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 ‘mismatch’ 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 ‘mismatched’ 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.
Selection against mismatched traits in hybrids is the phenotypic analogue of intrinsic hybrid incompatibilities. Mismatch occurs when hybrids resemble one parent population for some phenotypic traits and the other parent population for other traits, and is caused by dominance in opposing directions or from segregation of alleles in recombinant hybrids. In this study, we used threespine stickleback fish (Gasterosteus aculeatus L.) to test the theoretical prediction that trait mismatch in hybrids should increase with the magnitude of phenotypic divergence between parent populations. We measured morphological traits in parents and hybrids in crosses between a marine population representing the ancestral form and twelve freshwater populations that have diverged from this ancestral state to varying degrees according to their environments. We found that trait mismatch was greater in more divergent crosses for both F 1 and F 2 hybrids. In the F 1 , the divergence-mismatch relationship was caused by traits having dominance in different directions, whereas it was caused by increasing segregating phenotypic variation in the F 2 . Our results imply that extrinsic hybrid incompatibilities accumulate as phenotypic divergence proceeds.
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