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Heat disrupts host-parasitoid interactions mediated by a viral symbiont

ABSTRACT: High temperature events can disrupt species interactions, including those among hosts, symbionts, and natural enemies. Understanding the genetic and physiological processes underlying these disruptions is a critical scientific challenge in this era of anthropogenic climate change. We explore how high temperatures disrupt the interactions among an herbivorous insect host, Manduca sexta, its insect parasitoid, Cotesia congregata, and the parasitoid’s symbiotic virus. In this system, high temperatures kill developing parasitoids, but not hosts. We evaluated the physiological and transcriptomic causes of thermal mismatch in ecological interactions using parasitoid egg in vitro experiments, immunological assays, and RNAseq. We found that high temperatures disrupt the capacity of the parasitoid’s symbiotic virus to immunosuppress the host insect, resulting in thermal mismatch and death of the parasitoid. At the transcriptomic level, key viral genes involved in suppressing host immune pathways showed reduced expression, driven by the virus’s circular genomic structure. This work is among the first to demonstrate the genetic and physiological mechanisms by which a symbiont limits the ecological functioning of host-parasite dynamics, and provides a framework for understanding how molecular processes give rise to ecological outcomes in response to high temperature events caused by climate change.

ORGANISM(S): Manduca sexta

PROVIDER: GSE273477 | GEO | 2024/08/04

REPOSITORIES: GEO

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Project description:The whitefly Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae), and the viruses it transmits, are a major constraint to vegetable crops, worldwide. Although the whitefly is usually controlled using chemical pesticides, biological control agents constitute an important component in integrated pest management programs. One of these agents is the wasp Eretmocerus mundus (Mercet) (Hymenoptera: Aphelinidae). E. mundus lays its egg on the leaf underneath the pupa of B. tabaci. First instars of the wasp hatch and penetrate the whitefly larvae. Initiation of parasitization induces the host to form a cellular capsule around the parasitoid. Around this capsule, epidermal cells multiply and thick layers of cuticle are deposited. The physiological and molecular processes underlying B. tabaci-E. mundus interactions have not been investigated so far. We have used a cDNA microarray containing 6,000 expressed sequence tags (ESTs) from the whitefly genome to study the parasitoid-whitefly interaction. We compared RNA samples collected across two time points of the parasitization process: when the parasitoid first instar started the penetration process and once it had fully penetrated the host. The results clearly indicated that genes known to be part of the defense pathways described in other insects are also involved in the response of B. tabaci to parasitization by E. mundus. Some of the responses observed included the repression of a serine protease inhibitor (serpin) and the induction of a melanization cascade. A second set of genes that strongly responded to parasitization included bacterial genes encoded by whitefly symbionts. Quantitative real-time PCR and FISH analyses showed that proliferation of Rickettsia, a facultative secondary symbiont, was strongly induced following the initiation of the parasitization process, a result that supported previous reports suggesting that endosymbionts may be involved in the insect host resistance to various environmental stresses. This is the first study examining the transcriptional response of a hemipteran insect to the attack of a biological control agent (Hymenopterous parasitoid), using a new genomic approach developed for this insect pest. The defense response in B. tabaci seems to resemble that of model organisms such as Drosophila melanogaster. Moreover, endosymbionts of B. tabaci seem to play a role in the response to parasitization, and this is supported by previously published results from aphids. Keywords: time course

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Heat disrupts host-parasitoid interactions mediated by a viral symbiont

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