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 Frey^1,2, 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

ABSTRACT

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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