Early evolution of reproductive isolation: A case of weak inbreeder/strong outbreeder leads to an intraspecific hybridization barrier in Arabidopsis lyrata

Reproductive strategies play a major role in plant speciation. Notably, transitions from outcrossing to selfing may lead to relaxed sexual selection and parental conflict. Shifts in mating systems can affect maternal and paternal interests, and thus parent-specific influence on endosperm development, leading to reproductive isolation: if selfing and outcrossing species hybridize, the resulting seeds may not be viable due to endosperm failure. Nevertheless, it remains unclear how the switch in mating systems can impact reproductive isolation between recently diverged lineages, that is, during the process of speciation. We investigated this question using Arabidopsis lyrata, which recently transitioned to selfing (10,000 years ago) in certain North American populations, where European populations remain outcrossing. We performed reciprocal crosses between selfers and outcrossers, and measured seed viability and endosperm development. We show that parental genomes in the hybrid seed negatively interact, as predicted by parental conflict. This leads to extensive hybrid seed lethality associated with endosperm cellularization disturbance. Our results suggest that this is primarily driven by divergent evolution of the paternal genome between selfers and outcrossers. In addition, we observed other hybrid seed defects, suggesting that sex-specific interests are not the only processes contributing to postzygotic reproductive isolation.

Automated summary

Reproductive strategies in plants, particularly transitions from outcrossing to selfing, can result in parental conflict and affect endosperm development, leading to reproductive isolation between species. The divergence in paternal genomes between selfers and outcrossers can contribute to extensive hybrid seed lethality. Other factors besides sex-specific interests may also play a role in postzygotic reproductive isolation.