Heterogeneous genome divergence, differential introgression, and the origin and structure of hybrid zones

Abstract

Hybrid zones have been promoted as windows on the evolutionary process and as laboratories for studying divergence and speciation. Patterns of divergence between hybridizing species can now be characterized on a genomewide scale, and recent genome scans have focused on the presence of 'islands' of divergence. Patterns of heterogeneous genomic divergence may reflect differential introgression following secondary contact and provide insights into which genome regions contribute to local adaptation, hybrid unfitness and positive assortative mating. However, heterogeneous genome divergence can also arise in the absence of any gene flow, as a result of variation in selection and recombination across the genome. We suggest that to understand hybrid zone origins and dynamics, it is essential to distinguish between genome regions that are divergent between pure parental populations and regions that show restricted introgression where these populations interact in hybrid zones. The latter, more so than the former, reveal the likely genetic architecture of reproductive isolation. Mosaic hybrid zones, because of their complex structure and multiple contacts, are particularly good subjects for distinguishing primary intergradation from secondary contact. Comparisons among independent hybrid zones or transects that involve the 'same' species pair can also help to distinguish between divergence with gene flow and secondary contact. However, data from replicate hybrid zones or replicate transects do not reveal consistent patterns; in a few cases, patterns of introgression are similar across independent transects, but for many taxa, there is distinct lack of concordance, presumably due to variation in environmental context and/or variation in the genetics of the interacting populations.

Keywords: FST outlier; cline; gene flow; genomic divergence; mosaic hybrid zone; speciation.

Figure 1

Examples of two common hybrid zone structures. A) A clinal hybrid zone (or tension zone) formed between the subspecies Mus musculus musculus and M. m. domesticus in central Europe. These subspecies interact in a narrow zone along the edges of their distributions. Transects across the Mus hybrid zone reveal a continuous gradation from pure M. m. domesticus in the west, multi-generation hybrids in the center of the zone to M. m. musculus in the east. B) A mosaic hybrid zone formed between the field crickets, Gryllus firmus and G. pennsylvanicus in the eastern United States. Each species occupies distinct habitat types that are patchily distributed where the species ranges overlap. Transects across the field cricket hybrid zone pass through multiple habitat patches, with contact between the two species occurring across each patch boundary.

Figure 2

Patterns of admixture in the field cricket hybrid zone. The hybrid index is plotted against interspecific heterozygosity for crickets from allopatric populations (n = 71) and from two regions of the field cricket hybrid zone (n = 561). Allopatric populations are highly differentiated at these loci; crickets from within the hybrid zone represent complex multi-generation hybrids and backcrosses.