Mass of genes rather than master genes underlie the genomic architecture of amphibian speciation

Abstract

The genetic architecture of speciation, i.e., how intrinsic genomic incompatibilities promote reproductive isolation (RI) between diverging lineages, is one of the best-kept secrets of evolution. To directly assess whether incompatibilities arise in a limited set of large-effect speciation genes, or in a multitude of loci, we examined the geographic and genomic landscapes of introgression across the hybrid zones of 41 pairs of frog and toad lineages in the Western Palearctic region. As the divergence between lineages increases, phylogeographic transitions progressively become narrower, and larger parts of the genome resist introgression. This suggests that anuran speciation proceeds through a gradual accumulation of multiple barrier loci scattered across the genome, which ultimately deplete hybrid fitness by intrinsic postzygotic isolation, with behavioral isolation being achieved only at later stages. Moreover, these loci were disproportionately sex linked in one group (Hyla) but not in others (Rana and Bufotes), implying that large X-effects are not necessarily a rule of speciation with undifferentiated sex chromosomes. The highly polygenic nature of RI and the lack of hemizygous X/Z chromosomes could explain why the speciation clock ticks slower in amphibians compared to other vertebrates. The clock-like dynamics of speciation combined with the analytical focus on hybrid zones offer perspectives for more standardized practices of species delimitation.

Genome assembly, structural variants, and genetic differentiation between Lake Whitefish young species pairs (Coregonus sp.) with long and short reads

“…However, the genome-wide landscape of differentiation should be interpreted with caution as it results from complex interactions between gene flow, recombination, demography, and selection (Cruickshank & Hahn, 2014; Ravinet et al, 2017; Stevison & McGaugh, 2020). Analysing differentiation between evolutionarily “young” pairs of species has nevertheless proven to be informative, revealing widespread heterogeneity among and between chromosomes (Henderson & Brelsford, 2020; Martin, Davey, Salazar, & Jiggins, 2019), sometimes identifying genes underlying reproductive isolation (Hejase et al, 2020), and informing about the number and distribution of divergent loci (Dufresnes et al, 2021). Cases of ‘natural replicates’, including species pairs with similar ecological and phenotypic divergence, are of particular interest, along with instances of repeated hybridization due to secondary contacts.…”

European common frog (Rana temporaria) recolonized Switzerland from multiple glacial refugia in northern Italy via trans‐ and circum‐Alpine routes

“…Importantly, several different divergence times have been proposed between brown frogs, and a consensus has not yet been reached. For example, a much older divergence time of 4.1 Mya (compared to 1.12 Mya used in this study; Veith et al, 2003) has recently been estimated between R. parvipalmata and R. temporaria based on genome-wide nuclear phylogenies (Dufresnes et al, 2021 ). Thus, the timescale of divergence between the eastern and western clades may have occurred much earlier than estimated here.…”

“…parvipalmata and R . temporaria based on genome‐wide nuclear phylogenies (Dufresnes et al, 2021 ). Thus, the timescale of divergence between the eastern and western clades may have occurred much earlier than estimated here.…”

Sex chromosomes as supergenes of speciation: why amphibians defy the rules?

“…In fire salamanders, the genetic structure between populations inhabiting distinct habitats was hypothesized to reflect nascent ecological speciation [124], although the pattern can be explained by isolation-by-distance [125]. In European amphibians, hybrid zone analyses suggest that speciation proceeds from genomic divergence in allopatry, generating post-zygotic barriers between cryptic species long before the divergence of sexual traits responsible for pre-mating isolation in sympatry [126,127] (see also §4(c)). Hence, speciation by the rapid build up of pre-zygotic isolation does not seem common in amphibians, and sex chromosomes are not expected to play a major part in it.…”

“…In green toads ( Bufotes ), both types of markers behave similarly across the porous hybrid zone between two B. viridis lineages in north Italy ( B. v. viridis / balearicus ), as well as across the narrow hybrid zone between B. viridis and B. boulengeri in Sicily [128]. In common frogs, analyses of species-diagnostic single-nucleotide polymorphisms mapped on a reference genome revealed a homogeneous landscape of introgression between the sister species R. temporaria and R. parvipalmata , with the sex chromosomes actually admixing slightly more than the average autosome [127]. Remarkably, even the loci located near the presumed sex-determining gene ( Dmrt1 ) featured similar levels of introgression as the rest of the genome [127].…”