Natural variation in sexual traits and gene expression between selfing and outcrossing Arabidopsis lyrata suggests sexual selection at work.

Flowering plants show significant diversity in sexual strategies, profoundly impacting the evolution of sexual traits and associated genes. Sexual selection is one of the primary evolutionary forces driving sexual trait variation, particularly evident during pollen-pistil interactions, where pollen grains compete for fertilization and females select mating partners. Multiple mating may intensify competition among pollen donors for siring, while in contrast, self-fertilization reduces sire-sire competition, relaxing the sexual selection pressure. Traits involved in male-male competition and female choice are well described, and molecular mechanisms underlying pollen development and pollen-pistil interactions have been extensively studied in the model species Arabidopsis thaliana. However, whether these molecular mechanisms are involved in sexual selection in nature remains unclear. To address this gap, we measured intrinsic pollen performance and its interaction with female choice, and investigated the associated gene expression patterns in a selfing and an outcrossing population of Arabidopsis lyrata. We found that pollen germination and pollen tube growth were significantly higher in outcrossers than selfers, and this difference was accompanied by changes in expression of genes involved in vesicle transport and cytoskeleton. Outcrosser mother plants showed a negative impact on pollen tube growth compared to selfer mother plants, together with a difference of expression for genes involved in auxin and stress response, suggesting a potential mechanism for female choice through molecular crosstalk at the post-pollination stage. Our study provides insight on the impact of sexual selection on the evolution of sexual gene expression in plants.

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.