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

Abstract

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 geographic introgression across eleven transitions altogether, using cline analyses when possible. Results-We found sharp (2-11km wide) but leaky transitions (geographically extensive traces of introgression) in all parapatric areas, either measured from a few allozymes or thousands of speciesdiagnostic 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 geographic ranges and ecological differentiation that enforces tight boundaries regardless of the biogeographic 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.

Combining RADseq and contact zone analysis to decipher cryptic diversification in reptiles: insights from Acanthodactylus erythrurus (Reptilia: Lacertidae)

“…Even between mostly incompatible genomes, some neutral loci are expected to diffuse far within species ranges once recombination has broken down linkage between them and the barrier loci (Barton 1979, Polechová & Barton 2011). Accordingly, speciation is often achieved before interspecies gene flow entirely stops, so sharp clines may be paralleled by far-ranging introgression without questioning the taxonomic status of lineages (as shown in Bombina toads, Dufresnes et al 2021b). However, the potential unreliability of the outlier clines reported here and the use of diagnostic loci only prevents the interpretation of the genomic landscape of introgression.…”

Genetic traces of hybrid zone movement across a fragmented habitat

“…First, given the limited opportunity for sampling we cannot rule out that clines in the south were missed, just as we would not have encountered some displaced clines if the northern leg of the transect had been short. Second, we are forced to rely on a single transect whereas several studies on multiple transects across the same hybrid zone revealed different patterns of introgression, governed by a variety of demographic and environmental parameters (Dufresnes et al, 2021; Harrison & Larson, 2016; Janoušek et al, 2012; Szymura & Barton, 1986, 1991; Teeter et al, 2010). Further analysis of additional transects (if these were to exist) and extending the sampling of the southern populations could help to test and refine our inferences.…”

Buccal swabs for amphibian genomics

“…We compiled laboratory details (DNA yields and sequencing success) of 771 samples initially processed in genomic studies of Bombina (Dufresnes et al, 2021a), Hyla (Dufresnes et al, 2019a), Pelobates (Dufresnes et al, 2019b), Pelophylax (Dubey et al, 2019), Alytes (Dufresnes and Martinez-Solano, 2020a), Pelodytes and Discoglossus (Dufresnes et al, 2020b), and compared the performance of buccal swabs, tail clipping of tadpoles, toe clipping of adults, muscle tissue obtained from fixed specimens, and road kills.…”