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Studying host-based divergence naturally maintained by a balance between selection and gene flow can provide valuable insights into genetic underpinnings of host adaptation and ecological speciation in parasites. Selection-gene flow balance is often postulated in sympatric host races, but direct experimental evidence is scarce. In this study, we present such evidence obtained in host races of Aphidius ervi, an important hymenopteran agent of biological control of aphids in agriculture, using a novel fusion-fission method of gene flow perturbation. In our study, between-race genetic divergence was obliterated by means of advanced hybridisation, followed by a multi-generation exposure of the resulting genetically uniform hybrid swarm to a two-host environment. This fusion-fission procedure was implemented under two contrasting regimes of between-host gene flow in two replicated experiments involving different racial pairs. Host-based genetic fission in response to environmental bimodality occurred in both experiments in as little as six generations of divergent adaptation despite continuous gene flow. We demonstrate that fission recovery of host-based divergence evolved faster and hybridisation-induced linkage disequilibrium decayed slower under restricted (6.7%) compared with unrestricted gene flow, directly pointing at a balance between gene flow and divergent selection. We also show, in four separate tests, that random drift had no or little role in the observed genetic split. Rates and patterns of fission divergence differed between racial pairs. Comparative linkage analysis of these differences is currently under way to test for the role of genomic architecture of adaptation in ecology-driven divergent evolution.

Fusion–fission experiments in Aphidius: evolutionary split without isolation in response to environmental bimodality