Phylogeography of the brown hare (<i>Lepus europaeus</i>) in Europe: a legacy of south‐eastern Mediterranean refugia?

Stamatis, Costas; Suchentrunk, Franz; Moutou, Katerina A.; Giacometti, Marco; Haerer, Gunther; Djan, Mihajla; Vapa, Ljiljana; Vuković, Marijana; Tvrtković, Nikola; Sert, Hakan; Alves, Paulo C.; Mamuris, Zissis

doi:10.1111/j.1365-2699.2008.02013.x

Cited by 77 publications

(121 citation statements)

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“…Given that hybridization between Lepus species in Europe is a common phenomenon (Alves et al 2003Melo-Ferreira et al 2005Zachos et al 2010) we tried to verify whether hybrids occurred between and among the two Lepus species from Switzerland, searching for mtDNA introgression. Using methods of mtDNA analysis previously described (Stamatis et al, 2007(Stamatis et al, , 2009, we detected seven out of 133 (5.263%) L. europaeus individuals with the most common L. timidus mtDNA haplotype and five out of 92 (5.434%) L. timidus individuals with the most common L. europaeus mtDNA haplotype. Further comparative analysis of MC1R and mtDNA data revealed that the two L. timidus individuals with the L. europaeus MC1R sequence bore also a L. europaeus mtDNA haplotype and the same was true for one of the two heterozygous (L. europaeus/L.…”

Section: Resultsmentioning

confidence: 96%

“…Previous wide-ranged phylogenetic studies using the same set of L. europaeus samples as in the present study and based on both maternally (mtDNA) and/or paternally (SRY) transmitted molecular markers, have shown a deep phylogeographic separation, at least, between Europe and Anatolia (Mamuris et al 2010;Stamatis et al 2008Stamatis et al , 2009. Although several hares from Turkey and especially from the Ş anlıurfa region reported to have a generally yellowish fur, very similar to hares from the semiarid Be'er Sheva region in south-central Israel, north of the Negev desert (Suchentrunk et al 2000;Yom-Tov 1967), MC1R analysis failed to reveal any difference; all Turkish L. europaeus populations surveyed, regardless of their origin, bore the same MC1R allele as the European ones.…”

Section: Discussionmentioning

confidence: 95%

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Analysis of MC1R genetic variation in Lepus species in Mediterranean refugia

et al. 2012

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a b s t r a c tA study on the inter-and intraspecies variation of MC1R gene was performed in Lepus species inhabiting the Mediterranean basin (L. granatansis, L. europaeus, L. corsicanus, L. castroviejoi and L. mediterraneus) and their neighboring species in Europe (L. timidus) and Africa (L. saxatilis, L. capensis), in order to infer microversus macroevolutionary adaptation. Eleven different sequences were isolated that corresponded to five amino acid sequences. Comparison of MC1R nucleotide phylogenetic tree with phylogenies resulting from mtDNA regions of the same species showed absence of congruence between these sets of markers. The Mediterranean area that offered refugia during last glaciation retains more MC1R genotypes compared with populations of North and Central Europe as a consequence of founder effects. L. corsicanus and L. castroviejoi bore identical alleles supportive of their conspecificity, as indicated by other molecular markers. Within L. europaeus, a group of Israeli hares were distinguished by a different MC1R functional allele; additional differences in coat colour and other genetic markers raise doubts about its taxonomic status. Finally, the present data reinforced the idea of bi-directional introgressive hybridization between L. europaeus and L. timidus in Switzerland.

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Section: Resultsmentioning

confidence: 96%

Section: Discussionmentioning

confidence: 95%

Analysis of MC1R genetic variation in Lepus species in Mediterranean refugia

et al. 2012

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“…Starting with Thulin et al[7], several molecular studies have identified patterns of reticulate evolution and paraphyly in a number of Lepus species, both on the intraspecific (e.g., Kasapidis et al[14]; Stamatis et al[15]) and interspecific levels (e.g., Alves et al[8,16], Thulin et al[17], Melo-Ferreira et al[18], Wu et al[19], Fredsted et al[20], Ben Slimen et al[21]; Melo-Ferreira et al[22], Alves et al[23,24], Pietri et al[25], Zachos et al[26], Liu et al[9], Wu et al[27], Melo-Ferreira et al[28], Melo-Ferreira et al[10,11], Mengoni et al[29]). This may add to systematic ambiguity or confusion, particularly if phylogenetic conclusions are based solely on mtDNA data (e.g., Waltari and Cook[30]; Wu et al[19], Ben Slimen et al[31]) or geographically limited sample sizes, or when molecular samples are analyzed without concomitant phenotypic examination.…”

Section: Introductionmentioning

confidence: 99%

Mitochondrial and nuclear DNA reveals reticulate evolution in hares (Lepus spp., Lagomorpha, Mammalia) from Ethiopia

et al. 2017

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For hares (Lepus spp., Leporidae, Lagomorpha, Mammalia) from Ethiopia no conclusive molecular phylogenetic data are available. To provide a first molecular phylogenetic model for the Abyssinian Hare (Lepus habessinicus), the Ethiopian Hare (L. fagani), and the Ethiopian Highland Hare (L. starcki) and their evolutionary relationships to hares from Africa, Eurasia, and North America, we phylogenetically analysed mitochondrial ATPase subunit 6 (ATP6; n = 153 / 416bp) and nuclear transferrin (TF; n = 155 / 434bp) sequences of phenotypically determined individuals. For the hares from Ethiopia, genotype composition at twelve microsatellite loci (n = 107) was used to explore both interspecific gene pool separation and levels of current hybridization, as has been observed in some other Lepus species. For phylogenetic analyses ATP6 and TF sequences of Lepus species from South and North Africa (L. capensis, L. saxatilis), the Anatolian peninsula and Europe (L. europaeus, L. timidus) were also produced and additional TF sequences of 18 Lepus species retrieved from GenBank were included as well. Median joining networks, neighbour joining, maximum likelihood analyses, as well as Bayesian inference resulted in similar models of evolution of the three species from Ethiopia for the ATP6 and TF sequences, respectively. The Ethiopian species are, however, not monophyletic, with signatures of contemporary uni- and bidirectional mitochondrial introgression and/ or shared ancestral polymorphism. Lepus habessinicus carries mtDNA distinct from South African L. capensis and North African L. capensis sensu lato; that finding is not in line with earlier suggestions of its conspecificity with L. capensis. Lepus starcki has mtDNA distinct from L. capensis and L. europaeus, which is not in line with earlier suggestions to include it either in L. capensis or L. europaeus. Lepus fagani shares mitochondrial haplotypes with the other two species from Ethiopia, despite its distinct phenotypic and microsatellite differences; moreover, it is not represented by a species-specific mitochondrial haplogroup, suggesting considerable mitochondrial capture by the other species from Ethiopia or species from other parts of Africa. Both mitochondrial and nuclear sequences indicate close phylogenetic relationships among all three Lepus species from Ethiopia, with L. fagani being surprisingly tightly connected to L. habessinicus. TF sequences suggest close evolutionary relationships between the three Ethiopian species and Cape hares from South and North Africa; they further suggest that hares from Ethiopia hold a position ancestral to many Eurasian and North American species.

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“…In the Iberian Peninsula, this species is restricted to the Pyrenean foothills, but has a broad distribution north of the Pyrenees. This species likely invaded Iberia only when it colonised Western Europe (Stamatis et al, 2009) after the last glacial maximum, a period characterised by major range changes of numerous European taxa promoted by deglaciation (Hewitt, 2000). Iberian populations of this species harbour very high frequencies of mtDNA of L. timidus origin, which appears almost fixed (Melo-Ferreira et al, 2005;Alves et al, 2008).…”

Section: Introductionmentioning

confidence: 99%

Home-loving boreal hare mitochondria survived several invasions in Iberia: the relative roles of recurrent hybridisation and allele surfing

et al. 2013

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Genetic introgression from a resident species into an invading close relative can result from repeated hybridisation along the invasion front and/or allele surfing on the expansion wave. Cases where the phenomenon is massive and systematic, such as for hares (genus Lepus) in Iberia, would be best explained by recurrent hybridisation but this is difficult to prove because the donor populations are generally extinct. In the Pyrenean foothills, Lepus europaeus presumably replaced Lepus granatensis recently and the present species border is parallel to the direction of invasion, so that populations of L. granatensis in the contact zone represent proxies of existing variation before the invasion. Among three pairs of populations sampled across this border, we find less differentiation of mitochondrial DNA (mtDNA) across than along it, as predicted under recurrent hybridisation at the invasion front. Using autosomal microsatellite loci and X-and Y-linked diagnostic loci, we show that admixture across the border is quasi-absent, making it unlikely that lack of interspecific mtDNA differentiation results from ongoing gene flow. Furthermore, we find that the local species ranges are climatically contrasted, making it also unlikely that ongoing ecologydriven movement of the contact account for mtDNA introgression. The lack of mtDNA differentiation across the boundary is mostly due to sharing of mtDNA from a boreal species currently extinct in Iberia (Lepus timidus) whose mitochondria have thus remained in place since the last deglaciation despite successive invasions by two other species. Home-loving mitochondria thus witness past species distribution rather than ongoing exchanges across stabilised contact zones.

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Phylogeography of the brown hare (Lepus europaeus) in Europe: a legacy of south‐eastern Mediterranean refugia?

Abstract: Aim We analysed the population genetics of the brown hare (Lepus europaeus) in order to test the hypothesis that this species migrated into central Europe from a number of late glacial refugia, including some in Asia Minor.Location Thirty-three localities in Greece,

Cited by 77 publications

References 41 publications

Analysis of MC1R genetic variation in Lepus species in Mediterranean refugia

Analysis of MC1R genetic variation in Lepus species in Mediterranean refugia

Mitochondrial and nuclear DNA reveals reticulate evolution in hares (Lepus spp., Lagomorpha, Mammalia) from Ethiopia

Home-loving boreal hare mitochondria survived several invasions in Iberia: the relative roles of recurrent hybridisation and allele surfing

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