Abstract
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.
Highlights
Hares and jackrabbits are a difficult group, systematically, due to their large intraspecific phenotypic variation, their wide phenotypic overlap among species (e.g., Angermann[1,2], Palacios[3,4], Flux and Angermann[5]; see Suchentrunk et al [6]), and their shallow evolutionary divergence with the possibility of reticulate evolution (e.g., Thulin et al.[7], Alves et al.[8], Liu et al.[9], Melo-Ferreira et al [10,11])
All hares collected in Ethiopia, except for one neonate from the Abjiata Shala National Park (AB) and one subadult from Assosa (AS, Fig 1) could be unambiguously assigned phenotypically to one of the following three species: Ethiopian Hare, L. fagani Thomas, 1902; Abyssinian Hare, L. habessinicus Hemprich and Ehrenberg, 1832; Ethiopian Highland Hare, L. starcki Petter, 1963 [1, 60, 5]
We noticed similarities between the presently examined phenotypes and forms of East African cape hares, L. capensis L., 1758 or savanna hares, L. victoriae Thomas, 1893 as described by Flux and Flux [117] and the forms described by Azzaroli-Puccetti [57,58]
Summary
Hares and jackrabbits (genus Lepus; Leporidae; order Lagomorpha; Mammalia) are a difficult group, systematically, due to their large intraspecific phenotypic variation, their wide phenotypic overlap among species (e.g., Angermann[1,2], Palacios[3,4], Flux and Angermann[5]; see Suchentrunk et al [6]), and their shallow evolutionary divergence with the possibility of reticulate evolution (e.g., Thulin et al.[7], Alves et al.[8], Liu et al.[9], Melo-Ferreira et al [10,11]). 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, 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
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