The evolutionary history of the Cape hare (Lepus capensis sensu lato): insights for systematics and biogeography

Abstract

Inferring the phylogeography of species with large distributions helps deciphering major diversification patterns that may occur in parallel across taxa. Here, we infer the evolutionary history of the Cape hare, Lepus capensis sensu lato, a species distributed from southern Africa to Asia, by analyzing variation at 18 microsatellites and 9 DNA (1 mitochondrial and 8 nuclear) sequenced loci, from field and museum-collected samples. Using a combination of assignment and coalescent-based methods, we show that the Cape hare is composed of five evolutionary lineages, distributed in distinct biogeographic regions-north-western Africa, eastern Africa, southern Africa, the Near East and the Arabian Peninsula. A deep phylogenetic break possibly dating to the Early Pleistocene was inferred between the African and Asian L. capensis groups, and the latter appear more closely related to other Eurasian hare species than to African Cape hares. The inferred phylogeographic structure is shared by numerous taxa distributed across the studied range, suggesting that environmental changes, such as the progressive aridification of the Saharo-Arabian desert and the fluctuations of savannah habitats in Sub-Saharan Africa, had comparable impacts across species. Fine-scale analyses of the western Sahara-Sahel populations showed rich fragmentation patterns for mitochondrial DNA but not for microsatellites, compatible with the environmental heterogeneity of the region and female philopatry. The complex evolutionary history of L. capensis sensu lato, which possibly includes interspecific gene flow, is not reflected by taxonomy. Integrating evolutionary inference contributes to an improved characterization of biodiversity, which is fundamental to foster the conservation of relevant evolutionary units.

Fig. 1

Geographic distribution of Lepus capensis and samples unambiguously attributed to a microsatellite cluster. Gray background indicates the distribution of L. capensis according to IUCN Red List (www.redlist.org). Symbols indicate sampling localities: shapes indicate the eight mtDNA lineages (according to the BAPS and network analyses, which agrees with the phylogenetic inference shown in Fig. 2) and their gray shades depict the five evolutionary groups inferred from microsatellites (see Fig. S1). Symbols are not proportional to the number of individuals samples in the locality and more than one specimen may be represented in each geographical point. Arrows indicate hypothesized dispersal corridors in the Sahara-Sahel—Atlantic Sahara, Nile River and Red Sea mountains (Brito et al. 2014)

Fig. 2

Bayesian inference mtDNA phylogeny (cytochrome b) of L. capensis, L. saxatilis and Eurasian hare species (L. timidus, L. europaeus and L. granatensis), rooted by a rabbit (Oryctolagus cuniculus) haplotype. Bayesian posterior probabilities and maximum likelihood bootstrap supports (scaled from 0 to 1) are shown next to nodes when the first is above 0.50 (Bayesian/Maximum likelihood inferences). L. capensis clades agree with those depicted in Fig. 1

Fig. 3

Nuclear DNA species tree inferred from eight nuclear loci (posterior probabilities are shown on the right of each node), including a African and non-African populations of L. capensis and Eurasian Lepus species and b excluding South African and Chinese populations, for which not all loci were sequenced. Estimates of split times in units of million years (Ma) are indicated for L. capensis sensu lato nodes supported by posterior probabilities above 0.95 (95% confidence intervals shown in brackets)

Fig. 4

Distribution of empirical and simulated uncorrected p-distances between European L. europaeus and the Near East L. capensis population. Simulations were conducted based on population parameters estimated with the isolation-with-migration multi-locus analysis. Gray bars show the distribution of minimum pairwise uncorrected p-distances per simulation between L. europaeus and the Near East L. capensis population (the vertical line indicates the 5th percentile) and black bars depict the empirical pairwise p-distances between the same populations