Heterosis counteracts hybrid breakdown to forestall speciation by parallel natural selection

Abstract

In contrast to ecological speciation, where reproductive isolation evolves as a consequence of divergent natural selection, speciation by parallel natural selection has been less thoroughly studied. To test whether parallel evolution drives speciation, we leveraged the repeated evolution of benthic and limnetic ecotypes of threespine stickleback fish and estimated fitness for pure crosses and within-ecotype hybrids in semi-natural ponds and in laboratory aquaria. In ponds, we detected hybrid breakdown in both ecotypes but this was counterbalanced by heterosis and the strength of post-zygotic isolation was nil. In aquaria, we detected heterosis only in limnetic crosses and breakdown in neither ecotype, suggesting that hybrid incompatibilities are environment-dependent for both ecotypes and that heterosis is environment-dependent in benthic crosses. Heterosis and breakdown were 3× greater in limnetic crosses than in benthic crosses, contrasting the prediction that the fitness consequences of hybridization should be greater in crosses among more derived ecotypes. Consistent with a primary role for stochastic processes, patterns differed among crosses between populations from different lakes. Yet, we observed qualitatively similar patterns of heterosis and hybrid breakdown in benthic crosses and limnetic crosses when averaging the lake pairs, suggesting that the outcome of hybridization is repeatable in a general sense.