Oceans apart: Heterogeneous patterns of parallel evolution in sticklebacks

Abstract

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 throughout the northern hemisphere. Previous studies have identified numerous genomic regions showing consistent genetic differentiation between freshwater and marine ecotypes, but these are typically based on limited geographic sampling and are biased towards studies in the Eastern Pacific. We analysed population genomic data from marine and freshwater ecotypes of three-spined sticklebacks with from a comprehensive global collection of marine and freshwater ecotypes to detect loci involved in parallel evolution at different geographic scales. Our findings highlight that most signatures of parallel evolution were unique to the Eastern Pacific. Trans-oceanic marine and freshwater differentiation was only found in a very limited number of genomic regions, including three chromosomal inversions. Using both simulations and empirical data, we demonstrate that this is likely due to both the stochastic loss of freshwater-adapted alleles during founder events during the invasion of the Atlantic basin and selection against freshwater-adapted variants in the sea, both of which have reduced the amount of standing genetic variation available for freshwater adaptation outside the Eastern Pacific region. Moreover, the existence of highly elevated linkage disequilibrium associated with marine-freshwater differentiation in the Eastern Pacific is also consistent with a secondary contact scenario between marine and freshwater populations that have evolved in isolation from each other during past glacial periods. Thus, contrary to what earlier studies focused on Eastern Pacific populations have led us to believe, parallel marine-freshwater differentiation in sticklebacks is far less prevalent and pronounced in all other parts of the species global distribution range.