Abstract

The molecular mechanisms that allow generalist parasitoids to exploit many, often very distinct hosts are practically unknown. The wasp Aphidius ervi, a generalist koinobiont parasitoid of aphids, was introduced from Europe into Chile in the late 1970s to control agriculturally important aphid species. A recent study showed significant differences in host preference and host acceptance (infectivity) depending on the host A. ervi were reared on. In contrast, no genetic differentiation between A. ervi populations parasitizing different aphid species and aphids of the same species reared on different host plants was found in Chile. Additionally, the same study did not find any fitness effects in A. ervi if offspring were reared on a different host as their mothers. Here, we determined the effect of aphid host species (Sitobion avenae versus Acyrthosiphon pisum reared on two different host plants alfalfa and pea) on the transcriptome of adult A. ervi females. We found a large number of differentially expressed genes (between host species: head: 2,765; body: 1,216; within the same aphid host species reared on different host plants: alfalfa versus pea: head 593; body 222). As expected, the transcriptomes from parasitoids reared on the same host species (pea aphid) but originating from different host plants (pea versus alfalfa) were more similar to each other than the transcriptomes of parasitoids reared on a different aphid host and host plant (head: 648 and 1,524 transcripts; body: 566 and 428 transcripts). We found several differentially expressed odorant binding proteins and olfactory receptor proteins in particular, when we compared parasitoids from different host species. Additionally, we found differentially expressed genes involved in neuronal growth and development as well as signaling pathways. These results point towards a significant rewiring of the transcriptome of A. ervi depending on aphid-plant complex where parasitoids develop, even if different biotypes of a certain aphid host species (A. pisum) are reared on the same host plant. This difference seems to persist even after the different wasp populations were reared on the same aphid host in the laboratory for more than 50 generations. This indicates that either the imprinting process is very persistent or there is enough genetic/allelic variation between A. ervi populations. The role of distinct molecular mechanisms is discussed in terms of the formation of host fidelity.

Highlights

  • Parasitoids are widely used in biological control programs, which are based on introduced, naturalized, natural or released parasitoid wasps (Starý et al, 1993)

  • Our study provides the first comprehensive reference transcriptome for the aphid parasitoid wasp Aphidius ervi obtained from females reared on three different aphid hosts: two hostraces of the pea aphid A. pisum and the grain aphid S. avenae

  • Gene Ontology (GO) terms enriched in bodies such as peptidase activity (i.e Neprilysin) are probably associated with the presence of transcripts coding for venom proteins, as A. ervi females have glands for venom production that is injected at oviposition and enriched in peptidases (Colinet et al, 2014; Falabella et al, 2007; Nguyen et al, 2013)

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Summary

Introduction

Parasitoids are widely used in biological control programs, which are based on introduced, naturalized, natural or released parasitoid wasps (Starý et al, 1993). Endoparasitoids may attack many related host species (e.g., same family) (Loxdale & Harvey, 2016). They have at the same time the problem to overcome or avoid different defense mechanisms of their varied host species in order to survive through adulthood (Jones et al, 2015). A third alternative is that several host species can be parasitized by the parasitoid using the same strategy/phenotype The former two mechanisms will lead to differences in host preference and host acceptance, affecting behavioral traits associated to host selection (Zepeda-Paulo et al, 2013) but should not necessarily affect or change parasitoid fitness (Rivero, 2000; Wang et al, 2016)

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