Whole-Genome Resequencing Reveals Polygenic Signatures of Directional and Balancing Selection on Alternative Migratory Life Histories

Migration in animals and associated adaptations to contrasting environments are underpinned by complex genetic architecture. Here, we explore the genomic basis of facultative anadromy in brown trout (Salmo trutta), wherein some individuals migrate to sea while others remain resident in natal rivers, to better understand how alternative migratory tactics (AMTs) are maintained evolutionarily. To identify genomic variants associated with AMTs, we sequenced whole genomes for 194 individual trout from five anadromous-resident population pairs, situated above and below waterfalls, in five different Irish rivers. These waterfalls act as natural barriers to upstream migration and hence we predicted that loci underpinning AMTs should be under similar divergent selection across these replicate pairs. A sliding windows based analysis revealed a highly polygenic adaptive divergence between anadromous and resident populations, encompassing 329 differentiated genomic regions. These regions were associated with 292 genes involved in various processes crucial for AMTs, including energy homeostasis, reproduction, osmoregulation, immunity, circadian rhythm and neural function. Furthermore, examining patterns of diversity we were able to link specific genes and biological processes to putative AMT trait classes: migratory-propensity, migratory-lifestyle and residency. Importantly, AMT outlier regions possessed higher genetic diversity than the background genome, particularly in the anadromous group, suggesting balancing selection may play a role in maintaining genetic variation. Overall, the results from this study provide important insights into the genetic architecture of migration and the evolutionary mechanisms shaping genomic diversity within and across populations.