Conflict over fertilization underlies the transient evolution of reinforcement

• Published in: PLoS biology Vol. 20; no. 10; p. e3001814
• Main Authors: Rushworth, Catherine A, Wardlaw, Alison M, Ross-Ibarra, Jeffrey, Brandvain, Yaniv
• Format: Journal Article
• Language: English
• Published: United States Public Library of Science 13-10-2022; Public Library of Science (PLoS)
• Subjects: Adaptation; Animal reproduction; Biological Evolution; Biology and Life Sciences; Evolution; Evolutionary genetics; Female; Females; Fertilization; Gametes; Gender differences; Genetic aspects; Genetic research; Genotype; Germ Cells; Haplotypes; Human reproduction; Humans; Hybridization; Hybridization, Genetic; Hybrids; Male; Males; Opportunity costs; Phenotype; Plant reproduction; Population genetics; Preferences; Properties; Recombination; Reinforcement; Reproduction - genetics; Research and Analysis Methods; Sexes; Sperm; United States
• ISSN: 1545-7885; 1544-9173; 1545-7885
• DOI: 10.1371/journal.pbio.3001814

When two species meet in secondary contact, the production of low fitness hybrids may be prevented by the adaptive evolution of increased prezygotic isolation, a process known as reinforcement. Theoretical challenges to the evolution of reinforcement are generally cast as a coordination problem, i.e., "how can statistical associations between traits and preferences be maintained 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 reinforcement based on postmating prezygotic (PMPZ) incompatibilities, 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. We develop a population genetic model of interspecific conflict over reinforcement inspired by "gametophytic factors", which act as PMPZ barriers among Zea mays subspecies. We demonstrate that this conflict results in the transient evolution of reinforcement-after females adaptively evolve to reject gametes lacking a signal common in conspecific gametes, this gamete signal adaptively introgresses into the other population. Ultimately, the male gamete signal fixes in both species, and isolation returns to pre-reinforcement levels. We interpret geographic patterns of isolation among Z. mays subspecies considering these findings and suggest when and how this conflict can be resolved. Our results suggest that sexual conflict over fertilization may pose an understudied obstacle to the evolution of reinforcement.