Genome-phenotype-environment associations identify signatures of selection in a panmictic population of threespine stickleback

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 defence 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 loci linked to pelvic spine length were
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.