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Adaptive divergence and the evolution of trophic diversity in the threespine stickleback Lavin, Patrick A.


Five populations of the threespine stickleback, Gasterosteous aculeatus,from the upper Cowichan River system (Vancouver Island, British Columbia) were surveyed to assess interpopulation levels of variability in trophic morphology. Phenotypic divergence is assumed to be a post-glacial event. Nine characters were scored; eight were related to feeding and the ninth character was lateral plate number. All populations surveyed were the low plate morph; however populations of Gasterosteus in lakes lacking piscivorous fish had significantly fewer lateral plates than populations in lakes with predatory fish species. Three trophic 'morphotypes' were identified, each associated with one of three lake environments. Populations inhabiting benthic dominated environments ('benthic morph') were found to possess reduced gill raker number and reduced gill raker length but increased upper jaw length relative to populations from lentic environments ('limnetic morph'). An intermediate morph may also exist and is characterized by a morphology suitable to either trophic regime. Analysis of stomach contents showed diet type (benthic or limnetic) to be significantly dependent on morph. The functional significance of differences in trophic morphology was investigated in three feeding experiments using a representative population from each morphotype. The longer jaw of the benthic and intermediate morphs allowed them to ingest a larger benthic prey than the limnetic. No behavioural component to benthic foraging success between populations was identified, although increased jaw length shortened the time spent manipulating prey. Both the intermediate and limnetic morphs were better foragers on an experimental limnetic prey than was the benthic. Head length, snout length, gill raker density and gill raker number were strongly correlated with limnetic foraging success. The quantitative genetics governing the eight trophic characters were investigated using the same three representative populations. Broad sense estimates of character heritabilities ranged from 0.132 to 0.677; all estimates were significant. Character genetic correlations were reasonably strong (0.3 ≤ |rG| ≤ 0.9), while character correlations arising through environment tended to be lower. Cluster analyses of the genetic correlation matrices defined two character suites, the first grouped measures of head shape, the second grouped measures of gill raker structure. The patterns of genetic correlations suggest the three populations are distinct races. Selection gradients for divergence between morphotype indicated that directional selection had operated hardest on head length, snout length, gill raker number, head depth and upper jaw length; hence selection has operated to modify characters related to food size. The benthic-limnetic and intermediate-limnetic morphs were separated by the greatest selection distance while the intermediate-benthic morphs were separated by the shortest selection distance. These results support the conclusion that directional selection, arising from trophic resource differences between lakes, has organized interpopulation variability for Gasterosteus within the upper Cowichan drainage. The racial distinction of each population coupled with the functional significance of some components of trophic morphology indicate that at least the benthic and limnetic morphs must be considered 'ecotypes'.

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