Lasting through the ice age: The role of the proglacial refugia in the maintenance of genetic diversity, population growth, and high dispersal rate in a widespread freshwater crustacean

Abstract

Abstract The severe climatic changes during the Pleistocene ice ages have shaped the genetic structure and distribution of biota in Europe. We aimed to reveal in detail the genetic diversity, geographical population structure, historical and present demography, migration patterns, and the presence of possible glacial refugia within the nominative subspecies Asellus aquaticus aquaticus. We analysed DNA sequences of the mitochondrial cytochrome c oxidase subunit I gene and nuclear noncoding internal transcribed spacer II region, from populations inhabiting post‐glacial Europe (from the British Isles and Scandinavia to the northern Mediterranean and Black Sea coasts). The origin of the taxon, including establishment in the Dinaric Western Balkans, dates to the Middle/Late Pliocene, but most of its genetic diversity emerged during the Middle/Late Pleistocene before the Last Glacial Maximum. Despite the general absence of spatial genetic structure with population growth, we discovered two different phylogeographic stories across 11 clusters revealed by a coalescent approach. Firstly, the periglacial cluster group—spatially restricted mainly to the northern Balkans, Pannonian Basin, and Pontic Region—is older and more divergent. It apparently retained a relatively stable population size during the glacial‐interglacial cycles. Conversely, the proglacial cluster group—widely distributed in areas close to the glacier margins (north of the Alps, Sudetes, Carpathians) and in the Pannonian Basin—is younger and composed of closely related individuals. It originated in Pleistocene and lasted continuously through the Last Glacial Maximum in numerous high latitude refugia. This was probably due to the vast network of proglacial lakes and rivers, which played a crucial role in the maintenance of genetic diversity, population growth, and high dispersal rate. The evolutionary history of A. a. aquaticus reveals unexpected patterns and is an important lesson when making predictions for other aquatic taxa. Our results suggest that we should stop perceiving the proglacial habitats as lifeless ice desert.