Parasitic wasp-associated symbiont affects plant-mediated species interactions between herbivores

Antonino Cusumano*, Feng Zhu, Anne Nathalie Volkoff, Patrick Verbaarschot, Janneke Bloem, Heiko Vogel, Marcel Dicke, Erik H. Poelman

*Corresponding author for this work

Research output: Contribution to journalLetterAcademicpeer-review

12 Citations (Scopus)

Abstract

Microbial mutualistic symbiosis is increasingly recognised as a hidden driving force in the ecology of plant–insect interactions. Although plant-associated and herbivore-associated symbionts clearly affect interactions between plants and herbivores, the effects of symbionts associated with higher trophic levels has been largely overlooked. At the third-trophic level, parasitic wasps are a common group of insects that can inject symbiotic viruses (polydnaviruses) and venom into their herbivorous hosts to support parasitoid offspring development. Here, we show that such third-trophic level symbionts act in combination with venom to affect plant-mediated interactions by reducing colonisation of subsequent herbivore species. This ecological effect correlated with changes induced by polydnaviruses and venom in caterpillar salivary glands and in plant defence responses to herbivory. Because thousands of parasitoid species are associated with mutualistic symbiotic viruses in an intimate, specific relationship, our findings may represent a novel and widespread ecological phenomenon in plant–insect interactions.

Original languageEnglish
Pages (from-to)957-967
JournalEcology Letters
Volume21
Issue number7
DOIs
Publication statusPublished - 1 Jul 2018

Fingerprint

venom
symbiont
wasp
symbionts
trophic level
herbivore
venoms
herbivores
Polydnaviridae
parasitoid
virus
ecological phenomena
plant defense
caterpillar
symbiosis
microsymbionts
herbivory
viruses
colonization
salivary glands

Keywords

  • Herbivore colonisation
  • parasitoid
  • plant–insect interactions
  • polydnaviruses
  • tritrophic interactions

Cite this

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title = "Parasitic wasp-associated symbiont affects plant-mediated species interactions between herbivores",
abstract = "Microbial mutualistic symbiosis is increasingly recognised as a hidden driving force in the ecology of plant–insect interactions. Although plant-associated and herbivore-associated symbionts clearly affect interactions between plants and herbivores, the effects of symbionts associated with higher trophic levels has been largely overlooked. At the third-trophic level, parasitic wasps are a common group of insects that can inject symbiotic viruses (polydnaviruses) and venom into their herbivorous hosts to support parasitoid offspring development. Here, we show that such third-trophic level symbionts act in combination with venom to affect plant-mediated interactions by reducing colonisation of subsequent herbivore species. This ecological effect correlated with changes induced by polydnaviruses and venom in caterpillar salivary glands and in plant defence responses to herbivory. Because thousands of parasitoid species are associated with mutualistic symbiotic viruses in an intimate, specific relationship, our findings may represent a novel and widespread ecological phenomenon in plant–insect interactions.",
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author = "Antonino Cusumano and Feng Zhu and Volkoff, {Anne Nathalie} and Patrick Verbaarschot and Janneke Bloem and Heiko Vogel and Marcel Dicke and Poelman, {Erik H.}",
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Parasitic wasp-associated symbiont affects plant-mediated species interactions between herbivores. / Cusumano, Antonino; Zhu, Feng; Volkoff, Anne Nathalie; Verbaarschot, Patrick; Bloem, Janneke; Vogel, Heiko; Dicke, Marcel; Poelman, Erik H.

In: Ecology Letters, Vol. 21, No. 7, 01.07.2018, p. 957-967.

Research output: Contribution to journalLetterAcademicpeer-review

TY - JOUR

T1 - Parasitic wasp-associated symbiont affects plant-mediated species interactions between herbivores

AU - Cusumano, Antonino

AU - Zhu, Feng

AU - Volkoff, Anne Nathalie

AU - Verbaarschot, Patrick

AU - Bloem, Janneke

AU - Vogel, Heiko

AU - Dicke, Marcel

AU - Poelman, Erik H.

PY - 2018/7/1

Y1 - 2018/7/1

N2 - Microbial mutualistic symbiosis is increasingly recognised as a hidden driving force in the ecology of plant–insect interactions. Although plant-associated and herbivore-associated symbionts clearly affect interactions between plants and herbivores, the effects of symbionts associated with higher trophic levels has been largely overlooked. At the third-trophic level, parasitic wasps are a common group of insects that can inject symbiotic viruses (polydnaviruses) and venom into their herbivorous hosts to support parasitoid offspring development. Here, we show that such third-trophic level symbionts act in combination with venom to affect plant-mediated interactions by reducing colonisation of subsequent herbivore species. This ecological effect correlated with changes induced by polydnaviruses and venom in caterpillar salivary glands and in plant defence responses to herbivory. Because thousands of parasitoid species are associated with mutualistic symbiotic viruses in an intimate, specific relationship, our findings may represent a novel and widespread ecological phenomenon in plant–insect interactions.

AB - Microbial mutualistic symbiosis is increasingly recognised as a hidden driving force in the ecology of plant–insect interactions. Although plant-associated and herbivore-associated symbionts clearly affect interactions between plants and herbivores, the effects of symbionts associated with higher trophic levels has been largely overlooked. At the third-trophic level, parasitic wasps are a common group of insects that can inject symbiotic viruses (polydnaviruses) and venom into their herbivorous hosts to support parasitoid offspring development. Here, we show that such third-trophic level symbionts act in combination with venom to affect plant-mediated interactions by reducing colonisation of subsequent herbivore species. This ecological effect correlated with changes induced by polydnaviruses and venom in caterpillar salivary glands and in plant defence responses to herbivory. Because thousands of parasitoid species are associated with mutualistic symbiotic viruses in an intimate, specific relationship, our findings may represent a novel and widespread ecological phenomenon in plant–insect interactions.

KW - Herbivore colonisation

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