Polygenic Basis and the Role of Genome Duplication in Adaptation to Similar Selective Environments

Abstract

Abstract Genetic changes underlying adaptation vary greatly in terms of complexity and, within the same species, genetic responses to similar selective pressures may or may not be the same. We examine both complex (supergene) and simple (SNP) genetic variants occurring in populations of rainbow trout (Oncorhynchus mykiss) independently isolated from ocean access and compared them to each other and to an anadromous below-barrier population representing their ancestral source to search for signatures of both parallel and nonparallel adaptation. All landlocked populations displayed an increased frequency of a large inversion on chromosome Omy05, while 3 of the 4 populations exhibited elevated frequencies of another inversion located on chromosome Omy20. In addition, we identified numerous regions outside these 2 inversions that also show significant shifts in allele frequencies consistent with adaptive evolution. However, there was little concordance among above-barrier populations in these specific genomic regions under selection. In part, the lack of concordance appears to arise from ancestral autopolyploidy in rainbow trout that provides duplicate genomic regions of similar functional composition for selection to act upon. Thus, while selection acting on landlocked populations universally favors the resident ecotype, outside of the major chromosomal inversions, the resulting genetic changes are largely distinct among populations. Our results indicate that selection on standing genetic variation is likely the primary mode of rapid adaptation, and that both supergene complexes and individual loci contribute to adaptive evolution, further highlighting the diversity of adaptive genomic variation involved in complex phenotypic evolution.