Phylogeography of the prickly sculpin (Cottus asper) in north-western North America reveals parallel phenotypic evolution across multiple coastal–inland colonizations

Aim Glacial cycles during the Pleistocene may have frequently contributed to parallel evolution of phenotypes across independently evolving genetic lineages associated with separate glacial refugia. Previous studies based on morphology suggested that the prickly sculpin (Cottus asper) survived the Last Glacial Maximum (LGM) in southern coastal and inland refugia, favouring allopatric divergence between coastal and inland prickling phenotypes, which vary in the degree to which spine-like scales cover the body of the fish. Herein, we aimed to test whether parallel evolution across multiple genetic lineages rather than a single-lineage origin of highly prickled inland sculpins could serve as an explanation for the biogeographical distribution of prickling phenotypes. Location North-western North America, Southeast Alaska and Canada (British Columbia). Methods We used data from mitochondrial haplotypes and 19 microsatellite loci to identify distinct genetic lineages as a basis to interpret patterns of phenotypic evolution. Results The occurrence of multiple mtDNA groups suggests that highly prickled inland phenotypes comprise more than one genetic lineage. Both mtDNA and microsatellite data are consistent with post-glacial dispersal along the coast and repeated coastal to inland colonization events, as opposed to inland dispersal of a single lineage from a southern refugium to northern regions. Main conclusions Our results suggest that highly prickled inland phenotypes evolved repeatedly following multiple inland colonization events, probably via coastal rivers. The prickly sculpin therefore provides an example of recent (post-glacial) parallel evolution, potentially facilitated by standing genetic variation already present in the ancestral coastal populations