The evolutionary history of the field vole species complex revealed by modern and ancient genomes

Abstract Background The field vole, an abundant and widespread microtine rodent, is a complex comprised of three cryptic species: the short-tailed field vole (Microtus agrestis) which is present over much of Eurasia, the Mediterranean field vole (Microtus lavernedii) in southern Europe, and the Portuguese field vole (Microtus rozianus) in western Spain and Portugal. Previous research has shown high genomic differentiation of these three lineages. However, the details of the process underlying their divergence remain unknown. Results We analyse 70 mitogenomes and 16 nuclear genomes of modern specimens, and 83 mitogenomes and 12 nuclear genomes of ancient specimens spanning the last 75 thousand years (ka). We estimate the divergence of Portuguese from short-tailed and Mediterranean field voles to be ca. 220 ka ago and of the latter two species to be ca. 110 ka ago, earlier than previous estimates involving only modern sequences. The divergence times we obtain match those between major mitochondrial lineages of cold-adapted and steppe rodents in Europe. We find signatures of gene flow within and between field vole lineages, with some analyses suggesting a hybrid origin of the Mediterranean lineage. Ancient specimens from the Italian Peninsula reveal a previously unrecognised lineage that show evidence of genetic exchange with other populations. Conclusions The pattern of genetic variation in the field vole species complex demonstrates the impact of stadial-interstadial cycles in generating recurrent episodes of allopatry and connectivity of populations, a situation which could only be revealed by our dense genomic sampling over time.