Adaptive divergence and the evolution of hybrid phenotypes in threespine stickleback

The fitness of hybrids is a critical determinant of gene flow between hybridizing populations. If hybrid phenotypes change predictably as parental populations become increasingly divergent, this could provide insight into general mechanisms linking ecological divergence with reproductive isolation. In this study, we used threespine stickleback fish (Gasterosteus aculeatus L.) to examine how phenotypic divergence between populations drives the evolution of dominance, phenotypic variation, and trait `mismatch9 in hybrids. We generated F1 and F2 hybrids between 12 freshwater populations---which ranged from highly planktivorous to highly benthic-feeding---and an anadromous population that is highly planktivorous and resembles the ancestral state of derived freshwater populations. We measured 16 phenotypic traits in hybrids and pure parental individuals raised under common conditions. We found that dominance varied markedly among traits. By contrast, dominance for a given trait was typically consistent among populations except for two traits where dominance was predicted by the phenotype of the freshwater parent. We find that multivariate phenotypic variation is greater in hybrids between more divergent parents. Finally, we demonstrate that the extent to which parental traits are `mismatched9 in both F1 and F2 hybrids increases with the phenotypic distance between the parent populations. Critically, this relationship was clearer in F1 hybrids than in F2s---largely due to traits having different dominance coefficients and F1s having relatively little phenotypic variation. Our results demonstrate that some aspects of hybrid phenotypes evolve predictably as parental populations diverge. We also find evidence for a possible general mechanistic link between ecological divergence and reproductive isolation---that more divergent parent populations tend to produce hybrids with novel and potentially deleterious multivariate phenotypes.