Identification of Local- and Habitat-Dependent Selection: Scanning Functionally Important Genes in Nine-Spined Sticklebacks (Pungitius pungitius)

Abstract

Understanding the selective forces promoting adaptive population divergence is a central issue in evolutionary biology. The role of environmental salinity in driving adaptation and evolution in aquatic organisms is still poorly understood. We investigated the relative impacts of habitat type (cf. saltwater vs. freshwater) and geographic area in shaping adaptive population divergence, as well as genes responsible for adaptation to different salinities in nine-spined sticklebacks (Pungitius pungitius). To this end, we employed a hitchhiking mapping approach with 111 microsatellite loci and one insertion/deletion locus including 63 loci situated within or close to genes with important physiological functions such as osmoregulation, growth, and thermal response. Using three pairs of marine and freshwater populations from different geographic areas, we identified several loci showing consistent evidence of being under directional selection in different outlier tests. Analyses of molecular variance at the loci under selection indicated that geographic area rather than habitat type has been acting as a central force in shaping adaptive population divergence. Nevertheless, both outlier tests and a spatial analysis method indicated that two loci (growth hormone receptor 2 and DEAD box polypeptide 56) are involved in adaptation to different habitats, implying that environmental salinity has been affecting them as a selective force. These loci are promising candidates for further investigations focusing on the molecular mechanisms of adaptation to marine and freshwater environments.