Stuck on a small tropical island: wide in-situ diversification of an urban-dwelling bat

Bats are often the only mammals naturally colonizing isolated islands and are thus an excellent model to study evolutionary processes of insular ecosystems. Here, we studied the Reunion free-tailed bat (Mormopterus francoismoutoui), an endemic species to Reunion Island that has adapted to urban settings. At regional scale, we investigated the evolutionary history of Mormopterus species, as well as on Reunion Island sex-specific and seasonal patterns of genetic structure. We used an extensive spatio-temporal sampling including 1,136 individuals from 18 roosts and three biological seasons (non-reproductive/winter, pregnancy/summer, and mating), with additional samples from Mormopterus species from neighbouring islands (M. jugularis of Madagascar and M. acetabulosus of Mauritius). Complementary information gathered from both microsatellite and mitochondrial markers revealed a high genetic diversity but no signal of spatial genetic structure and weak evidence of female philopatry. Regional analysis suggests a single colonization event for M. francoismoutoui, dated around 175,000 years ago, and followed by in-situ diversification and the evolution of divergent ancestral lineages, which today form a large metapopulation. Population expansion was relatively ancient (55,000 years ago) and thus not linked to human colonization of the island and the availability of new anthropic day-roost sites. Discordant structure between mitochondrial and microsatellite markers suggests the presence of yet-unknown mating sites, or the recent evolution of putative ecological adaptations. Our study illustrates how understanding mechanisms involved in speciation can be challenging and the importance of both mitochondrial and nuclear DNA in resolving the wide in-situ diversification of an urban-dwelling bat, endemic to a small island.