Polyploidy breaks speciation barriers in Australian burrowing frogs Neobatrachus

Novikova, Polina Yu.; Brennan, Ian G.; Booker, William; Mahony, Michael; Doughty, Paul; Lemmon, Alan R.; Moriarty Lemmon, Emily; Roberts, J. Dale; Yant, Levi; Van de Peer, Yves; Keogh, J. Scott; Donnellan, Stephen C.

Abstract

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.

Citation

Novikova, P. Y., Brennan, I. G., Booker, W., Mahony, M., Doughty, P., Lemmon, A. R., Moriarty Lemmon, E., Roberts, J. D., Yant, L., Van de Peer, Y., Keogh, J. S., & Donnellan, S. C. (2020). Polyploidy breaks speciation barriers in Australian burrowing frogs Neobatrachus. PLoS Genetics, 16(5), Article e1008769. https://doi.org/10.1371/journal.pgen.1008769

• Journal Article Type: Article
• Acceptance Date: Apr 8, 2020
• Online Publication Date: May 11, 2020
• Publication Date: May 11, 2020
• Deposit Date: May 16, 2020
• Publicly Available Date: Jun 15, 2020
• Journal: PLoS genetics
• Print ISSN: 1553-7390
• Electronic ISSN: 1553-7404
• Publisher: Public Library of Science
• Peer Reviewed: Peer Reviewed
• Volume: 16
• Issue: 5
• Article Number: e1008769
• DOI: https://doi.org/10.1371/journal.pgen.1008769
• Keywords: Genetics(clinical); Genetics; Cancer Research; Ecology, Evolution, Behavior and Systematics; Molecular Biology
• Public URL: https://nottingham-repository.worktribe.com/output/4442668
• Publisher URL: https://journals.plos.org/plosgenetics/article?id=10.1371/journal.pgen.1008769