Complex evolution in Aphis gossypii group (Hemiptera: Aphididae), evidence of primary host shift and hybridization between sympatric species

Aphids provide a good model system to understand the ecological speciation concept, since the majority of the species are host-specific, and they spend their entire lifecycle on certain groups of host plants. Aphid species that apparently have wide host plant ranges have often turned out to be complexes of host-specialized biotypes. Here we investigated the various host-associated populations of the two recently diverged species, Aphis gossypii and A. rhamnicola, having multiple primary hosts, to understand the complex evolution with host-associated speciation. Using mitochondrial DNA marker and nine microsatellite loci, we reconstructed the haplotype network, and analyzed the genetic structure and relationships. Approximate Bayesian computation was also used to infer the ancestral primary host and host-associated divergence, which resulted in Rhamnus being the most ancestral host for A. gossypii and A. rhamnicola. As a result, Aphis gossypii and A. rhamnicola do not randomly use their primary and secondary host plants; rather, certain biotypes use only some secondary and specific primary hosts. Some biotypes are possibly in a diverging state through specialization to specific primary hosts. Our results also indicate that a new heteroecious race can commonly be derived from the heteroecious ancestor, showing strong evidence of ecological specialization through a primary host shift in both A. gossypii and A. rhamnicola. Interestingly, A. gossypii and A. rhamnicola shared COI haplotypes with each other, thus there is a possibility of introgression by hybridization between them by cross-sharing same primary hosts. Our results contribute to a new perspective in the study of aphid evolution by identifying complex evolutionary trends in the gossypii sensu lato complex.