The Evolution of Sex is Tempered by Costly Hybridization in Boechera (Rock Cress)

Abstract

Abstract Despite decades of research, the evolution of sex remains an enigma in evolutionary biology. Typically, research addresses the costs of sex and asexuality to characterize the circumstances favoring one reproductive mode. Surprisingly few studies address the influence of common traits that are, in many organisms, obligately correlated with asexuality, including hybridization and polyploidy. These characteristics have substantial impacts on traits under selection. In particular, the fitness consequences of hybridization (i.e., reduced fitness due to interspecific reproductive isolation) will influence the evolution of sex. This may comprise a cost of either sex or asexuality due to the link between hybridity and asexuality. We examined reproductive isolation in the formation of de novo hybrid lineages between 2 widespread species in the ecological model system Boechera. Seventeen percent of 664 crosses produced F1 fruits, and only 10% of these were viable, suggesting that postmating prezygotic and postzygotic barriers inhibit hybrid success in this system. The postmating prezygotic barrier was asymmetrical, with 110 of 115 total F1 fruits produced when Boechera stricta acted as maternal parent. This asymmetry was confirmed in wild-collected lineages, using a chloroplast phylogeny of wild-collected B. stricta, Boechera retrofracta, and hybrids. We next compared fitness of F2 hybrids and selfed parental B. stricta lines, finding that F2 fitness was reduced by substantial hybrid sterility. Multiple reproductively isolating barriers influence the formation and fitness of hybrid lineages in the wild, and the costs of hybridization likely have profound impacts on the evolution of sex in the natural environment.