Evol Ecol Res 20: 231-245 (2019)     Full PDF if your library subscribes.

Predictive covariation among trophic, isotopic, and genomic traits is consistent with intrapopulation diversifying selection

Thomas E. Reimchen1, Sandra Frey1,2, Shannon D. Brady3 and David M. Kingsley3

1Department of Biology, University of Victoria, Victoria, British Columbia, Canada, 2School of Environmental Studies, University of Victoria, Victoria, British Columbia, Canada and 3Department of Developmental Biology, Howard Hughes Medical Institute and Stanford University School of Medicine, Stanford, California, USA

Correspondence: T.E. Reimchen, Department of Biology, PO Box 3020, University of Victoria, Victoria, BC V8W 3N5, Canada. email: reimchen@uvic.ca


Questions: To what extent does intra-sex variation in size-corrected feeding structures covary with stable isotopic values and genotype within Threespine stickleback populations?

Hypothesis: Phenotype, isotopic niche space, and genome-wide markers of fish will covary.

Field site: Boulton Lake, a small shallow bog lake on Graham Island, Haida Gwaii, western Canada.

Organism: An endemic population of sexually dimorphic Threespine stickleback (Gasterosteus aculeatus).

Methods: We sampled 225 male stickleback from 11 microsites on a lake-wide grid that differed in water depth and substrate (mud, sand, hardpan). The fish were scored for: (1) trophic morphology (jaw length, eye size, gill raker length, inter-raker distance); (2) stable isotope signatures (δ15N, δ13C) of muscle tissue; and (3) genome-wide, single nucleotide polymorphisms (SNP) (3072 marker microarray). We reduced all data using principal component analysis (PCA). We compared distance matrices among data sets using Mantel r-tests. To visualize the genetic distances among individuals, we also computed unrooted, neighbour-joining trees from the SNPs.

Results: The first three principal components of trophic morphology (PCtroph) accounted for 85% of the variance, with highest loadings for char Symbol:43eye and char Symbol:43gape on PC1, char Symbol:43inter-raker distance and char Symbol:43raker length on PC2, and char Symbol:43raker length and char Symbol:45inter-raker distance on PC3. PC1troph was significantly positively correlated with δ15N and this occurred at each of the three habitat types. Euclidean distance matrices of individuals of PC1troph against PC2troph were correlated with Euclidean distances for δ15N against δ13C arrays. We extracted 25 principal components from the informative SNPs, which accounted for 30% of the total genetic variance. Four principal components, with most SNPs on Chromosomes IV, VIII, and XII, were significantly associated with trophic phenotype variation. Neighbour-joining trees on genomic data yielded branches. These differed in their position in dual isotopic niche space including the extent of dietary specialization.

Conclusions: The cumulative data indicate that size-corrected phenotypic variation in trophic morphospace represents a combination of niche specialists and generalists with phenotypic outliers concordant with isotopic outliers. These data are largely consistent with diversifying selection for maintenance of intrapopulation, adaptive variation.

Keywords: diversifying selection, ecogenomics, Gasterosteus aculeatus, Haida Gwaii, individual niche, intrapopulation variation, stable isotopes, stickleback.

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