Oceans apart: Heterogeneous patterns of parallel evolution in sticklebacks

Abstract Reuse of standing genetic variation is thought to be the main mechanism behind the repeated evolution of the same phenotypes in similar environments. An important model system for the study of genomic mechanisms underlying parallel ecological adaptation in the wild is the three-spined stickleback (Gasterosteus aculeatus), which has repeatedly colonized and adapted to freshwater from the sea. Previous studies have identified numerous genomic regions showing consistent genetic divergence between freshwater and marine ecotypes, but most of these studies have been based on limited geographic sampling, and with strong biases towards studies conducted in the Eastern Pacific area. We analysed population genomic data from three-spined sticklebacks with comprehensive global sampling using unsupervised methods to detect loci involved in parallel evolution at different geographical areas. In line with previous studies, we find several genomic regions, including two chromosomal inversions, contributing to global differentiation of marine and freshwater ecotypes. However, signatures of parallel evolution were far stronger in the Eastern Pacific region than anywhere else in the world. With simulations, we demonstrate that since freshwater-adapted alleles exist in the marine populations only at low frequencies, they are easily lost during founder events, thereby reducing the amount of standing genetic variation available for freshwater adaptation outside of the ancestral Eastern Pacific region. Hence, geographic heterogeneity in access to standing genetic variation due to historical demographic factors appears to provide an explanation to marked geographic differences in the pervasiveness of parallel evolution in the three-spined stickleback. Therefore, the degree of genetic parallelism in the three-spined stickleback model system appears not be as pervasive as earlier studies focused on Eastern Pacific populations have led us to believe.