Phylogeographic history of grey wolves in Europe

Abstract

Background: While it is generally accepted that patterns of intra-specific genetic differentiation are substantially affected by glacial history, population genetic processes occurring during Pleistocene glaciations are still poorly understood. In this study, we address the question of the genetic consequences of Pleistocene glaciations for European grey wolves. Combining our data with data from published studies, we analysed phylogenetic relationships and geographic distribution of mitochondrial DNA haplotypes for 947 contemporary European wolves. We also compared the contemporary wolf sequences with published sequences of 24 ancient European wolves.

Results: We found that haplotypes representing two haplogroups, 1 and 2, overlap geographically, but substantially differ in frequency between populations from south-western and eastern Europe. A comparison between haplotypes from Europe and other continents showed that both haplogroups are spread throughout Eurasia, while only haplogroup 1 occurs in contemporary North American wolves. All ancient wolf samples from western Europe that dated from between 44,000 and 1,200 years B.P. belonged to haplogroup 2, suggesting the long-term predominance of this haplogroup in this region. Moreover, a comparison of current and past frequencies and distributions of the two haplogroups in Europe suggested that haplogroup 2 became outnumbered by haplogroup 1 during the last several thousand years.

Conclusions: Parallel haplogroup replacement, with haplogroup 2 being totally replaced by haplogroup 1, has been reported for North American grey wolves. Taking into account the similarity of diets reported for the late Pleistocene wolves from Europe and North America, the correspondence between these haplogroup frequency changes may suggest that they were associated with ecological changes occurring after the Last Glacial Maximum.

Figure 1

Spatial distribution and phylogenetic relationships between mtDNA haplotypes of contemporary European wolves. Based on 230 bp sequences. (a) Distribution of different wolf haplotypes in Europe, against the background of the current wolf range (based on Ref. [54], modified). (b) Maximum parsimony tree (50% majority rule consensus) of mtDNA haplotypes of European wolves. Bootstrap support, if found in more than 50% of 1000 replicates, is indicated as: stars above the branches for the maximum likelihood tree, stars below the branches for the minimum evolution tree, and "+"above the branches for the maximum parsimony tree. "+" below the branches indicate clade credibility values for the Bayesian tree with a coalescent prior, if higher than 0.5. Two main haplogroups correspond to the main clades of the network. Haplotype w20 has an ambiguous haplogroup assignment. (c) Statistical parsimony network of mtDNA haplotypes of European wolves. Large circles represent the haplotypes and small circles indicate interior nodes that were absent from the sample because of insufficient sampling or extinct haplotypes. Each line represents a single mutational change. Dashed lines denote alternative mutational connections. Similar haplotypes are grouped into nested clades, denoted by rectangles.

Figure 2

Statistical parsimony network of mtDNA haplotypes of worldwide grey wolves. Based on 230 bp sequences. As many alternative mutational connections are present in the network, only the first level clades are presented to make the picture clear. Two dashed line rectangles denote haplotype groups corresponding to clades 1 and 2 from Figure 1c. Haplotypes unique to one continent are marked in one colour, and haplotypes occurring in two continents are marked in two respective colours. Haplotypes of Indian and Himalayan wolves were separated from all the other haplotypes by more than 6 mutational steps, which denoted the threshold of the 95% parsimonious connection.

Figure 3

Distribution of haplogroups 1 and 2 in contemporary and ancient European wolves. The map is based on the authors' data and the data from other studies [13-17,24].

Figure 4

Statistical parsimony network of mtDNA haplotypes of contemporary (black) and ancient (white) European wolves. Based on 57 bp sequences. The contemporary haplotypes come from published studies or GenBank (see Table S1 in Additional file 1), and the ancient haplotypes from Stiller et al. [24]. Three ancient haplotypes are identical to extant haplotypes (black and white). Thin dashed lines denote alternative mutational connections. Two thick dashed line rectangles denote haplogroups corresponding to clades 1 and 2 from Figure 1c.