Polyploidy breaks speciation barriers in Australian burrowing frogs Neobatrachus

Author summary Polyploidy or whole genome duplication is rare in animals and usually polyploid animals reproduce asexually. The Australian burrowing frogs of the genus Neobatrachus form an interesting exception amongst vertebrates with multiple independently originated autotetraploid sexual species. We generated population genomic data from 87 animals representing all six diploid and three tetraploid species of Neobatrachus. We show that, while diploid Neobatrachus species seem to be isolated from each other, their sister tetraploid species experience substantial levels of gene flow, and have wider distributions. Furthermore, we observe asymmetric gene flow from diploids to tetraploids. Based on our genomic and climate analyses we suggest that such inter-specific hybridization mediated by whole genome duplication rescues species diversity and allows tetraploids to more easily avoid impacts of climate-induced habitat loss. Polyploidy has played an important role in evolution across the tree of life but it is still unclear how polyploid lineages may persist after their initial formation. While both common and well-studied in plants, polyploidy is rare in animals and generally less understood. The Australian burrowing frog genus Neobatrachus is comprised of six diploid and three polyploid species and offers a powerful animal polyploid model system. We generated exome-capture sequence data from 87 individuals representing all nine species of Neobatrachus to investigate species-level relationships, the origin and inheritance mode of polyploid species, and the population genomic effects of polyploidy on genus-wide demography. We describe rapid speciation of diploid Neobatrachus species and show that the three independently originated polyploid species have tetrasomic or mixed inheritance. We document higher genetic diversity in tetraploids, resulting from widespread gene flow between the tetraploids, asymmetric inter-ploidy gene flow directed from sympatric diploids to tetraploids, and isolation of diploid species from each other. We also constructed models of ecologically suitable areas for each species to investigate the impact of climate on differing ploidy levels. These models suggest substantial change in suitable areas compared to past climate, which correspond to population genomic estimates of demographic histories. We propose that Neobatrachus diploids may be suffering the early genomic impacts of climate-induced habitat loss, while tetraploids appear to be avoiding this fate, possibly due to widespread gene flow. Finally, we demonstrate that Neobatrachus is an attractive model to study the effects of ploidy on the evolution of adaptation in animals.