The landmarks were recordedTable 1 Composition of sample of vertebrae from the71 humans, 36 chimpanzees, and 15 orangutansincluded in studyTaxon Female Male Unknown TotalOrangutansLast thoracic 4 8 0 12First lumbar 5 9 1 15Combined 9 17 1 27ChimpanzeesLast thoracic 8 17 0 25First lumbar 6 19 6 31Combined 14 36 6 56Healthy humansLast thoracic 12 14 0 26First lumbar 15 17 2 34Combined 27 31 2 60Pathological humansLast thoracic 13 20 0 33Figure 1 Location of the 17 landmarks used to capture thesuperior aspect of vertebrae. The eight landmarks on the posteriorPlomp et al. BMC Evolutionary Biology  (2015) 15:68 Page 3 of 10(the chimpanzee) and the vertebrae of a quadruman-ous climber (the orangutan). Humans, chimpanzees, andorangutans vary in modal vertebral formulae, with 12 thor-acic and 5 lumbar vertebrae in humans, 12 thoracic and 4lumbar vertebrae in orangutans, and 13 thoracic and 3 to 4lumbar vertebrae in chimpanzees [42]. Consequently,the last thoracic (T12/13) and the first lumbar (L1)vertebrae were included in the study to ensure pos-itional homology between vertebrae of different speciesand to represent the functionally distinct thoracic andlumbar spines. Another important consideration was thathuman T12s and L1s are commonly afflicted by Schmorl’snodes [20] and previous studies have found their shapesto correlate with the presence of these lesions [25,43].Following Plomp et al. [25], the presence of Schmorl’snodes was used as an indicator of vertical intervertebraldisc herniation. We tested two predictions of the ances-tral shape hypothesis: 1) there should be differences inshape between healthy human, chimpanzee, and orangu-tan vertebrae; and 2) human vertebrae with evidence ofvertical intervertebral disc herniation should be moresimilar in shape to the vertebrae of chimpanzees ororangutans than are human vertebrae without evidencefor intervertebral disc herniation.MethodsLast thoracic and first lumbar vertebrae from 71 humans,36 chimpanzees, and 15 orangutans were included in thesample (Table 1). Only adult individuals were included inthe analysis. Due to preservation issues and curationpractices, not all individuals had both vertebrae present.In total, the sample comprised 114 human vertebrae(59 thoracic, 55 lumbar), 56 chimpanzee vertebrae(25 thoracic, 31 lumbar), and 27 orangutan vertebrae(12 thoracic, 15 lumbar). The human vertebrae analysedin this study are the same as those analysed by Plompet al. [43]. They are Medieval-period specimens from thesites of Fishergate House, York [44], and Coach Lane,North Shields [45], and are curated at Durham University,UK (see Additional file 1 for details). Of the 114 humanvertebrae, 54 exhibited Schmorl’s nodes, and 60 didnot. For the purposes of this paper, we will refer to theformer as “pathological” and the latter as “healthy”.The chimpanzee and orangutan vertebrae are housedat the American Museum of Natural History, NewYork, and the Smithsonian National Museum of NaturalHistory, Washington DC, and are a mixture of zoo andwild-caught animals. None of the non-human ape verte-brae exhibit signs of pathology.The dataset comprised the 2D Cartesian coordinatesof 17 landmarks recorded on 197 dry-bone vertebrae(Figure 1). The landmarks were based on those used byPlomp et al. [25]. As we explained earlier, these authorsfound an association between certain vertebral shapesFirst lumbar 6 13 2 21Combined 19 33 2 54Pathological humans = human vertebrae with Schmorl’s nodes. Healthyhumans = human vertebrae without Schmorl’s nodes or other pathologies.None of the orangutan or chimpanzee vertebrae were pathological.elements are Type II and the nine landmarks along the curve of thebody are semi-landmarks. The vertebra depicted here is a human L1.Plomp et al. BMC Evolutionary Biology  (2015) 15:68 Page 4 of 10on standardized digital photographs with the aid of TPSDig [47].The first step in a geometric morphometric analysis isto reduce the effects of confounding factors [38]. As verte-brae are symmetrical along the sagittal midline, wefollowed the protocol outlined by Klingenberg et al. [48]to remove the influence of asymmetry on the results. Tobegin with, we created two datasets, one comprising theoriginal landmark coordinates and the other the reflectedand relabelled landmark coordinates [49]. We then slidthe semi-landmarks to remove shape differences arisingfrom the small differences that occur in the placement ofsemi-landmarks [50,51]. Next, we subjected the coordi-nates of the Type II landmarks and slid semi-landmarks ofboth datasets to generalized Procrustes analysis (GPA)[50,51]. GPA is designed to remove translation, rotational,and size effects [38]. Lastly, asymmetry was removed bycalculating the average Procrustes coordinates betweenthe original and reflected landmarks. These coordinateswere used in all further analyses. The reflection, slidingprocedure, and GPA were applied separately to the T12/T13 and L1 vertebrae. The semi-landmarks were slid, andthe GPA performed, with the aid of TPSRelW [47].Intra observer error was assessed as per Neubaueret al. [52]. A T12 vertebra and an L1 vertebra were eachdigitized ten times, and the greatest Procrustes distancebetween the repeated measurements for a given speci-men was then compared to the smallest Procrustes dis-tance among all specimens of the same type. In bothanalyses, the between-specimen distances were close tothree times greater than the within-specimen distances.According to Neubauer et al. [52], this level of differenceindicates that intra-observer error is unlikely to be aconfounding factor. This analysis was carried out withMorphologika [53].The impact of allometry was assessed by regressingthe Procrustes coordinates on log centroid size. The stat-istical significance of male–female shape differences wasdetermined using MANOVAs on all principal compo-nent (PC) scores obtained through principal componentsanalyses (PCA). These analyses were performed in SPSS16.0 [54] and MorphoJ [55], and carried out separately forthe last thoracic and first lumbar vertebrae. Allometrywas found to be a factor in vertebral shape (T12/T13:r2 = 0.092, p < 0.001; L1: r2 = 0.072, p < 0.001), but sex-ual dimorphism was not (p > 0.10). The frequency ofSchmorl’s nodes between the two human populationswas not statistically different (χ2 p > 0.339) and therewas no statistical difference in vertebral shape betweenhuman populations (p > 0.108). In light of these results,we opted to employ allometry-free regression residualsderived from pooled-sex samples in the remainder ofthe analyses [56], with humans analyzed as a homoge-neous population.Following Klingenberg and Monteiro [57], we appliedcanonical variates analysis (CVA) to the pooled-sex regres-sion residuals to determine the maximum Procrustes dis-tances among taxa. The significance of differences wasassessed using permutations of pair-wise Procrustes dis-tances among all possible pairs of taxa. We carried this outinitially for the last thoracic vertebrae and repeated it forthe first lumbar vertebrae. The analyses were conducted inMorphoJ [55].We used PCA to explore the pattern of inter-taxonshape variation [38]. Only PCs representing at least 5% ofthe total variance were considered in order to minimizenoise from higher components [58]. The statistical sig-nificance of inter-taxon PCA score differences was assessedusing MANOVAs. As in the previous analysis, the last thor-acic and first lumbar vertebrae were analyzed separately.This analysis was performed in TPSRelW [47] and SPSS16.0 [54].ResultsLast thoracic vertebraeThe CVA of the Procrustes coordinates for the last thor-acic vertebrae returned three CVs (canonical vectors).The first accounts for 67.1% of the variance, the second24.1%, and the third 8.8%. There is little separation amongtaxa when CV3 is plotted against CV1 (Additional file 2:Figure S1). When CV1 is plotted against CV2 (Figure 2a),it is apparent that the shape of the last thoracic vertebraeof orangutans is different from the shape of the lastthoracic vertebrae of not only healthy and pathologicalhumans but also of chimpanzees. It is also apparentwhen CV1 is plotted against CV2, that pathologicalhuman vertebrae have more in common with chimpan-zee vertebrae than do healthy humans. All the inter-taxon Procrustes distances are significant except forthe one between pathological humans and chimpan-zees (Table 2). Pair-wise analyses using permutationsof Mahalanobis distances produce the same pattern(Additional file 3: Table S1).The PCA yielded six PCs that met the ≥5% of variancecriterion. PC1 accounts for 30.3% of the variance, PC225.6%, PC3 18.1%, PC4 9.6%, PC5 5.1%, and PC6 4.8%.There is considerable overlap among the taxa on PC1,PC4, PC5, and PC6 (Additional file 2: Figure S2-S4).However, the taxa are distinguishable when PC2 andPC3 are plotted against each other. Healthy humanvertebrae tend to score more positively on PC2 andnegatively on PC3, while orangutan vertebrae tend toscore more negatively on PC2 and more positively onPC3 (Figure 2b). Pathological humans and chimpan-zees plot between healthy humans and orangutans onboth PCs. The deformation grids in Figure 2b illustratethe shape differences between the negative and positiveextremes of PC2 and PC3. Moving from the positiverteforaePlomp et al. BMC Evolutionary Biology  (2015) 15:68 Page 5 of 10extreme of PC2 to the negative one, there is a transitionfrom heart-shaped vertebral bodies with flared pedicles torounder vertebral bodies without flared pedicles. There isalso a decrease in neural foramen size relative to the verte-bral body, and a translation of the posterior margin of thebody into the neural canal. The shape differences thatFigure 2 CVA and PCA plots depicting shape variance of T12/T13 vepathological human, P. troglodytes, P. pygmaeus vertebrae on CV1 and CV2healthy human, pathological human, P. troglodytes, P. pygmaeus vertebshape differences occurring on each PC.occur as we move from negative to positive scores on PC3are a relative decrease in neural foramen size and a rela-tive increase in the width of the pedicles. Thus, comparedto healthy humans, pathological humans and chimpanzeeshave relatively smaller neural foramina, shorter, widerpedicles, and rounder vertebral bodies, whereas comparedto orangutans, they have relatively larger neural foramina,longer, narrower pedicles, and more heart-shaped verte-bral bodies. The MANOVA on the PCs that met the cri-terion for inclusion is significant (p < 0.0001). Pair-wiseMANOVAs are significant for all inter-taxon compari-sons, except those between pathological humans andchimpanzees (Table 3).Table 2 Procrustes distances between taxon means forT12/T13 vertebra shapePathological humans Orangutans ChimpanzeesHealthy humans 0.0248 0.0539 0.0248p = 0.018* p < 0.0001* p = 0.028*Chimpanzees 0.0119 0.0352p = 0.5190 p = 0.012*Orangutans 0.0402p < 0.0001**indicates significant value.Thus, the results of the analyses of the last thoracicvertebrae are consistent with the test predictions. The find-ing of differences among healthy human, chimpanzee, andorangutan vertebrae is in line with the prediction that thevertebral shape of these taxa should be distinguishable dueto their locomotion. The analyses also indicate that healthybrae. a) CVA scatter-plot illustrating shape variation of healthy human,r T12/T13 vertebrae b) PCA scatter-plot illustrating shape variance ofon PC2 and PC3 of T12/T13 vertebrae. Deformation grids illustratehuman vertebrae are statistically distinguishable fromchimpanzee vertebrae, whereas pathological human verte-brae are not. This finding is consistent with the predictionthat human vertebrae with evidence of vertical interverte-bral disc herniation should be more similar in shape to thevertebrae of chimpanzees than are human vertebrae with-out evidence of intervertebral disc herniation.First lumbar vertebraeThe CVA of the Procrustes coordinates for the first lum-bar vertebrae returned three CVs. The first CV accountsfor 68.6% of the variance, the second 20.1%, and thethird 11.3%. There is little distinction among the taxaTable 3 Results of pairwise MANOVAs for T12/T13vertebrae on PCs 1 through 6, which collectivelyrepresent 93.5% of the total shape variancePathologicalhumansOrangutans ChimpanzeesHealthyhumansλ 0.745 F = 3.762p = 0.005*λ 0.374 F = 11.362p < 0.0001*λ 0.728 F = 3.804p = 0.005*Chimpanzees λ 0.986 F = 0.164p = 0.975λ 0.537 F = 6.377p < 0.0001*Orangutans λ 0.668 F = 4.077p < 0.004**indicates significant value.when CV3 is plotted against CV1 (Additional file 2: FigureS5). In contrast, when CV2 is plotted against CV1, it is ap-parent that pathological human vertebrae are more similarin shape to chimpanzee vertebrae than are healthy humanvertebrae (Figure 3a). The Procrustes distances supportthese observations. All inter-taxon Procrustes distancesare significant except the one between pathological humanand chimpanzee vertebrae (Table 4). The same pattern isproduced by pair-wise analyses using permutations ofMahalanobis distances (Additional file 3: Table S2).The PCA for the first lumbar vertebrae yielded five PCsthat met the ≥5% of variance criterion. PC1 accounts for39.6% of the variance, PC2 23.8%, PC3 16.0%, PC4 7.4%,and PC5 5.1%. There is considerable overlap among taxaon PCs 3 through 5 (Additional file 2: Figure S6-S7). How-ever, taxa are distinguishable on PC1 and PC2 (Figure 3b).Healthy humans score more negatively than orangutanson PC1 and PC2, with pathological humans and chimpan-zees between them on both PCs. Deformation grids showthat the shape differences between samples are similar tothose seen in the T12/13 analysis (Figure 3b). Again, themore laterally angled from the body as we move from thepositive end of PC2 to the negative one. To reiterate,healthy humans and orangutans score at the extremes ofthe shape variation on both PCs, with pathologicalhumans and chimpanzees between them. Thus, whencompared to healthy humans, pathological humans andchimpanzees tend to have smaller neural foramina, wider,shorter pedicles, and more shovel-shaped bodies. Whencompared to orangutans, pathological humans and chim-panzees have larger neural foramina, narrow pedicles, andless shovel-shaped vertebral bodies. The MANOVA onthe PCs that met the ≥5% of variance criterion is statisti-cally significant (p = 0.001). Pair-wise MANOVAs are sig-nificant for all inter-taxon comparisons, except betweenpathological humans and chimpanzees (Table 5).Thus, the results of the analyses of the first lumbarvertebrae are also consistent with the test predictions.The finding of differences in shape between the healthyhuman, chimpanzee, and orangutan specimens is con-sistent with the first test prediction, while the findingthat pathological human vertebrae are closer in shape toraeV2Plomp et al. BMC Evolutionary Biology  (2015) 15:68 Page 6 of 10most obvious shape differences relate to the pedicles andvertebral body. Moving from the negative end of PC1 tothe positive end, there is a decrease in neural foramen sizerelative to the vertebral body and the pedicles becomeshorter and wider. In addition, there is a backward transla-tion of the posterior margin of the vertebral body thatresults in it becoming less heart-shaped and more shovel-shaped. The shape differences captured by PC2 are a dif-ference in pedicle orientation, with the pedicles becomingFigure 3 CVA and PCA plots depicting shape variance of L1 vertebpathological human, P. troglodytes, P. pygmaeus vertebrae on CV1 and Chealthy human, pathological human, P. troglodytes, P. pygmaeus vertebrae odifferences occurring on each PC.chimpanzees than are healthy human vertebrae is con-sistent with the second test prediction.DiscussionThis study explicitly tested the ancestral shape hypothesis,which holds that intervertebral disc herniation preferentiallyaffects individuals with vertebrae that are towards the ances-tral end of the range of shape variation within H. sapiensand therefore are less well adapted for bipedalism. We. a) CVA scatter-plot illustrating shape variation of healthy human,for L1 vertebrae b) PCA scatter-plot illustrating shape variance ofn PC1 and PC2 of L1 vertebrae. Deformation grids illustrate shapeTable 4 Procrustes distances between taxon means forfirst lumbar vertebra shapePathological humans Orangutans ChimpanzeesHealthy humans 0.0303 0.0779 0.0367p = 0.004* p < 0.0001* p = 0.0004*Chimpanzees 0.0161 0.0458p = 0.4590 p = 0.0001*Orangutans 0.0549Plomp et al. BMC Evolutionary Biology  (2015) 15:68 Page 7 of 10tested two predictions of this hypothesis with shapedata recorded on the last thoracic and first lumbar verte-brae of orangutans, chimpanzees, healthy humans, andhumans with Schmorl’s nodes, which are bony indicatorsof intervertebral disc herniation. The first prediction wasthat there should be differences in shape between healthyhuman vertebrae, chimpanzee vertebrae, and orangutanvertebrae, due to the different modes of locomotion of thetaxa. The second prediction was that pathological humanvertebrae should share more similarities in shape withchimpanzee or orangutan vertebrae than do healthy hu-man vertebrae. The results of the analyses were consistentwith both predictions. We found that the last thoracic andfirst lumbar vertebrae of healthy humans, orangutans, andchimpanzees differ significantly in shape, which is in linewith the first prediction. We also found that human verte-brae with Schmorl’s nodes share more similarities in shapewith chimpanzee vertebrae than do healthy human verte-brae, which is consistent with the second prediction. Thus,the study supports the ancestral shape hypothesis.A potential alternative explanation for our findingsneeds to be considered. The vertebral shapes associatedwith Schmorl’s nodes may be a consequence of interver-tebral disc herniation rather than its cause. It is certainlythe case that vertebrae can remodel. For example, theshape of the vertebral body is known to change with in-creasing age. Body height tends to decrease and there isoften an increase in surface concavity as the endplatep < 0.0001**indicates significant value.collapses [59]. However, we do not consider interverte-bral disc herniation causing changes in vertebral shapeTable 5 Results of pairwise MANOVAs for first lumbarvertebra on PCs 1 through 5, which collectively represent92.0% of the total shape variancePathologicalhumansOrangutans ChimpanzeesHealthyhumansλ 0.781 F = 2.744p = 0.029*λ 0.409 F = 11.854p < 0.0001*λ 0.723 F = 4.513p = 0.002*Chimpanzees λ 0.892 F = 1.113p = 0.367λ 0.640 F = 4.277p = 0.003*Orangutans λ 0.445 F = 6.985p < 0.0001**indicates significant value.to be a good explanation for our results. One of themain shape differences identified between healthy hu-man vertebrae and those with Schmorl’s nodes relates tothe neural foramen [25]. Previous work indicates thatthe shape of the neural foramen does not change afterthe neural arch fuses to the vertebral body [60,61] ataround six years of age in humans [62]. Therefore, anyfactor that influences the shape of the neural foramenmust act during spinal development. Bone remodellingduring development could influence the shape of thevertebrae, including the neural foramen. Although thiscould explain why there is a difference in shape betweenpathological and healthy human vertebrae, it does notexplain the relationship identified between pathologicalhuman and chimpanzee vertebrae. This explanation wouldrequire that bone remodelling result in vertebral shapechanges that systematically approach a shape functionallyrelated to quadrupedal locomotion. This, we submit, isless parsimonious than the ancestral vertebral hypothesis.A possible functional explanation for the associationbetween vertical disc herniation and vertebral shape isprovided by Harrington et al. [24]. These authors suggestthat the diameter of the vertebral disc influences itsability to withstand tension during compression. Theirargument rests on LaPlace’s law [62], which states thatthe ability of a fluid-filled tube to withstand tensiondecreases with increasing radius. According to Harringtonet al. [24], the rounder bodies of pathological vertebraewould have a larger diameter than the more heart-shapedbodies seen in healthy vertebrae, making the intervertebraldisc less able to withstand stress [24,62]. We also foundthat pathological vertebrae have shorter pedicles comparedto healthy vertebrae. The pedicles act as structural but-tresses for the vertebral body and play an important role inload bearing during axial compression [63-68]. It has beenhypothesized that the shorter pedicles identified in verte-brae with Schmorl’s nodes may be less able to withstandphysical strain placed on the spine [25,45]. Since bipedal-ism causes a large amount of axial loading on the lowervertebrae [30], we hypothesize that the combination ofround vertebral bodies with short pedicles may provideless support for the spine during bipedal posture andlocomotion.Our results have implications for medical science be-yond shedding light on the causes of intervertebral discherniation. One is that vertebral shape may be a factorthat could help predict an individual’s susceptibility tovertical intervertebral disc herniation. The shape analysistechniques used in this study can also be used on med-ical images, such as CT scans. It may be possible for cli-nicians to investigate an individual’s vertebral shape andidentify those who may be at risk of developing the con-dition. This ability would have significant diagnostic andpreventative value, especially for high-risk individuals,into how bipedalism evolved, and suggest whether itshape analyses of human and non-human ape vertebrae toPlomp et al. BMC Evolutionary Biology  (2015) 15:68 Page 8 of 10such as athletes [69]. In addition, a better understandingof the role that locomotion and posture plays in thehealth of the spine could aid in the treatment of individ-uals afflicted with symptomatic vertical intervertebraldisc herniation. Locomotion is recognized as an im-portant factor in rehabilitation for sufferers of backpain [70], and understanding the role that vertebralvariation can play in spinal health could aid physio-therapists to refine activity and exercise regimes.Thus, the findings of this study may not only helpmedical practitioners to understand why some individ-uals are more commonly afflicted with back problemsthan others, but may also lead to advances in the identifi-cation, prevention, and treatment of people suffering fromintervertebral disc herniation.In addition to offering these potential clinical benefits,our results provide further support for the claim that anevolutionary perspective can shed important light on hu-man health problems [71-74]. Evolutionary medicine hasidentified the value of considering evolutionary adapta-tions to enable better understanding of human develop-mental issues, chronic diseases, and nutritional needs[74], but the influence of skeletal morphology on humanhealth has received little attention. Our study highlightsthe potential of using osteological analyses of skeletal vari-ation, including comparative analyses between humansand non-human primate species, in evolutionary medicalstudies. Bipedalism has been suggested to impact humanspinal and joint health [28-30,75,76], but few studies havebeen carried out to evaluate this proposition [30]. Theidentification of an ancestral vertebral shape that influ-ences the occurrence of a common spinal pathologysupports the idea that the relatively rapid evolution ofbipedalism in the hominins may continue to impactmodern human health.The main goal of our study was to shed light on amajor contemporary health problem with the conceptualand analytical tools of evolutionary biology, but our re-sults also contribute to the understanding of humanevolution. Specifically, they shed additional light on theevolution of bipedalism, and in particular, the functionalanatomy associated with it. Previous studies have identi-fied morphological characteristics purported to relate tobipedalism [77-80]. The present findings add features tothis list—a larger neural foramen relative to body size,taller, narrower pedicles, and a more heart-shaped verte-bral body. There are two persistent debates in palaeoan-thropology regarding the evolution of bipedalism and abetter understanding of the functional anatomy of bipedalvertebrae may contribute to their resolution. The firstdebate regards the timing of the emergence of bipedal-ism in the evolutionary record. The understanding ofhow human vertebrae are unique among hominoidsenables the identification of fossil vertebrae adaptedinvestigate how 3D vertebral morphology relates to loco-motion and human spinal health. Lastly, the clinical valueof this research would be substantially increased with theinclusion of in-vivo medical images of individuals withand without back problems.ConclusionsOur study supports the hypothesis that intervertebral discherniation preferentially affects individuals with vertebraethat are towards the ancestral end of the range of shapevariation within Homo sapiens and therefore are less welladapted for bipedalism. As predicted by the hypothesis, weidentified a relationship between the shape of the last thor-acic and first lumbar vertebrae and locomotion in humans,chimpanzees, and orangutans, and we found that humanvertebrae with signs of vertical intervertebral disc her-niation are indistinguishable from those of chimpanzees.When compared to healthy humans, pathological humanand chimpanzee vertebrae tend to have smaller neural for-amina, shorter, wider pedicles, and more shovel-shapedvertebral bodies. Our study’s support for the ancestralshape hypothesis not only has clinical implications, but alsoprovides another illustration of the benefits of bringing theconceptual and analytical tools of evolutionary biology tobear on problems in medicine and public health.Additional filesfollowed a gradual or punctuated pattern of evolution.The second debate surrounding the evolution of bipedal-ism is whether early bipeds walked with their knees andhips in a flexed position, like chimpanzees, or if theirmode of bipedalism resembled our own [81-84]. The abil-ity to identify vertebral shape characteristics unique tohumans and compare these with features unique to mod-ern chimpanzees may provide additional insight into thefunctional anatomy required for habitual bipedalism andhelp understand the evolutionary trends that led to themodern human gait.With regard to future research, several possibilities sug-gest themselves. Firstly, if the ancestral shape hypothesis isaccepted, it prompts the question of how this shape in-fluences the occurrence of vertical intervertebral discherniation. This could be investigated with biomechanicalstudies of the interaction between locomotion, vertebralmorphology, and the soft tissues of the spine. Secondly,this area of research would benefit from the use of 3Dfor bipedal locomotion; this will help researchers inferwhich species were bipedal, provide additional insightAdditional file 1: Archaeological site information for FishergateHouse, York, and Coach Lane, North Shields, Tyne and Wear.Plomp et al. BMC Evolutionary Biology  (2015) 15:68 Page 9 of 10Additional file 2: Figure S1. CVA scatter-plot illustrating shape varianceof healthy human, pathological humans, P. troglodytes, P. pygmaeusvertebrae on CV1 and CV3 for T12/T13 vertebrae. Figure S2. PCAscatter-plot illustrating shape variance on PC1 and PC2 for T12/T13vertebrae. Legend: yellow circle - healthy humans, red circles – pathologicalhumans, green triangles – chimpanzees, blue octagons – orangutans.Figure S3. PCA scatter-plot illustrating shape variance on PC4 and PC5for T12/T13 vertebrae. Legend: yellow circle - healthy humans, red circles –pathological humans, green triangles – chimpanzees, blue octagons –orangutans. Figure S4. PCA scatter-plot illustrating shape variance on PC5and PC6 for T12/T13 vertebrae. Legend: yellow circle - healthy humans, redcircles – pathological humans, green triangles – chimpanzees, blueoctagons – orangutans. Figure S5. CVA scatter-plot illustrating shapevariance of healthy human, pathological humans, P. troglodytes, P. pygmaeusvertebrae on CV1 and CV3 for L1 vertebrae. Figure S6. PCA scatter-plotillustrating shape variance on PC2 and PC3 for L1 vertebrae. Legend: yellowcircle - healthy humans, red circles – pathological humans, green triangles –chimpanzees, blue octagons – orangutans. Figure S7. PCA scatter-plotillustrating shape variance on PC4 and PC5 for L1 vertebrae. Legend:yellow circle - healthy humans, red circles – pathological humans, greentriangles – chimpanzees, blue octagons – orangutans.Additional file 3: Table S1. Mahalanobis distances between taxonmeans for the last thoracic vertebrae shape. Table S2. Mahalanobisdistances between taxon means for first lumbar vertebrae shape.Competing interestsThe authors declare that they have no competing interests.Authors’ contributionsAll authors have contributed to the preparation of this manuscript. KAPcollected and analyzed the data, and led the preparation of the manuscript.MC supervised the project and provided substantial contributions to theanalysis and interpretation of the data, and the preparation of themanuscript. USV, DAW, and KD contributed to the project by aiding in theinterpretation of the data and the preparation of the manuscript. All authorsapproved the final manuscript.AcknowledgmentsWe thank York Osteoarchaeology, Pre-Construct Archaeology, Durham University,the Natural History Museum, and the American Museum of Natural Historyfor access to the specimens used in the study. We also thank Helgi PéturGunnarsson for his assistance with the analyses. The study was funded bythe Social Sciences and Humanities Research Council, Canada ResearchChairs Program, Canada Foundation for Innovation, British ColumbiaKnowledge Development Fund, MITACS, and Simon Fraser University. Wethank the editor and two anonymous reviewers for their insightful commentsand suggestions on this paper.Author details1Human Evolutionary Studies Program and Department of Archaeology,Simon Fraser University, Burnaby, BC, Canada. 2Biomedical Center, Universityof Iceland, Reykjavik, Iceland. 3Department of Anthropology, University ofBritish Columbia, Vancouver, BC, Canada. 4Department of Human Evolution,Max Planck Institute for Evolutionary Anthropology, Leipzig, Germany.5Department of Archaeology, University of Aberdeen, Aberdeen, UK.Received: 21 November 2014 Accepted: 19 March 2015References1. Walker BF. The prevalence of low back pain: a systematic review of theliterature from 1966 to 1998. J Spinal Disord. 2000;13:205–17.2. Balague F, Mannion AF, Pellise F, Cedraschi C. Non-specific low back pain. Lancet.2012;379:482–91.3. Buchbiner R, Blyth FM, March LM, Brooks P, Woolf AD, Hoy DG. Placing theglobal burden of low back pain in context. Best Pract Res Cl Rh.2013;27:575–89.4. 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