Hybridization and introgression between toads with different sex chromosome systems

Abstract

The growing interest in the lability of sex determination in non‐model vertebrates such as amphibians and fishes has revealed high rates of sex chromosome turnovers among closely related species of the same clade. Can such lineages hybridize and admix with different sex‐determining systems, or could the changes have precipitated their speciation? We addressed these questions in incipient species of toads (Bufonidae), where we identified a heterogametic transition and characterized their hybrid zone with genome‐wide markers (RADseq). Adult and sibship data confirmed that the common toad B. bufo is female heterogametic (ZW), while its sister species the spined toad B. spinosus is male heterogametic (XY). Analysis of a fine scale transect across their parapatric ranges in southeastern France unveiled a narrow tension zone (∼10 km), with asymmetric mitochondrial and nuclear admixture over hundreds of kilometers southward and northward, respectively. The geographic extent of introgression is consistent with an expansion of B. spinosus across B. bufo ’s former ranges in Mediterranean France, as also suggested by species distribution models. However, widespread cyto‐nuclear discordances ( B. spinosus backrosses carrying B. bufo mtDNA) run against predictions from the dominance effects of Haldane's rule, perhaps because Y and W heterogametologs are not degenerated. Common and spined toads can thus successfully cross‐breed despite fundamental differences in their sex determination mechanisms, but remain partially separated by reproductive barriers. Whether and how the interactions of their XY and ZW genes contribute to these barriers shall provide novel insights on the debated role of labile sex chromosomes in speciation.

Novel genetic sex markers reveal unexpected lack of, and similar susceptibility to, sex reversal in free-living common toads in both natural and anthropogenic habitats

“…The novel sex markers developed in our study confirmed that Hungarian populations of the common toad are female heterogametic, echoing recent findings from Switzerland (Dufresnes et al, 2020). Identification of the common toad's sex chromosomes remained unresolved so far (Dufresnes et al, 2020).…”

“…The novel sex markers developed in our study confirmed that Hungarian populations of the common toad are female heterogametic, echoing recent findings from Switzerland (Dufresnes et al, 2020). Identification of the common toad's sex chromosomes remained unresolved so far (Dufresnes et al, 2020). Genome BLAST showed that at least three of the four new sex markers are located on different scaffolds, but specific position of these scaffolds is unknown, except for one which is located on chromosome 5.…”

“…In this study, we first aimed to produce a reliable molecular marker set for diagnosing genetic sex in the common toad (Bufo bufo), an anuran amphibian widespread in Eurasia that occupies a wide range of habitats from pristine woodlands to anthropogenic areas (Agasyan et al, 2009). This species has a female-heterogametic (ZZ/ZW) sex-chromosome system (Dufresnes et al, 2020), and is liable to chemically induced sex reversal (Hayes, 1998). Then, using our novel marker set, we investigated whether the frequency of sex reversal in toads differed between natural, agricultural, and urban habitats.…”

Revisiting a speciation classic: Comparative analyses support sharp but leaky transitions betweenBombinatoads

“…For instance, hybridization events during post‐glacial range expansions have left traces of introgression over extensive geographical areas (Wielstra & Arntzen, 2012; Wielstra, Burke, Butlin, Avcı, et al., 2017). Hybrid zones often move (Buggs, 2007; Wielstra, 2019), as the parental species shifted distributions since the initial contact, and foreign alleles may persist hundreds of kilometres away from the current transitions (Dufresnes, Litvinchuk, et al., 2020; Wielstra, Burke, Butlin, & Arntzen, 2017). At the regional level, geographical or ecological changes altering population connectivity, such as large river displacements or human‐induced habitat disturbances, can further contribute to dynamically promote or disrupt species boundaries over short time‐scales (e.g.…”

“…We recently highlighted this matter when re‐investigating European amphibian hybrid zones with hundreds of SNPs obtained from RAD‐sequencing data, which yielded drastically different results compared to previous surveys based on conventional markers (e.g. Dufresnes, Nicieza, et al., 2020; Dufresnes, Litvinchuk, et al., 2020). Therefore, targeting replicate transects with multilocus datasets representative of the entire genome appears necessary to fully grasp the outcome of secondary contacts between hybridizing species (Harrison & Larson, 2016).…”