Incipient speciation by divergent adaptation and antagonistic epistasis in yeast

Establishing the conditions that promote the evolution of reproductive isolation and speciation has long been a goal in evolutionary biology(1-3). In ecological speciation, reproductive isolation between populations evolves as a by-product of divergent selection and the resulting environment-specific adaptations(4-6). The leading genetic model of reproductive isolation predicts that hybrid inferiority is caused by antagonistic epistasis between incompatible alleles at interacting loci(1,7). The fundamental link between divergent adaptation and reproductive isolation through genetic incompatibilities has been predicted(1,4,5), but has not been directly demonstrated experimentally. Here we empirically tested key predictions of speciation theory by evolving the initial stages of speciation in experimental populations of the yeast Saccharomyces cerevisiae. After replicate populations adapted to two divergent environments, we consistently observed the evolution of two forms of postzygotic isolation in hybrids: reduced rate of mitotic reproduction and reduced efficiency of meiotic reproduction. This divergent selection resulted in greater reproductive isolation than parallel selection, as predicted by the ecological speciation theory. Our experimental system allowed controlled comparison of the relative importance of ecological and genetic isolation, and we demonstrated that hybrid inferiority can be ecological and/or genetic in basis. Overall, our results show that adaptation to divergent environments promotes the evolution of reproductive isolation through antagonistic epistasis, providing evidence of a plausible common avenue to speciation and adaptive radiation in nature.