Serial population extinctions in a small mammal indicate Late Pleistocene ecosystem instability

Abstract

The Late Pleistocene global extinction of many terrestrial mammal species has been a subject of intensive scientific study for over a century, yet the relative contributions of environmental changes and the global expansion of humans remain unresolved. A defining component of these extinctions is a bias toward large species, with the majority of small-mammal taxa apparently surviving into the present. Here, we investigate the population-level history of a key tundra-specialist small mammal, the collared lemming (Dicrostonyx torquatus), to explore whether events during the Late Pleistocene had a discernible effect beyond the large mammal fauna. Using ancient DNA techniques to sample across three sites in North-West Europe, we observe a dramatic reduction in genetic diversity in this species over the last 50,000 y. We further identify a series of extinction-recolonization events, indicating a previously unrecognized instability in Late Pleistocene small-mammal populations, which we link with climatic fluctuations. Our results reveal climate-associated, repeated regional extinctions in a keystone prey species across the Late Pleistocene, a pattern likely to have had an impact on the wider steppe-tundra community, and one that is concordant with environmental change as a major force in structuring Late Pleistocene biodiversity.

Fig. 1.

The locations of the three archaeological sites from which samples of D. torquatus used in our analyses were recovered. Symbols represent the approximate geographical locations: ▲, Bridged Pot Cave; ■, Trou Al’Wesse; ●, Caverne Marie-Jeanne.

Fig. 2.

Phylogeny for mtDNA haplotypes (cyt b) of D. torquatus with corresponding AMS dates and stratigraphic locations for the samples used in this study. Phylogeny: numbers above branches represent Bayesian posterior probabilities. The outgroup D. hudsonius is removed for display purposes. M, modern samples (GenBank); H, haplotype (ancient sample). Symbols indicate the source archaeological site for each sample: triangle, Bridged Pot Cave; circle, Caverne Marie-Jeanne; square, Trou Al’Wesse. Symbol colors indicate the stratigraphic location of the sample within each of the archaeological sites, L, layer (site specific number). Schematic stratigraphic columns represent an approximate position of the layers sampled from each site and the approximate relation of those layers across sites.

Fig. 3.

Bayesian-derived highest probability ranges for the periods of lineage turnover of D. torquatus, based on AMS dated samples. Collared lemming lineage turnover events are shaded red and labeled A–D; gray box: M. primigenius absence, from AMS dated samples (21). cal BP, calibrated years Before Present; GI, Greenland Interstadials; NGRIP ¹⁸O, NorthGRIP ¹⁸O data (19).