Response to selection for parasitism of a suboptimal, low‐preference host in an aphid parasitoid

Abstract

Risks of postintroduction evolution in insects introduced to control invasive pests have been discussed for some time, but little is known about responses to selection or genetic architectures of host adaptation 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 suboptimal, low‐preference host species by an aphid parasitoid, Aphelinus rhamni, a candidate for introduction against the soy bean 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 2 and 3, and at generation 3, we 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. Selection for R. padi parasitism reduced parasitism of Aphis glycines, the original host of A. rhamni. However, parasitism of R. padi did not increase from generation 2 to generation 3 of selection, suggesting reduced variance available for selection, which was indeed found. We tested the associations between 184 single nucleotide polymorphisms (SNP) and increased parasitism of R. padi and found 28 SNP loci, some of which were associated with increased and others with decreased parasitism of R. padi. We assembled and annotated the A. rhamni genome, mapped all SNP loci to contigs and tested whether genes on contigs with SNP loci associated with parasitism were enriched for candidate genes or gene functions. We identified 80 genes on these contigs that mapped to 1.2 Mb of the 483 Mb genome of A. rhamni but found little enrichment of candidate genes or gene functions.

Limited gains in native parasitoid performance on an invasive host beyond three generations of selection

“…The speed at which parasitoids respond to selection on a novel host can be rapid but there can also be limits to the level of adaptation achieved. For example, parasitism by Aphelinus rhamni (Hopper and Woolley) (Hymenoptera: Aphelinidae) on the novel aphid host, Rhopalosiphum padi (L.) (Hemiptera: Aphididae) increased significantly after two generations of selection but further improvement was not observed in generation three (Hopper et al, 2021 ). Despite the rapid response to selection, A. rhamni parasitism on the novel host remained well below parasitism rates on its original host of Aphis glcyines (Matsumura) (Hemiptera: Aphididae) even after 150 generations of selection (Hopper et al, 2021 ), which could be partly due to its initial restricted host range.…”

“…For example, parasitism by Aphelinus rhamni (Hopper and Woolley) (Hymenoptera: Aphelinidae) on the novel aphid host, Rhopalosiphum padi (L.) (Hemiptera: Aphididae) increased significantly after two generations of selection but further improvement was not observed in generation three (Hopper et al, 2021 ). Despite the rapid response to selection, A. rhamni parasitism on the novel host remained well below parasitism rates on its original host of Aphis glcyines (Matsumura) (Hemiptera: Aphididae) even after 150 generations of selection (Hopper et al, 2021 ), which could be partly due to its initial restricted host range. Similarly, we found that the response to selection of both P. vindemmiae and T. drosophilae was initially rapid but developmental success did not continue to increase after the third generation of selection for either species.…”

“…In biological control programs, laboratory selection has been used in rare cases to increase the performance of parasitoids on sub‐optimal hosts (Lirakis & Magalhães, 2019 ) and to improve effectiveness of native parasitoids at attacking invasive hosts (Jarrett et al, 2022 ; Kruitwagen et al, 2021 ). Laboratory selection has also been used to assess the possibility of postintroduction evolution of exotic parasitoids to infest native nontarget hosts more effectively (Hopper et al, 2021 ). The few studies to date highlight the variable responses of parasitoids to selection imposed by a novel host that may stem from differences in the parasitoid's initial host range, life history traits, or standing genetic variation within the population.…”

“…We know from multiple systems including Drosophilids (Jarrett et al, 2022 ), various aphid (Dion et al, 2011 ; Henry et al, 2010 ; Hopper et al, 2021 ), and moth (Jones et al, 2015 ) host species that in the laboratory parasitoids can evolve increased developmental success on a novel host rapidly, often within 3–10 generations. It is unclear how universal these responses may be among different parasitoid species and if there may be an ideal length for laboratory selection that balances increased effectiveness and the cost of conducting long selection experiments.…”

“…It is unclear how universal these responses may be among different parasitoid species and if there may be an ideal length for laboratory selection that balances increased effectiveness and the cost of conducting long selection experiments. Some studies indicate that response to selection can be as rapid as 2–4 generations, beyond which further improvement of parasitoids is negligible (Dion et al, 2011 ; Hopper et al, 2021 ). However, there are also examples of continued improvement of parasitoid performance on a sub‐optimal host for up to 40 generations of selection (Henry et al, 2008 ).…”