Two different adaptive speciation mechanisms operate during adaptation to a novel hot environment

Abstract Background Ecological speciation and mutation-order speciation are two different mechanisms of adaptation-driven speciation. Both mechanisms predict different patterns of reproductive isolation for replicate populations adapting to the same environment. With ecological speciation, barriers to gene flow emerge between populations from different environments, but not among replicate populations from the same environment. Mutation-order speciation predicts reproductive isolation among populations adapted to the same environment. Results We demonstrate that both speciation processes occurred within about 100 generations when replicate Drosophila simulans populations adapted to a novel, hot environment. Gene expression analysis identified the underlying molecular mechanisms. Premating ecological speciation is the byproduct of an altered lipid metabolism, which also changed the cuticular hydrocarbon (CHC) composition in hot-evolved flies. Postmating reproductive isolation supports mutation-order speciation most likely driven by co-evolution of reproduction-associated genes. Conclusion Adaptation processes can rapidly induce incipient speciation and different speciation mechanisms affect pre- and postmating reproductive isolation. We propose that the definition of mutation-order speciation should be expanded to account for polygenic processes from standing genetic variation.