Drift and Selection in a Recently Colonized Sea: The Genomic Basis of Adaptation to Low-Salinity Waters in Baltic Harbour Porpoises.

Understanding how demography and natural selection interact during colonization of novel environments is a central question in evolutionary biology. The Baltic Sea region combines one of the world's strongest salinity gradients with a well-characterized postglacial history of less than ~12,000 years. The harbour porpoise (Phocoena phocoena) is distributed across this gradient as three populations-the North Sea, Belt Sea and Proper Baltic Sea populations. Using whole genome resequencing data from 59 individuals, we reconstructed the demographic history of Baltic colonization and identified genomic signatures of local adaptation. Demographic modelling supported a sequential colonization in which the Belt Sea population diverged first from an ancestral North Sea population, followed by an independent divergence of the Proper Baltic Sea population, with two equally supported timing hypotheses placing initial colonization either during the Yoldia Sea (~11,800 years ago) or the Baltic Sea period (~8000 years ago). The Proper Baltic Sea population showed drift-dominated divergence consistent with a founder effect, while two discrete genomic islands of differentiation with selective sweep signatures were identified between North and Belt Sea populations, pointing to recent positive selection. Both regions contain osmoregulatory candidate genes, most notably SCNN1D, encoding part of the epithelial Na+ channels, a key regulator of sodium homeostasis. A non-synonymous mutation in SCNN1D showed striking allele frequency divergence along the salinity gradient, confirmed across ~400 individuals. Together, these results reveal how genetic drift and divergent selection interact to drive rapid adaptation to a brackish environment, and identify SCNN1D as a compelling candidate for cetacean osmoregulatory adaptation.