Rapid speciation via parallel, directional selection on regulatory geneticpathways

Regulatory genetic pathways are ubiquitous in organisms and play a central role in the realization of the phenotype during development. We explored th e proposition that these pathways can provide a plausible source of the epi static variation that has been implicated in the evolution of postzygotic r eproductive isolation. We modeled gene regulation as a matching function be tween the product of one locus and the promoter site of the next locus in t he pathway, with binding strength determining the amount of product. When t he phenotype is subject to parallel selection in a pair of independent popu lations, we find that the fitnesses of F-1 and F-2 hybrids often drop to ve ry low values as the populations respond in genetically different and incom patible ways. The simulations support the predictions of the analytical mod els. Hybrid fitness reduction occurs more often as the number of loci in th e pathway increases, and as the binding site interactions become more compl ex. Less hybrid fitness reduction is seen when the populations start with i mperfect binding in the pathway. In contrast, when we constructed the pheno type without gene regulation using multiplicative rules, isomorphic to the additive phenotype commonly assumed in evolutionary models, we found no app reciable F-1 fitness reduction and only slight F-2 fitness reduction. The i nteraction of genetic drift and mutation, even at very high rates, did not reduce hybrid fitness at all on the time-scales we considered. Clearly, the evolution of regulatory genetic pathways can play an important role in spe ciation, but much more empirical information is needed on the effect of all elic variability in regulatory site interactions before this role is fully understood. (C) 2000 Academic Press.