Abstract

Generalist parasitoids of aphids, such as the wasp Aphidius ervi, display significant differences in terms of host preference and host acceptance, depending on the host on which they developed (natal host), which is preferred over a non-natal host, a trait known as host fidelity. This trait allows females to quickly find hosts in heterogeneous environments, a process mediated by chemosensory/olfactory mechanisms, as parasitoids rely on olfaction and chemical cues during host selection. Thus, it is expected that proteins participating in chemosensory recognition, such as odorant-binding proteins (OBPs) and odorant receptors (ORs) would play a key role in host preference. In this study, we addressed the effect of parasitoid reciprocal host switching between two aphid hosts (Sitobion avenae and Acyrthosiphon pisum) on the expression patterns of chemosensory genes in the wasp A. ervi. First, by using a transcriptomic approach based on RNAseq of A. ervi females reared on S. avenae and A. pisum, we were able to annotate a total of 91 transcripts related to chemoperception. We also performed an in-silico expression analysis and found three OBPs and five ORs displaying different expression levels. Then, by using qRT-PCR amplification, we found significant differences in the expression levels of these eight genes when the parasitoids were reciprocally transplanted from S. avenae onto A. pisum and vice versa. This suggests that the expression levels of genes coding for odorant receptors and odorant-binding proteins would be regulated by the specific plant–aphid host complex where the parasitoids develop (maternal previous experience) and that chemosensory genes coding for olfactory mechanisms would play a crucial role on host preference and host acceptance, ultimately leading to the establishment of host fidelity in A. ervi parasitoids.

Highlights

  • Parasitoid wasps are a diverse group of hymenopterans that are natural enemies of a broad range of arthropods, including those of agronomic significance [1]

  • We performed a thorough annotation for genes encoding odorant-binding proteins (OBPs), chemosensory proteins (CSPs), and odorant receptors (ORs) found within the A. ervi transcriptome [33]

  • We observed a variation in the expression levels when comparing chemosensory genes of parasitoids originated from A. pisum and S. avenae that were reared on their natal host or transplanted to non-natal hosts (Figures 1 and 2)

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Summary

Introduction

Parasitoid wasps are a diverse group of hymenopterans that are natural enemies of a broad range of arthropods, including those of agronomic significance [1]. Parasitoids have an important role in the regulation of arthropod population sizes in natural environments [1] and have been used as biocontrol agents to reduce the population densities of target pest species [2,3]. This is the case of the endoparasitoid wasp Aphidius ervi Haliday (Hymenoptera: Braconidae), a worldwide distributed koinobiont parasitoid. Used in biological control programs, A. ervi mainly parasitizes the pea aphid Acyrthosiphon pisum Harris (Hemiptera: Aphididae) [5,6], it has become an important biocontrol agent of the grain aphid Sitobion avenae Fabricius (Hemiptera: Aphididae) [7,8]. The successful use of A. ervi in biological control programs depends on the specificity of host selection and host acceptance behaviors and on host suitability, as not all host species are suitable for parasitoids [9]

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