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. 2017 Aug 2;12(8):e0180137.
doi: 10.1371/journal.pone.0180137. eCollection 2017.

Mitochondrial and Nuclear DNA Reveals Reticulate Evolution in Hares (Lepus Spp., Lagomorpha, Mammalia) From Ethiopia

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Mitochondrial and Nuclear DNA Reveals Reticulate Evolution in Hares (Lepus Spp., Lagomorpha, Mammalia) From Ethiopia

Zelalem Tolesa et al. PLoS One. .
Free PMC article

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.

Conflict of interest statement

Competing Interests: The authors have declared that no competing interests exist.

Figures

Fig 1
Fig 1. Geographical sample distribution.
Full red circles–Lepus habessinicus, full brown triangles–L. fagani, full blue squares–L. starcki. Open symbols indicate geographical positions of respective holotypes; also given are acronyms of sample localities (for details see Table 1).
Fig 2
Fig 2. Median joining network of ATP6 haplotypes.
Haplotypes (pies) are proportional to total sample number, taxon assignments of single haplotypes (pie slices) represent percentages of taxa per haplotype. Black dots indicate inferred haplotypes, not revealed presently, numbers associated with lines give numbers of substitutions between any two haplotypes/inferred haplotypes, if more than one (single mutational steps between any two haplotypes are not indicated). Evolutionary distances between haplotypes are only roughly in proportional scale. Taxa acronyms: cn–Lepus capensis, North Africa, cs–L. capensis, South Africa, e–L. europaeus, f–L. fagani, h–L. habessinicus, s–L. starcki, x–L. saxatilis, Lsp.–phenotypically undetermined hare specimen.
Fig 3
Fig 3. Bayesian dendrogram of mtATP6 haplotypes.
Node support above 50% is given for Bayesian Inference, ML, and NJ analyses, respectively. For details see “Material and methods”.
Fig 4
Fig 4. Median joining network of TF haplotypes.
Haplotypes (pies) are proportional to the total sample number, taxon assignments of single haplotypes (pie slices) represent percentages of taxa per haplotype. Black dots indicate inferred haplotypes, not revealed presently, numbers associated with lines give numbers of substitutions between any two haplotypes/inferred haplotypes, if more than one; single mutational steps between any two haplotypes are not indicated. Evolutionary distances between haplotypes are only roughly in proportional scale. Taxa acronyms: cn–Lepus capensis, North Africa, cs–L. capensis, South Africa, f–L. fagani, h–L. habessinicus, s–L. starcki, x–L. saxatilis, Lsp.–phenotypically undetermined hare specimen, cc–L. capensis, China, co–L. comus, hn–L. hainanus, m–L. mandshuricus, si–L. sinensis, oi–L. oiostolus, y–L. yarkandensis, a–L. arcticus, am–L. americanus, cf–L. californicus, cj–L. castroviejoi, cr–L. corsicanus, e–L. europaeus, g–L. granatensis, o–L. othus, t–L. timidus, tw–L. twonsendii, sf–Sylvilagus floridanus, Oc–Oryctolagus cuniculus.
Fig 5
Fig 5. Bayesian dendrogram of TF haplotypes.
Node support above 50% is given for Bayesian Inference, ML, and NJ analyses (for details see “Materials and methods” section). Acronyms of taxa: a–Lepus arcticus, am–L. americanus, c–L. comus, cc–L. capensis, China, cf–L. californicus, cj–L. castroviejoi, cn–L. capensis, North Africa, cr–L. corsicanus, cs–L. capensis, South Africa, e–L. europaeus, f–L. fagani, h–L. habessinicus, hn–L. hainanus, m–L. mandshuricus, o–L. othus, oi–L. oiostolus, s–L. starcki, si–L. sinensis, t–L. timidus, tw–L. townsendii, x–L. saxatilis, y–L. yarkandensis, Oc–Orycotlagus cuniculus, Sf–Sylvilagus floridanus.
Fig 6
Fig 6. Microsatellite-based Bayesian structure and admixture analysis of the genotypes of the three Ethiopian hare species.
Model results are based on A: 12 loci, correlated allele frequencies, and no species priors, B: 12 loci, correlated allele frequencies, species priors, C: 8 loci, correlated allele frequencies, no species priors, D: 8 loci, correlated allele frequencies, species priors. For more details see “Material and methods”.

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Grant support

Substantial financial support was provided by Wildlife Research - Franz Suchentrunk/Vienna nr. 4/2009. In addition FS was involved in the conceptualization, study design, data analysis, decision to publish and preparation of the manuscript.
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