Consequences of coupled barriers to gene flow for the build‐up of genomic differentiation

Abstract

Theory predicts that when different barriers to gene flow become coincident, their joint effects enhance reproductive isolation and genomic divergence beyond their individual effects, but empirical tests of this "coupling" hypothesis are rare. Here, we analyze patterns of gene exchange among populations of European corn borer moths that vary in the number of acting barriers, allowing for comparisons of genomic variation when barrier traits or loci are in coincident or independent states. We find that divergence is mainly restricted to barrier loci when populations differ by a single barrier, whereas the coincidence of temporal and behavioral barriers is associated with divergence of two chromosomes harboring barrier loci. Furthermore, differentiation at temporal barrier loci increases in the presence of behavioral divergence and differentiation at behavioral barrier loci increases in the presence of temporal divergence. Our results demonstrate how the joint action of coincident barrier effects leads to levels of genomic differentiation that far exceed those of single barriers acting alone, consistent with theory arguing that coupling allows indirect selection to combine with direct selection and thereby lead to a stronger overall barrier to gene flow. Thus, the state of barriersindependent or coupled-strongly influences the accumulation of genomic differentiation.

Temperature impacts how sugar resources alter reproductive investment in the European corn borer moth

“…For example, our results suggest there could be environmentally-driven variability in breeding among E- and Z-strain corn borer populations in the wild, if differential reproductive investment only occurs under some temperature and resource conditions, but not others. Indeed, hybridization rates among E and Z strains are known to be highly variable across North America (Coates et al 2013, Kunerth et al 2022). However, many other behaviors and traits contribute to reproductive isolation among corn borer strains (Dopman et al 2010) and the way in which all of these barriers respond to both temperature and resource availability needs to be investigated to predict the outcomes of forecasted environmental changes on hybridization rates among corn borers.…”

“…Mate attractiveness in corn borers has also been well-studied and corresponds to variation in female pheromone usage among populations, which is related to genetic differences in pheromone production and pheromone perception loci (Dopman et al 2004, Coates et al 2018, Unbehend et al 2021, Kunerth et al 2022). E- and Z-pheromone strains differ in the ratios of chemical isomers present in the female pheromone, with E males preferentially responding to E female pheromone blends and Z males preferentially responding to Z pheromone blends (Roelofs et al 1985, Linn et al 1997, Koutroumpa et al 2014).…”

Computer Simulation and Mathematical Modeling of the Interactions Between Ecological and Sexual Selection to Reveal the Mechanism of Sympatric Speciation

“…Two mechanisms are thought to facilitate coupling [67, 109, 113]. Coupling leads to linkage disequilibrium among the genes responsible for different reproductive barriers.…”

How chromosomal inversions reorient the evolutionary process

“…In M. guttatus , an inversion appears to have suppressed recombination between loci influencing life‐history traits that contribute to both local adaptation as well as prezygotic isolation (Coughlan & Willis, 2019; Lowry & Willis, 2010). A particularly clear example is the European corn borer, Ostrinia nubilalis , where an inversion spanning about 40% of the Z chromosome (~10 Mb) contains both a pheromone receptor locus and a locus contributing to seasonal adaptation of different ecotypes (Kozak et al., 2017; Kunerth et al., 2022).…”