Global Phylogeographic and Admixture Patterns in Grey Wolves and Genetic Legacy of An Ancient Siberian Lineage

Abstract

The evolutionary relationships between extinct and extant lineages provide important insight into species' response to environmental change. The grey wolf is among the few Holarctic large carnivores that survived the Late Pleistocene megafaunal extinctions, responding to that period's profound environmental changes with loss of distinct lineages and phylogeographic shifts, and undergoing domestication. We reconstructed global genome-wide phylogeographic patterns in modern wolves, including previously underrepresented Siberian wolves, and assessed their evolutionary relationships with a previously genotyped wolf from Taimyr, Siberia, dated at 35 Kya. The inferred phylogeographic structure was affected by admixture with dogs, coyotes and golden jackals, stressing the importance of accounting for this process in phylogeographic studies. The Taimyr lineage was distinct from modern Siberian wolves and constituted a sister lineage of modern Eurasian wolves and domestic dogs, with an ambiguous position relative to North American wolves. We detected gene flow from the Taimyr lineage to Arctic dog breeds, but population clustering methods indicated closer similarity of the Taimyr wolf to modern wolves than dogs, implying complex post-divergence relationships among these lineages. Our study shows that introgression from ecologically diverse con-specific and con-generic populations was common in wolves' evolutionary history, and could have facilitated their adaptation to environmental change.

Figure 1

Distribution of wild canids and free-ranging dogs analysed in this study. (A) Sample distribution across the Holarctic, (B) sample distribution in Europe, (C) distribution range of the grey wolf. Each symbol represents multiple individuals sampled in the same locations. The map does not include samples of black backed jackals (from Namibia), free-ranging dogs from North America (with unknown sampling locations) and pure-bred dogs. For the list of all samples analysed in the study, see Supplementary Table 1. Software used to generate the map: ESRI 2014. ArcGIS Desktop: Release 10.2.2. Redlands, CA: Environmental Systems Research Institute. Shaded relief generated from SRTM DEM 90 m. Countries marked using Natural Earth data (Free vector and raster map data @ naturalearthdata.com). All versions of Natural Earth raster and vector map data are in the public domain. They can be used in any manner without a licence, including modifying the content and design, electronic dissemination, and offset printing. Gray wolf geographic range drawn according to Boitani et al..

Figure 2

Linkage disequilibrium patterns in wolf populations. Linkage disequilibrium is represented by average genotypic association coefficient r² and is plotted as a function of inter-SNP distance. The estimate was carried out for 10 unrelated individuals per population. The data for Mexican wolves were excluded from the plot for clarity, and are presented instead in Supplementary Fig. 1.

Figure 3

Population structure inferred for all canids studied (A,B) and wolves only (C,D) using Admixture and Eigensoft.

Figure 4

Ancestry relationships between the Taimyr wolf and modern wolf and dog populations inferred in TreeMix for (A) the whole set of canid populations, (B) a reduced population set, excluding those with known admixture history, and assuming 10 events of gene flow. Gene flow is represented by arrows, with colours reflecting the intensity of gene flow, from lowest (yellow) to highest (red). Nodes with 95–100% bootstrap support are marked with an asterisk, and nodes with bootstrap support 50–95% are marked with a plus symbol.