Local adaptation and hybrid failure share a common genetic basis

Testing whether local adaptation and intrinsic reproductive isolation share a genetic basis can reveal important connections between adaptation and speciation. Local adaptation arises as advantageous alleles spread through a population, but whether these same advantageous alleles fail on the genetic backgrounds of other populations remains largely unknown. We used a quantitative genetic breeding design to produce a late generation (F4) recombinant hybrid population by equally mating amongst four contrasting ecotypes of a native Australian daisy for four generations. We tracked fitness across generations and measured morphological traits in the glasshouse, and used a reciprocal transplant to quantify fitness in all four parental habitats. In the glasshouse, plants in the second generation showed a reduction in fitness as a loss of fertility, but this was fully recovered in the following generation. The F4 hybrid lacked extreme phenotypes present in the parental ecotypes, suggesting that genes reducing hybrid fitness were linked to traits specific to each ecotype. In the natural habitats, additive genetic variance for fitness was greatest for habitats that showed stronger native-ecotype advantage, suggesting that a loss of genetic variation present in the parental ecotypes were adaptive in the natural habitats. Reductions in genetic variance for fitness were associated with a loss of ecological trade-offs previously described in the parental ecotypes. Furthermore, natural selection on morphological traits differed amongst the parental habitats, but was not predicted to occur towards the morphology of the parental ecotypes. Together, these results suggest that intrinsic reproductive isolation removed adaptive genetic variation present in the parental ecotypes. The evolution of these distinct ecotypes was likely governed by genetic variation that resulted in both ecological trade-offs and intrinsic reproductive isolation among populations adapted to contrasting environments.