Response to selection for parasitism of a sub-optimal, low-preference host in an aphid parasitoid

Authors: Hopper, Keith; Wittmeyer, Kameron; Kuhn, Kristen; Lanier, Kathryn

Submitted to: Evolutionary Applications
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 5/10/2021
Publication Date: 5/20/2021
Citation: Hopper, K.R., Wittmeyer, K.T., Kuhn, K.L., Lanier, K. 2021. Response to selection for parasitism of a sub-optimal, low-preference host in an aphid parasitoid. Evolutionary Applications. 00:1-13. https://doi.org/10.1111/eva.13254.
DOI: https://doi.org/10.1111/eva.13254

Interpretive Summary: Little is known about the likelihood of evolutionary shifts in beneficial insects introduced to control invasive pests. We studied the response to selection and genetics for parasitism of a low-preference, low-quality host species, oat-birdcherry aphid, by an aphid parasite, Aphelinus rhamni, that is a candidate for introduction against soybean aphid. Aphelinus rhamni responded rapidly to selection for parasitism of oat-birdcherry aphid but this did not reduce soybean aphid parasitism. We tested the association between genetic markers and parasitism by Aphelinus rhamni and found 28 markers that either increased or decreased parasitism of oat-birdcherry aphid, across many gene regions that produced similar parasitism. We identified 80 genes associated with parasitism of oat-birdcherry aphid distributed across the A. rhamni genome. This is one of the few studies of the genetics of host specificity in parasitic wasps.

Technical Abstract: Risks of post-introduction evolution in insects introduced to control invasive pests have been discussed for some time, but little is known about responses to selection and genetic architectures of host specificity and thus about the likelihood or rapidity of evolutionary shifts. We report here results on the response to selection and genetic architecture of parasitism of a sub-optimal, low-preference host species by an aphid parasitoid, Aphelinus rhamni, a candidate for introduction against the soybean aphid, Aphis glycines. We selected A. rhamni for increased parasitism of Rhopalsiphum padi by rearing the parasitoid on this aphid for three generations. We measured parasitism of R. padi at generations two and three, and at generation three, crossed and backcrossed parasitoids from the populations reared on R. padi with those from populations reared on Aphis glycines and compared parasitism of both R. padi and Aphis glycines among F1 and backcross females. Aphelinus rhamni responded rapidly to selection for parasitism of R. padi. However, selection for R. padi parasitism did not reduce parasitism of Aphis glycines, the original host of A. rhamni. Furthermore, the response to selection appeared to be asymptotic, with no increase in parasitism from generation two to generation three of selection. We tested the associations between genetic markers and parasitism and found that the genetic architecture appears complex. There were 28 markers that either increased or decreased parasitism of R. padi, across many gene regions that produce similar phenotypes. We assembled and annotated the A. rhamni genome and tested whether genes near genetic markers were enriched for candidate genes or classes of gene functions. We identified 80 genes associated with parasitism of R. padi distributed across the A. rhamni genome but not enrichment of candidate genes or functions. These results provide one of the few studies of the genetic architecture of host specificity in parasitic wasps.