The ubiquitous mountain hare mitochondria: multiple introgressive hybridization in hares, genus Lepus

Abstract

Climatic oscillations during the glaciations forced dramatic changes in species distributions, such that some presently temperate regions were alternately occupied by temperate and arctic species. These species could have met and hybridized during climatic transitions. This phenomenon happened for three hare species present in Iberia (Lepus granatensis, Lepus europaeus and Lepus castroviejoi), which display high frequencies of mitochondrial DNA (mtDNA) from Lepus timidus, an arctic/boreal species presently extinct in Iberia. Here, we extend our previous geographical survey to determine whether the distribution of this mtDNA lineage extends beyond the northern half of the Iberian Peninsula, where it is found at high frequencies. We also review the taxonomy, distribution and molecular phylogeny of the genus Lepus. The phylogenetic inference reveals the presence of L. timidus-like mtDNA in several other hare species in Asia and North America, suggesting that the mitochondrial introgression observed in Iberia might be generalized. Comparison with the available nuclear gene phylogenies suggests that introgression could have happened repeatedly, possibly during different climatic transitions. We discuss demographic and adaptive scenarios that could account for the repetition in time and space of this spectacular phenomenon and suggest ways to improve our understanding of its determinants and consequences. Such high levels of introgressive hybridization should discourage attempts to revise hare taxonomy based solely on mtDNA.

Figure 1

Current species ranges of L. europaeus and L. timidus in Eurasia according to Flux & Angermann (1990) and Mitchell-Jones et al. (1999). The dashed box depicts the Iberian Peninsula. (See figure 2 for the ranges of hare species in this region.)

Figure 2

Ranges of the species of hares in the Iberian Peninsula and geographical distribution and frequencies of the four mitochondrial lineages observed in 39 populations (updated from Melo-Ferreira et al. 2005): 33 from L. granatensis (Ala1, Álava; Alb, Albacete; Alc, Alcañiz; Ali, Alicante; Alj, Aljustrel; Amd, Almeida; Ben, Benavente; Brg, Bragança; CBr, Castelo Branco; Cac, Cáceres; Crd, Córdoba; Crn, La Coruña; Cre, Ciudad Real; Cue, Cuenca; Grn, Granada; Hue, Huesca; Mad, Madrid; Mer, Mértola; Mur, Múrcia; Nav1, Navarra; Pan, Pancas; Ptm, Portimão; Sal, Salamanca; SE, Serra da Estrela; San, Santarém; Sen, Sendim; Sev, Sevilla; Sor, Soria; TC, Tierra de Campos; Tol, Toledo; Tor, Tordesillas; Val, Valência; Zar, Zaragoza); 5 from L. europaeus (Ala2, Álava; Can, Cantabria; Jac, Jaca; Nav2, Navarra; Vlc, Villarcayo) and 1 from L. castroviejoi (Cas, Cantabria). Sample sizes and population codes are shown next to the pie charts.

Figure 3

The proportion of the mountain hare mitochondrial lineage within the three hare species from the Iberian Peninsula: (a) L. granatensis with 31.7% L. timidus mtDNA, (b) L. europaeus with 92.3% L. timidus mtDNA and (c) L. castroviejoi with 11.1% L. timidus mtDNA.

Figure 4

Neighbour-joining tree of cytochrome b sequences (552 bp) of 19 species of hares, computed using the Kimura two-parameter model of evolution (Kimura 1980) and 1000 bootstrap replicates, using the program MEGA v. 3.1 (Kumar et al. 2004). Sequences from the European rabbit (Oryctolagus cuniculus) and cottontail (Sylvilagus floridanus) were used as outgroups. All sequences were downloaded from GenBank (accession numbers are depicted on the tips of the tree). Species names and specimen locations are also indicated.