Whole genome duplication potentiates inter-specific hybridisation and niche shifts in Australian burrowing frogs Neobatrachus

Abstract

Polyploidy plays an important role in evolution because it can lead to increased genetic complexity and speciation. It also provides an extra copy buffer and increases genetic novelty. While both common and well-studied in plants, polyploidy is rare in animals, and most polyploid animals reproduce asexually. Amphibians represent a dramatic vertebrate exception, with multiple independent sexually reproducing polyploid lineages, but very few cases have been studied in any detail. The Australian burrowing frog genus Neobatrachus is comprised of six diploid and three polyploid species and offers a powerful model animal polyploid system. We generated exome-capture sequence data from 87 individuals representing all nine species of Neobatrachus to investigate species-level relationships, the origin of polyploid species, and the population genomic effects of polyploidy on genus-wide demography. We resolve the phylogenetic relationships among Neobatrachus species and provide further support that the three polyploid species have independent origins. We document higher genetic diversity in tetraploids, resulting from widespread gene flow specifically between the tetraploids, asymmetric inter-ploidy gene flow directed from sympatric diploids to tetraploids, and current isolation of diploid species from each other. We also constructed models of ecologically suitable areas for each species to investigate the impact of climate variation on frogs with differing ploidy levels. These models suggest substantial change in suitable areas compared to past climate, which in turn corresponds 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 into tetraploid lineages specifically. Finally, we demonstrate that Neobatrachus is an attractive model to study the effects of ploidy on evolution of adaptation in animals.

Evolution of gene-rich germline restricted chromosomes in black-winged fungus gnats through introgression (Diptera: Sciaridae)

“…Although animals of similar divergence have been successfully hybridised in the lab [47], we present the first evidence for a cross-family hybridisation event in nature with evolutionary consequences. Gene flow between very divergent lineages seems to be frequently associated with polyploidisation (for example in burrowing frogs [48], or Arabidopsis [49]), supporting our view that GRCs evolved in the current form a whole genome introgressed from the ancestor of Cecidomyiidae.…”

GenomeScope 2.0 and Smudgeplots: Reference-free profiling of polyploid genomes

“…Higher ploidy levels have also been documented in many fungal species (Todd, Forche, and Selmecki 2017). Polyploidy in animals is less common than in these other taxa, but is far from rare, including many species of frogs (Novikova et al 2019), fish (Comber and Smith 2004), crustaceans and molluscs (Goldman, LoVerde, and Chrisman 1983), as well as many species of nematodes (Szitenberg et al 2017). The nematode species that are major pests of polyploid crops also happen to be polyploid (Abad et al 2008).…”

GenomeScope 2.0 and Smudgeplot for reference-free profiling of polyploid genomes

“…Higher ploidy levels have also been documented in many fungal species 3 . Polyploidy in animals is less common than in these other taxa, but is far from rare, including many species of frogs 4 , fish 5 , crustaceans, and molluscs 6 , as well as many species of nematodes 7 . The nematode species that are major pests of polyploid crops also happen to be polyploid 8 .…”