Birth of a hotspot of intraspecific genetic diversity: notes from the underground

Hotspots of intraspecific diversity have been observed in most species, often within areas of putative Pleistocene refugia. They have thus mostly been viewed as the outcome of prolonged stability of large populations within the refugia. However, recent evidence has suggested that several other microevolutionary processes could also be involved in their formation. Here, we investigate the contribution of these processes to current range-wide patterns of genetic diversity in the Italian endemic mole Talpa romana, using both nuclear (30 allozyme loci) and mitochondrial markers (cytochrome b sequences). Southern populations of this species showed an allozyme variation that is amongst the highest observed in small mammals (most populations had an expected heterozygosity of 0.10 or above), which was particularly unexpected for a subterranean species. Population genetic, phylogeographic and historical demographic analyses indicated that T. romana populations repeatedly underwent allopatric differentiations followed by secondary admixture within the refugial range in southern Italy. A prolonged demographic stability was reliably inferred from the mitochondrial DNA data only for a population group located north and east of the Calabrian peninsula, showing comparatively lower levels of allozyme variability, and lacking evidence of secondary admixture with other groups. Thus, our results point to the admixture between differentiated lineages as the main cause of the higher levels of diversity of refugial populations. When compared with the Pleistocene evolutionary history recently inferred for species from both the same and other geographic regions, these results suggest the need for a reappraisal of the role of gene exchange in the formation of intraspecific hotspots of genetic diversity.