The genetic architecture of hybrid incompatibilities and their effect on barriers to introgression in secondary contact

Abstract

Genetic incompatibilities are an important component of reproductive isolation. Although theoretical studies have addressed their evolution, little is known about their maintenance when challenged by potentially high migration rates in secondary contact. Although theory predicts that recombination can erode barriers, many empirical systems have been found to retain species-specific differences despite substantial gene flow. By simulating whole genomes in individuals of hybridizing species, we find that the genetic architecture of two contrasting models of epistatic hybrid incompatibilities and the context of hybridization can substantially affect species integrity and genomic heterogeneity. In line with theory, our results show that intergenomic incompatibilities break down rapidly by recombination, but can maintain genome-wide differentiation under very limited conditions. By contrast, intragenomic interactions that arise from genetic pathways can maintain species-specific differences even with high migration rates and gene flow, whereas introgression at large parts of the genome can simultaneously remain extensive, consistent with empirical observations. We discuss the importance of intragenomic interactions in speciation and consider how this form of epistatic fitness variation is implicated and supported by other theoretical and empirical studies. We further address the relevance of replicates and knowledge of context when investigating the genomics of speciation.

Selection against recombinant hybrids maintains reproductive isolation in hybridizing Populus species despite F1 fertility and recurrent gene flow

“…In fact, genetic evidence supporting the presence of epistasis in these poplar hybrid zones was put forward previously (Lexer et al . ), and simulation studies suggest that genotypic patterns in these poplar hybrids are compatible with the intragenomic coadaptation model of RI (Lindtke & Buerkle ; Dorothea Lindtke, personal communication). This agrees well with the observation that F 1 hybrids of these species are at least partially fit and fertile (Macaya‐Sanz et al .…”

Differential introgression and reorganization of retrotransposons in hybrid zones between wild wheats

“…However, unlike previously documented types of incompatibility among host genes (e.g. Lindtke & Buerkle ), conflicting interactions between LTR‐RTs likely account for genomewide, asymmetrical reproductive isolation. To what extent LTR‐RTs drive preferential backcrossing towards the maternal parent, as here observed in hybrid zones between wild wheats, remains a largely open question.…”

Adaptive evolution and segregating load contribute to the genomic landscape of divergence in two tree species connected by episodic gene flow

“…), consistent with DM incompatibilities and/or intrinsic coadaptation of genes in genetic or biochemical pathways (Caseys et al . ; Lindtke & Buerkle ). An important role for intrinsic barriers is also suggested by extremely steep genomic clines and the presence of epistatic interactions in natural hybrids (Lexer et al .…”