Genomics of freshwater adaptation in threespine stickleback from eastern Canada

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Abstract

The threespine stickleback (Gasterosteus aculeatus) is a key species for studying parallel evolution. However, most evidence for parallel evolution at the genetic and phenotypic levels comes from the west coast of North America and Europe. Here, we use restriction site-associated DNA sequencing (‘RAD-seq’) of pooled samples to examine marine-freshwater differentiation in stickleback populations from Atlantic Canada and to test for signatures of parallel evolution. Our results reveal substantial heterogeneity in the degree of genomic differentiation between marine and freshwater populations. The strongest candidate loci were two SNPs near dopamine receptor genes (Drd4a and Drd2l), which were repeatedly differentiated between marine and freshwater habitats. Gene ontology (GO) analysis of candidate genes showed enrichment for functions related to nervous system development and dopamine receptor activity. These findings suggest a more complex evolutionary history for Atlantic stickleback populations than previously recognized, potentially involving multiple colonization events or ongoing gene flow. The repeated differentiation of genomic regions linked to dopaminergic signalling suggests that changes in neurological phenotypes could play an important role in adaptation to freshwater environments.

Significance statement

Threespine stickleback are a model for parallel evolution, yet most research has focused on Pacific and European populations. We studied overlooked Atlantic Canadian populations and found distinct genomic patterns of freshwater adaptation. Unlike the classic armour plate changes, adaptation in this region involves divergence near dopamine receptor genes, pointing to behavioural and hormonal pathways. These results highlight how evolution can take different genetic routes to similar ecological outcomes, underscoring the value of studying diverse geographic lineages.

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