Large-scale mitochondrial DNA analysis reveals new light on the phylogeography of Central and Eastern-European Brown hare (Lepus europaeus Pallas, 1778)

Abstract

European brown hare, Lepus europaeus, from Central and Eastern European countries (Hungary, Poland, Serbia, Lithuania, Romania, Georgia and Italy) were sampled, and phylogenetic analyses were carried out on two datasets: 1.) 137 sequences (358 bp) of control region mtDNA; and 2.) 105 sequences of a concatenated fragment (916 bp), including the cytochrome b, tRNA-Thr, tRNA-Pro and control region mitochondrial DNA. Our sequences were aligned with additional brown hare sequences from GenBank. A total of 52 and 51 haplotypes were detected within the two datasets, respectively, and assigned to two previously described major lineages: Anatolian/Middle Eastern (AME) and European (EUR). Furthermore, the European lineage was divided into two subclades including South Eastern European (SEE) and Central European (CE). Sympatric distribution of the lineages of the brown hare in South-Eastern and Eastern Europe revealed contact zones there. BAPS analysis assigned sequences from L. europaeus to five genetic clusters, whereas CE individuals were assigned to only one cluster, and AME and SEE sequences were each assigned to two clusters. Our findings uncover numerous novel haplotypes of Anatolian/Middle Eastern brown hare outside their main range, as evidence for the combined influence of Late Pleistocene climatic fluctuations and anthropogenic activities in shaping the phylogeographic structure of the species. Our results support the hypothesis of a postglacial brown hare expansion from Anatolia and the Balkan Peninsula to Central and Eastern Europe, and suggest some slight introgression of individual haplotypes from L. timidus to L. europaeus.

Positive selection and precipitation effects on the mitochondrial NADH dehydrogenase subunit 6 gene in brown hares (Lepus europaeus) under a phylogeographic perspective

“…Particularly the study of Djan et al [21] also suggested a long lasting ancestral population history in the Anatolian Peninsula [29], a subsequent population expansions in the southeastern and southern Balkans, and a relative young population expansion into central and northern/northwestern continental Europe. Additional population expansion in eastern Europe, probably from southwestern Eurasian regions with lineages phylogenetically closely related to those found on the Anatolian Peninsula and other regions in the Near East were particularly suggested by Ashrafzadeh et al [20]. Those latter mentioned lineages have, however, so far not managed to expand much towards central Europe; rather their western front does not seem to extend much further west than eastern Poland and the Ukraine.…”

“…The latter has acted as a source region for further colonization of the Balkan Peninsula and later on–after the last glacial maximum (ca. 18.000 ybp)–to central Europe [20–22, 24]. Particularly the study of Djan et al [21] also suggested a long lasting ancestral population history in the Anatolian Peninsula [29], a subsequent population expansions in the southeastern and southern Balkans, and a relative young population expansion into central and northern/northwestern continental Europe.…”

“…Brown hares ( Lepus europaeus ) are widespread throughout Europe and Asia Minor and other parts of western and southwestern Eurasia, occurring in a variety of environments with a considerable ecological plasticity (see e.g., [19]). MtDNA-based phylogeographic and ancient demographic data indicate distinct regional evolutionary units for this species [20–25], despite relatively little changes (i.e., high gene flow) across larger geographical distances in the nuclear genome [26–35]. According to the phylogeographic model based on non-coding D-loop sequences of the mtDNA proposed by Djan et al [21], the southeastern central Balkans has been identified as the source of all populations of the southern and northern Balkans, while populations from central and northwestern Europe have originated from the northern Balkans, and all Balkan lineages have been derived from evolutionarily older lineages from the Anatolian Peninsula.…”

“…According to the phylogeographic model based on non-coding D-loop sequences of the mtDNA proposed by Djan et al [21], the southeastern central Balkans has been identified as the source of all populations of the southern and northern Balkans, while populations from central and northwestern Europe have originated from the northern Balkans, and all Balkan lineages have been derived from evolutionarily older lineages from the Anatolian Peninsula. Additional routes of hares colonizing eastern and northeastern Europe via west or east of the Black Sea are suggested by Strzala et al [36] and Ashrafzadeh et al [20]. As the mtDNA genetically represents a haploid, maternally inherited linkage group with a high mutation rate, with no or very little recombination, it can be expected that genetic differentiation in other mtDNA genes, such as MT-ND6 , will follow the same signal of phylogeographic partitioning as observed for D-loop lineages.…”

Mitogenome Phylogeny Including Data from Additional Subspecies Provides New Insights into the Historical Biogeography of the Eurasian lynx Lynx lynx

“…Clade B likely colonized Europe along a southern route. This route was probably via the Bosphorus junction while sea levels had receded during glacial maxima, as has been inferred for other species [14,30,64,65]. This could explain why the diversification in clade B preceded the one in clade C by ~5 ky (Fig.…”