The population genomics of repeated freshwater colonizations by Gulf pipefish

How organisms adapt to the novel challenges imposed by the colonization of a new habitat has long been a central question in evolutionary biology. When multiple populations of the same species independently adapt to similar environmental challenges, the question becomes whether the populations have arrived at their adaptations through the same genetic mechanisms. In recent years, genetic techniques have been used to tackle these questions by investigating the genome-level changes underlying local adaptation. Here, we present a genomic analysis of colonization of freshwater habitats by a primarily marine fish, the Gulf pipefish (Syngnathus scovelli). We sample pipefish from four geographically distinct freshwater locations and use double-digest restriction site associated DNA sequencing to compare them to 12 previously studied saltwater populations. The two most geographically distant and isolated freshwater populations are the most genetically distinct, although demographic analysis suggests that these populations are experiencing ongoing migration with their saltwater neighbours. Additionally, outlier regions were found genome-wide, showing parallelism across ecotype pairs. We conclude that these multiple freshwater colonizations involve similar genomic regions, despite the large geographical distances and different underlying mechanisms. These similar patterns are probably facilitated by the interacting effects of intrinsic barriers, gene flow among populations and ecological selection in the Gulf pipefish.