Differences in mating system and predicted parental conflict affect post-pollination reproductive isolation in a flowering plant

Mating system shifts from outcrossing to selfing are frequent in plant evolution. Relative to outcrossing, selfing is associated with reduced parental conflict over seed provisioning, which may result in postzygotic, asymmetric, reproductive isolation in crosses between populations of different mating systems. To test the hypothesis that post-pollination reproductive isolation between populations increases with increasing differences in mating system and predicted parental conflict, we performed a crossing experiment involving all combinations of three self-compatible populations (with low outcrossing rates), and three self-incompatible populations (with high outcrossing rates) of the arctic-alpine herb Arabis alpina, assessing fitness-related seed and plant traits of the progeny. Predicted levels of parental conflict (genome strength) were quantified based on strength of self-incompatibility and estimates of outcrossing rates. Crosses between self-compatible and self-incompatible populations yielded very small seeds of low viability, resulting in strong reproductive isolation. In 14 of 15 reciprocal between-population crosses, seeds were heavier when the paternal plant had the stronger genome, and seed mass differences between cross directions increased with an increased difference in parental conflict. Overall, our results suggest that, when sufficiently large, differences in mating system and hence in expected parental conflict may result in strong post-pollination reproductive barriers contributing to speciation.

Automated summary

Mating system shifts from outcrossing to selfing are common in plant evolution. Selfing reduces parental conflict over seed provisioning, potentially leading to postzygotic, asymmetric, reproductive isolation between populations. In a crossing experiment with Arabis alpina, we found strong reproductive isolation between self-compatible and self-incompatible populations, resulting in smaller and less viable seeds. Differences in parental conflict also influenced seed mass, with larger seeds produced when the paternal plant had the stronger genome. These findings suggest that differences in mating system and parental conflict can contribute to strong post-pollination reproductive barriers and speciation.