Whole-genome resequencing reveals complex effects of geographical-palaeoclimatic interactions on diversification of moustache toads in East Asia.

ABSTRACT

Geographical features and palaeoclimatic fluctuations are two classical evolutionary forces that shape genetic diversification within species. Fine-grained analysis of the mechanisms involved through population demographic processes, however, remains limited. Taking advantage of two recently published reference genomes, we resequenced the genomes and examined the evolutionary history of the moustache toads, a group endemic to East Asia where complex topography and fluctuating palaeoclimate are known to have had profound impacts on organisms. Moustache toads probably originated in southeast Yunnan, China, and diversified towards the northwestern of Yunnan, as well as central and eastern China. Further exploration based on three widespread species (Leptobrachium ailaonicum, L. boringii and L. liui) using demographic modelling and species distribution models revealed that mountains and river valleys in East Asia not only functioned as geographical barriers, but also provided dispersal corridors and facilitated continuous migration or post-glacial secondary contact among moustache toad populations. Furthermore, periodic oscillation of effective population sizes accompanying fluctuations of historical temperature and population contraction at the Last Glacial Maximum support the widespread impact of climatic changes of the Pleistocene on species diversification in East Asia. This impact was moderate for populations of L. ailaonicum and L. boringii in the southwestern mountains but severe for populations of L. liui in the eastern lowland regions of continental East Asia, which is supported by different degrees of change of their effective population sizes. Our findings reveal mechanisms underlying genetic diversification among moustache toads, and highlight the power of genomic data and demographic modelling for examining complex historical population-level processes and for understanding how geographical and palaeoclimatic factors interactively shape current intraspecific diversity.