Revisiting a speciation classic: Comparative analyses support sharp but leaky transitions between Bombina toads

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Dufresnes, Christophe | Suchan, Tomasz | Smirnov, Nazar | Denoël, Mathieu | Rosanov, Juriy | Litvinchuk, Spartak

Edité par CCSD ; Wiley -

International audience. Aim - The amount of gene flow between parapatric species can be greatly variable depending on how species boundaries are maintained in respect to numerous genetic and ecological factors that affect the strength of reproductive isolation. We quantified this variability to understand its effect on the genetic integrity of a well‐studied pair of hybridizing amphibians. Location - Central and Eastern Europe. Taxa The fire‐ and yellow‐bellied toads Bombina bombina and B. variegata . Methods - We first complemented the mitochondrial phylogeography of European Bombina by barcoding additional populations and built MaxEnt species distribution models to identify the routes of post‐glacial colonization that led to hybrid zone formation. Second, we targeted the areas of parapatry in Poland and Ukraine to assess nuclear admixture by population genetics (PCA, Bayesian clustering) of allozyme and genomic markers (RAD‐seq). Third, we harvested the rich Bombina literature to thoroughly compare the extent of geographical introgression across 11 transitions altogether, using cline analyses when possible. Results - We found sharp (2–11 km wide) but leaky transitions (geographically extensive traces of introgression) in all parapatric areas, either measured from a few allozymes or thousands of species‐diagnostic SNPs, and irrespective of the intraspecific lineages involved or the relative ages since first contact. Main conclusion - Bombina species are permeable to gene flow despite selection against hybrids that retards but cannot ultimately prevent putatively neutral introgression into the parental gene pools. Although local hybrid swarms face genetic assimilation, the species’ integrities remain intact due to their large geographical ranges and ecological differentiation that enforces tight boundaries regardless of the biogeographical attributes of the contacts. Opposing the great variability of introgression patterns found between cryptic species, these results support that gene flow should not be viewed as a force of despeciation when reproductive isolation involves multiple intrinsic and extrinsic barriers.

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