Conflict over fertilization underlies the transient evolution of reinforcement

Abstract

When two populations or species hybridize, their offspring often experience reductions in fitness relative to either parental population. The production of low fitness hybrids may be prevented by the evolution of increased prezygotic isolation; a process known as reinforcement. Theoretical challenges to the evolution of reinforcement are generally cast as a coordination problem — e.g., linkage disequilibrium between trait and preference loci is difficult to maintain in the face of recombination. However, the evolution of reinforcement also poses a potential conflict between mates. For example, the opportunity costs to hybridization may differ between the sexes or species. This is particularly likely for postmating prezygotic isolation, as the ability to fertilize both conspecific and heterospecific eggs is beneficial to male gametes, but heterospecific mating may incur a cost for female gametes. Motivated by this problem, we develop a population genetic model of interspecific conflict over reinforcement, inspired by ‘gametophytic factors’, which act as postmating prezygotic barriers among Zea mays subspecies. We demonstrate that this conflict results in the transient evolution of reinforcement – after female preference for a conspecific gamete trait rises to high frequency, male traits adaptively introgress into the other population. Ultimately the male gamete trait fixes in both species, and prezygotic isolation returns to pre-reinforcement levels. We interpret geographic patterns of isolation among Z. mays subspecies in light of these findings, and suggest when and how this conflict can be mediated. Our results suggest that sexual conflict may pose an understudied obstacle to the evolution of reinforcement via postmating prezygotic isolation.

Assortative mating enhances postzygotic barriers to gene flow via ancestry bundling

“…For example, there are a number of cases where sexual selection has favored the asymmetric introgression of display traits across species boundaries ( 53 , 54 ). Additionally, the introgression of preference alleles from one population into the other can facilitate the subsequent introgression of the preferred trait via sexual selection ( 55 – 57 ). Such scenarios involve more complicated dynamics than we have modeled, including situations where selection favors introgression of certain parts of the genome but not others.…”

Strong postmating reproductive isolation inMimulussectionEunanus

“…Crossing failure (postmating prezygotic isolation) can be caused by a failure of pollen tube germination, failure of pollen tube growth, failure of fertilization, or even early seed abortion (Wheeler et al, 2001); it may be a passive incompatibility between pollen and pistil, or an active rejection mechanism to prevent maladaptive hybridization (Hogenboom et al, 1975; Roda & Hopkins, 2019; Rushworth et al, 2022). Most studies on the mechanisms of postmating prezygotic isolation come from systems with self-incompatibility, where they are thought to be related to self-incompatibility mechanisms, e.g.…”