Genetic analyses of brown hare (Lepus europaeus) support limited migration and translocation of Greek populations

Abstract

Numerous studies have shown that the phylogeography of many species, including European brown hare, has been affected by the climatic oscillations of the Pleistocene. During this period the Balkans acted as a major refugium offering habitable conditions for many species. However, few studies have focused on the specific role of the Greek peninsula in the phylogeographic history of species in this southernmost margin of Balkans. We, therefore analyzed a 528 bp fragment of the D-loop region of mitochondrial DNA in 154 wild brown hare individuals from unsampled areas from both mainland and island Greece and compared it to 310 available brown hare sequences (including 110 Greek samples). Newly identified haplotypes show characteristic distribution in specific Greek areas reinforcing the theory that Greece can be considered as a subrefuge within Balkans for a number of species, with several “refugia within refugia” spots, holding significant genetic diversity. No haplotypes from wild Greek individuals clustered with the Central and Western Europe group revealing a minimal contribution of this area to the colonization of central Europe. One hundred and ten reared brown hares were also analyzed to elucidate the impact of introductions on local populations. Most of these samples presented close genetic affinity with haplotypes from Central and Western Europe indicating that farms in Greece use breeders from those areas. Therefore, despite human translocation of individuals, the genetic structure of brown hare has mostly been influenced by paleoclimatic conditions and minimally by human actions.

Lepus europaeus(Lagomorpha: Leporidae)

“…Data from a broad genetic analysis of L. europaeus specimens (n = 154) from mainland and island populations in Greece as well as captive-reared individuals (n = 110) were compared with existing sequences (n = 310, includes the 110 captive-reared individuals) retrieved from GenBank with the aim to create a pan-European analysis (Minoudi et al 2018). The results confirm the deviation of the phylogenetic tree into two clades, the Anatolian and the European.…”

Population genetics analysis of Tolai hares (Lepus tolai) in Xinjiang, China using genome-wide SNPs from SLAF-seq and mitochondrial markers

“…At the genome-wide level, the genetic diversity of Tolai hares based on SNPs was higher (Table 2) (π = 0.05926, He = 0.37412, Ho = 0.40226, PIC = 0.2974) than that of other reported species, including rabbits (PIC = 0.2-0.2281, He = 0.2511-0.2857, Ho = 0.3072-0.3418, (Ren et al, 2019), and Yarkand hares (π = 0.0655, He = 0.3130, Ho = 0.2852, PIC = 0.2543 (Ababaikeri et al, 2021). The estimated nucleotide diversity of Tolai hares (π = 0.0442) based on mtDNA was also relatively high compared to other Lepus taxa, such as brown hares (π D-LOOP = 0.030, (Minoudi et al, 2018), Yarkand hares (π D-LOOP = 0.033, π CYTB = 0.008, (Shan et al, 2011), and Italian hares (L. corsicanus, π D-LOOP = 0.018, (Pierpaoli et al, Frontiers in Genetics frontiersin.org 2003). These higher genetic diversity values indicated that Tolai hare populations evolved under long-term favorable environmental conditions and remained relatively stable and genetically variable (Pironon et al, 2017).…”

“…Unlike other species in Europe and eastern China, such as the Brown hare (Minoudi et al, 2018), Panda (Ailuropoda melanoleuca) (Zhao et al, 2013), and Lizards (Shinisaurus crocodilurus) (Xie et al, 2022), our comprehensive indexes of two markers showed that L. t. lehmanni population remained stable, even in the LGM (0.0265-0.019 MYA) (Clark et al, 2009;Liang et al, 2017). Other studies have shown that among the Tibetan Plateau species, population size did not decline in the LGM (Liang et al, 2017), implying that the geographical distribution of species and climate oscillation indeed play an important role in population history.…”

“…Climate factors and habitat environment will profoundly impact the evolution of biological populations, thus leaving historical traces in the genetic diversity, population structure, distribution pattern, and other aspects of today's populations. For example, climate changes profoundly affected phylogeographic structure and the evolutionary history of brown hares (L. europaeus) by isolating populations in the distinct refugia where they adapted and differentiated in allopatry, leading to genome incompatibilities (Djan et al, 2017;Minoudi et al, 2018;Giannoulis et al, 2019). The southwest of Tarim Basin in Xinjiang, China, as the origin of rivers in the basin, was a glacial refugia for Yarkand hares (L. yarkandensis) during the Quaternary climate oscillations, providing a suitable environment for maintaining the relatively high genetic diversity of this species (Shan et al, 2011).…”

Common patterns in the molecular phylogeography of western palearctic birds: a comprehensive review

“…In regard to other fauna and flora taxa inhabiting the Western Palearctic, certain degrees of genetic variation can be observed and very often, individuals can be linked to certain populations or geographic areas. This is illustrated by recent studies on Brown Hares (Lepus europaeus) (Minoudi et al 2018), Stone Martins (Martes foina) (Tsoupas et al 2019), plus Balkan Mole (Talpa stankovici) and European Mole (Talpa europaea) (Tryfonopoulos et al 2010), which revealed that populations from the Balkans have region specific haplotypes. However, the Wild Cat (Felis silvestris) only shows five main geographic groups across the whole of Europe, with some populations hybridizing with domestic cats (Mattucci et al 2016).…”