The effects of selfing on lineage diversification across multiple genera

Abstract

AbstractThe transition from outcrossing to self-fertilization is one of the most frequent evolutionary trends in flowering plants. Selfing has long been hypothesized as an evolutionary dead end, and the prevalence of intermediate selfing populations despite their evolutionary instability is considered an enigma Nevertheless, recent theories suggest that it is high selfing populations that elevate extinction, while an intermediate selfing rate may be a best-of-both-world strategy. By estimating the dependency of speciation and extinction rates on mating system states for 27 genera, we find that outcrossing lineages overall have significantly higher net diversification rates than selfing lineages. However, whether selfing promotes or reduces speciation rates vary greatly across genera, with no significant overall effects. Moreover, self-compatible annuals tend to have lower diversification rates than self-compatible perennials. Given that annuals are much more likely to be highly selfing than perennials, this finding indirectly supports the hypothesis that suppressed diversification rates may be restricted to highly selfing, instead of intermediate selfing, populations. Consistently, models incorporating hidden states are best fitted for most of the genera, suggesting that the effects of selfing on diversification and transitions in mating systems may often depend on other factors driving diversification variation.Significance statementThe consequences of mating system evolution have received great attention, and selfing has long been hypothesized as an evolutionary dead end. By analyzing 27 genera to mitigate clade dependency, we find that, overall, selfing lineages show lower diversification rates, but similar speciation rates, compared to outcrossing lineages. However, the dependency of diversification rates on mating system may be often caused by the association of mating system transitions with hidden factors driving diversification variation. Indeed, diversification rates for self-compatible annuals are much lower than self-compatible perennials, which also indirectly supports recent theories that suppressed diversification may be restricted to highly selfing, instead of intermediate selfing, populations. This study offers a definitive conclusion about the macroevolutionary consequences of self-fertilization with nuanced insights.