Conflict over fertilization underlies the transient evolution of reinforcement

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 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.

Early acting inbreeding depression can evolve as an inbreeding avoidance mechanism

“…In fact, this view is quite similar to Uyenoyama’s models that show that the differing costs and benefits of self-incompatibility alleles to pollen and style can favor pollen with novel SI specificities, (42, 43), consistent with the idea that pollen benefit more from having potentially low-fitness offspring than do mothers. This tension between pollen (or pollen parent) and style (or seed parent) over fertilization and development is not unique to self-fertilization – for example upon secondary contact the benefit to pollen in overcoming stylar incompatibilities and siring potentially low-fitness hybrids can frustrate the evolution of reinforcement (44).…”

Strong postmating reproductive isolation in Mimulus section Eunanus

“…Crossing failure (postmating prezygotic isolation) can be caused by a failure of pollen tube germination, pollen tube growth or fertilization (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, for example, Solanum (Bernacchi & Tanksley, 1997; Tovar‐Méndez et al, 2014), Nicotiana (Kuboyama et al, 1994) and Lilium (Ascher & Drewlow, 1975), although a mechanism unrelated to self‐incompatibility has been described in Brassica (Fujii et al, 2019).…”

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.…”