Past vicariance promoting deep genetic divergence in an endemic frog species of the espinhaço range in Brazil: The historical biogeography of bokermannohyla saxicola (Hylidae)

Abstract

The highland endemic frog Bokermannohyla saxicola occurs within the Espinhaço Range, the most extensive and continuous orogenic belt of the Brazilian territory, located in Southeastern Brazil. We used mitochondrial DNA markers to test for spatial structure, to investigate the likely influence of past vicariant events, to evaluate demographic dynamics along the species range, and to understand the role of habitat discontinuities in promoting connectivity and diversity along the range. We found four major monophyletic lineages, each one associated with distinct mountain tops. The divergence time found between the four main clades clearly pre-dated the Pleistocene, except for the most recent separation. We observed no signs of population expansion for most of the sampling sites along the range, and a higher genetic diversity in the most continuous and central highland plateau, compared to smaller marginal regions. The Espinhaço Range harbors four deeply divergent lineages of B. saxicola within areas restricted by barriers for millions of years. These relatively isolated populations were kept apart by discontinuities represented by lowland habitats between mountain tops. Most of the lineage divergences occurred earlier than the Pleistocene, thus they cannot be solely explained by climatic oscillations of this epoch. However, within-lineage divergence times were all dated from the Pleistocene, suggesting an important effect in population dynamics. We also suggest that some marginal populations like those from Serra Negra and Serra de Itacambira can be the result of recent colonization events. Finally, in the Southern Espinhaço region, the most continuous central highland area shows greater genetic diversity than the marginal discontinuous areas, where we have also observed a significant correlation between genetic and geographic distances. Bokermannohyla saxicola is a good model to study the biogeography of the Espinhaço Range because its high genetic structure reflects ancient as well as recent geological/climatic events, with important implications for conservation.