Genome-phenotype-environment associations identify signatures of
selection in a panmictic population of threespine stickleback
Abstract
Adaptive genetic divergence occurs when selection imposed by the
environment causes the genomic component of the phenotype to
differentiate. However, genomic signatures of natural selection are
usually identified without information on which trait is responding to
selection by which selective agent(s). Here, we integrate
whole-genome-sequencing with phenomics and measures of putative
selective agents to assess the extent of adaptive divergence in
threespine stickleback occupying the highly heterogeneous lake Mývatn,
NE Iceland. We find negligible genome wide divergence, yet multiple
traits (body size, gill raker structure and defense traits) were
divergent along known ecological gradients (temperature, predatory bird
densities and water depth). SNP based heritability of all measured
traits was high (h2 = 0.42 – 0.65), indicating adaptive potential for
all traits. Whilst environment-association analyses identified thousands
of loci putatively involved in selection, related to genes linked to
neuron development and protein phosphorylation, only allelic variation
linked to pelvic spine length was concurrently linked to environmental
variation (water depth) - supporting the conclusion that divergence in
pelvic spine length occurred in face of gene flow. Our results suggest
that whilst there is substantial genetic variation in the traits
measured, phenotypic divergence of Mývatn stickleback is mostly weakly
associated with environmental gradients, potentially as a result of
substantial gene flow. Our study illustrates the value of integrative
studies that combine genomic assays of multivariate trait variation with
landscape genomics.