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Conflict over fertilization underlies the transient evolution of reinforcement

View ORCID ProfileCatherine A. Rushworth, Alison M. Wardlaw, Jeffrey Ross-Ibarra, Yaniv Brandvain
doi: https://doi.org/10.1101/2020.11.10.377481
Catherine A. Rushworth
1Dept. of Biology, Utah State UniversityLogan, UT, USA
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Alison M. Wardlaw
2Dept. of Plant and Microbial Biology, University of Minnesota, St. Paul, MN, USA
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Jeffrey Ross-Ibarra
3Dept. of Evolution and Ecology and Center for Population Biology, University of California, Davis, CA, USA
4Genome Center, University of California, Davis, CA, USA
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Yaniv Brandvain
2Dept. of Plant and Microbial Biology, University of Minnesota, St. Paul, MN, USA
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  • For correspondence: ybrandva@umn.edu
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ABSTRACT

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 LD between trait and preference 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 in light of 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.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • This version of the manuscript has been revised by 1. Refocussing the introduction around the theoretical problem, rather than the biological system that motivated it, 2. The inclusion of a cost to the male compatibility (Fig S8 and related text) 3. Edits for clarity throughout.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted June 24, 2022.
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Conflict over fertilization underlies the transient evolution of reinforcement
Catherine A. Rushworth, Alison M. Wardlaw, Jeffrey Ross-Ibarra, Yaniv Brandvain
bioRxiv 2020.11.10.377481; doi: https://doi.org/10.1101/2020.11.10.377481
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Conflict over fertilization underlies the transient evolution of reinforcement
Catherine A. Rushworth, Alison M. Wardlaw, Jeffrey Ross-Ibarra, Yaniv Brandvain
bioRxiv 2020.11.10.377481; doi: https://doi.org/10.1101/2020.11.10.377481

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