Ancient DNA of narrow-headed vole reveal common features of the Late Pleistocene population dynamics in cold-adapted small mammals

Abstract

The narrow-headed vole, collared lemming and common vole were the most abundant small mammal species across the Eurasian Late Pleistocene steppe-tundra environment. Previous ancient DNA studies of the collared lemming and common vole have revealed dynamic population histories shaped by climatic fluctuations. To investigate the extent to which species with similar adaptations share common evolutionary histories, we generated a dataset comprised the mitochondrial genomes of 139 ancient and 6 modern narrow-headed voles from several sites across Europe and northwestern Asia covering approximately the last 100 thousand years (kyr). We inferred Bayesian time-aware phylogenies using 11 radiocarbon-dated samples to calibrate the molecular clock. Divergence of the main mtDNA lineages across the three species occurred during marine isotope stages (MIS) 7 and MIS 5, suggesting a common response of species adapted to open habitat during interglacials. We identified several time-structured mtDNA lineages in European narrow-headed vole, suggesting lineage turnover. The timing of some of these turnovers was synchronous across the three species, allowing us to identify the main drivers of the Late Pleistocene dynamics of steppe- and cold-adapted species.

Ancient DNA Contradicts the Presence of Social Voles (Genus Microtus, Subgenus Sumeriomys) in the Late Pleistocene of Western Europe

“…The reconstructed intraspecific phylogeny of narrow-headed voles was similar to the previous ones [7] and revealed three main lineages corresponding to the Asiatic S. gregalis and S. raddei (Polyakov, 1881) and the European S. anglicus (Figure 3A). Six lineages were distinguished (AA-AF) within the S. anglicus clade.…”

“…The AF lineage was widespread in Europe until ca. 40 ka ago, but later it became confined to southwestern France [7]. The reconstructed intraspecific phylogeny of narrow-headed voles was sim previous ones [7] and revealed three main lineages corresponding to the Asiatic lis and S. raddei (Polyakov, 1881) and the European S. anglicus (Figure 3A).…”

“…We used this fragment because it was the only one available for the specimen identified as M. arvalis. We used previously published intraspecific mitogenomic datasets on the common vole (Microtus arvalis) [29] and the European narrowheaded vole (Stenocranius anglicus) [7] to estimate the phylogenetic position and age of the samples using the tip-dating approach [31]. The common vole dataset consisted of 199 sequences of 4.2 kb fragment of mtDNA.…”

“…First the age of each specimen was estimated in separate analyses using sequences of modern and radiocarbon-dated specimens to calibrate the molecular clock before we ran joint analysis using the whole dataset. In this analysis we fixed ages of not dated specimens to the values estimated previously [7,29] and we set lognormal priors on the ages of the specimens from Les Petits Guinards based on the results of individual age estimations (see Supplementary Information for more details).…”

“…Molecular tools have been successfully used to study the demographic history of small mammals from the Late Pleistocene and both morphological and molecular data should be coupled whenever possible. Recent studies of ancient mitochondrial DNA (mtDNA) allowed revision of the taxonomic status of the Late Pleistocene European narrow-headed vole and ranking it as Stenocranius anglicus (Hinton, 1910), a species distinct from the Asiatic Stenocranius gregalis (Pallas, 1779) [6,7]. In another case, among Late Pleistocene grey voles (subgenus Microtus) from southeastern Europe, a new cryptic species was discovered representing a divergent lineage of the Tien Shan vole (Microtus ilaeus Thomas, 1912) [8].…”