Cargando…

Parasitism causes changes in caterpillar odours and associated bacterial communities with consequences for host-location by a hyperparasitoid

Microorganisms living in and on macroorganisms may produce microbial volatile compounds (mVOCs) that characterise organismal odours. The mVOCs might thereby provide a reliable cue to carnivorous enemies in locating their host or prey. Parasitism by parasitoid wasps might alter the microbiome of thei...

Descripción completa

Detalles Bibliográficos
Autores principales: Bourne, Mitchel E., Gloder, Gabriele, Weldegergis, Berhane T., Slingerland, Marijn, Ceribelli, Andrea, Crauwels, Sam, Lievens, Bart, Jacquemyn, Hans, Dicke, Marcel, Poelman, Erik H.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10069771/
https://www.ncbi.nlm.nih.gov/pubmed/36947551
http://dx.doi.org/10.1371/journal.ppat.1011262
_version_ 1785018914200092672
author Bourne, Mitchel E.
Gloder, Gabriele
Weldegergis, Berhane T.
Slingerland, Marijn
Ceribelli, Andrea
Crauwels, Sam
Lievens, Bart
Jacquemyn, Hans
Dicke, Marcel
Poelman, Erik H.
author_facet Bourne, Mitchel E.
Gloder, Gabriele
Weldegergis, Berhane T.
Slingerland, Marijn
Ceribelli, Andrea
Crauwels, Sam
Lievens, Bart
Jacquemyn, Hans
Dicke, Marcel
Poelman, Erik H.
author_sort Bourne, Mitchel E.
collection PubMed
description Microorganisms living in and on macroorganisms may produce microbial volatile compounds (mVOCs) that characterise organismal odours. The mVOCs might thereby provide a reliable cue to carnivorous enemies in locating their host or prey. Parasitism by parasitoid wasps might alter the microbiome of their caterpillar host, affecting organismal odours and interactions with insects of higher trophic levels such as hyperparasitoids. Hyperparasitoids parasitise larvae or pupae of parasitoids, which are often concealed or inconspicuous. Odours of parasitised caterpillars aid them to locate their host, but the origin of these odours and its relationship to the caterpillar microbiome are unknown. Here, we analysed the odours and microbiome of the large cabbage white caterpillar Pieris brassicae in relation to parasitism by its endoparasitoid Cotesia glomerata. We identified how bacterial presence in and on the caterpillars is correlated with caterpillar odours and tested the attractiveness of parasitised and unparasitised caterpillars to the hyperparasitoid Baryscapus galactopus. We manipulated the presence of the external microbiome and the transient internal microbiome of caterpillars to identify the microbial origin of odours. We found that parasitism by C. glomerata led to the production of five characteristic volatile products and significantly affected the internal and external microbiome of the caterpillar, which were both found to have a significant correlation with caterpillar odours. The preference of the hyperparasitoid was correlated with the presence of the external microbiome. Likely, the changes in external microbiome and body odour after parasitism were driven by the resident internal microbiome of caterpillars, where the bacterium Wolbachia sp. was only present after parasitism. Micro-injection of Wolbachia in unparasitised caterpillars increased hyperparasitoid attraction to the caterpillars compared to untreated caterpillars, while no differences were found compared to parasitised caterpillars. In conclusion, our results indicate that host-parasite interactions can affect multi-trophic interactions and hyperparasitoid olfaction through alterations of the microbiome.
format Online
Article
Text
id pubmed-10069771
institution National Center for Biotechnology Information
language English
publishDate 2023
publisher Public Library of Science
record_format MEDLINE/PubMed
spelling pubmed-100697712023-04-04 Parasitism causes changes in caterpillar odours and associated bacterial communities with consequences for host-location by a hyperparasitoid Bourne, Mitchel E. Gloder, Gabriele Weldegergis, Berhane T. Slingerland, Marijn Ceribelli, Andrea Crauwels, Sam Lievens, Bart Jacquemyn, Hans Dicke, Marcel Poelman, Erik H. PLoS Pathog Research Article Microorganisms living in and on macroorganisms may produce microbial volatile compounds (mVOCs) that characterise organismal odours. The mVOCs might thereby provide a reliable cue to carnivorous enemies in locating their host or prey. Parasitism by parasitoid wasps might alter the microbiome of their caterpillar host, affecting organismal odours and interactions with insects of higher trophic levels such as hyperparasitoids. Hyperparasitoids parasitise larvae or pupae of parasitoids, which are often concealed or inconspicuous. Odours of parasitised caterpillars aid them to locate their host, but the origin of these odours and its relationship to the caterpillar microbiome are unknown. Here, we analysed the odours and microbiome of the large cabbage white caterpillar Pieris brassicae in relation to parasitism by its endoparasitoid Cotesia glomerata. We identified how bacterial presence in and on the caterpillars is correlated with caterpillar odours and tested the attractiveness of parasitised and unparasitised caterpillars to the hyperparasitoid Baryscapus galactopus. We manipulated the presence of the external microbiome and the transient internal microbiome of caterpillars to identify the microbial origin of odours. We found that parasitism by C. glomerata led to the production of five characteristic volatile products and significantly affected the internal and external microbiome of the caterpillar, which were both found to have a significant correlation with caterpillar odours. The preference of the hyperparasitoid was correlated with the presence of the external microbiome. Likely, the changes in external microbiome and body odour after parasitism were driven by the resident internal microbiome of caterpillars, where the bacterium Wolbachia sp. was only present after parasitism. Micro-injection of Wolbachia in unparasitised caterpillars increased hyperparasitoid attraction to the caterpillars compared to untreated caterpillars, while no differences were found compared to parasitised caterpillars. In conclusion, our results indicate that host-parasite interactions can affect multi-trophic interactions and hyperparasitoid olfaction through alterations of the microbiome. Public Library of Science 2023-03-22 /pmc/articles/PMC10069771/ /pubmed/36947551 http://dx.doi.org/10.1371/journal.ppat.1011262 Text en © 2023 Bourne et al https://creativecommons.org/licenses/by/4.0/This is an open access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Bourne, Mitchel E.
Gloder, Gabriele
Weldegergis, Berhane T.
Slingerland, Marijn
Ceribelli, Andrea
Crauwels, Sam
Lievens, Bart
Jacquemyn, Hans
Dicke, Marcel
Poelman, Erik H.
Parasitism causes changes in caterpillar odours and associated bacterial communities with consequences for host-location by a hyperparasitoid
title Parasitism causes changes in caterpillar odours and associated bacterial communities with consequences for host-location by a hyperparasitoid
title_full Parasitism causes changes in caterpillar odours and associated bacterial communities with consequences for host-location by a hyperparasitoid
title_fullStr Parasitism causes changes in caterpillar odours and associated bacterial communities with consequences for host-location by a hyperparasitoid
title_full_unstemmed Parasitism causes changes in caterpillar odours and associated bacterial communities with consequences for host-location by a hyperparasitoid
title_short Parasitism causes changes in caterpillar odours and associated bacterial communities with consequences for host-location by a hyperparasitoid
title_sort parasitism causes changes in caterpillar odours and associated bacterial communities with consequences for host-location by a hyperparasitoid
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10069771/
https://www.ncbi.nlm.nih.gov/pubmed/36947551
http://dx.doi.org/10.1371/journal.ppat.1011262
work_keys_str_mv AT bournemitchele parasitismcauseschangesincaterpillarodoursandassociatedbacterialcommunitieswithconsequencesforhostlocationbyahyperparasitoid
AT glodergabriele parasitismcauseschangesincaterpillarodoursandassociatedbacterialcommunitieswithconsequencesforhostlocationbyahyperparasitoid
AT weldegergisberhanet parasitismcauseschangesincaterpillarodoursandassociatedbacterialcommunitieswithconsequencesforhostlocationbyahyperparasitoid
AT slingerlandmarijn parasitismcauseschangesincaterpillarodoursandassociatedbacterialcommunitieswithconsequencesforhostlocationbyahyperparasitoid
AT ceribelliandrea parasitismcauseschangesincaterpillarodoursandassociatedbacterialcommunitieswithconsequencesforhostlocationbyahyperparasitoid
AT crauwelssam parasitismcauseschangesincaterpillarodoursandassociatedbacterialcommunitieswithconsequencesforhostlocationbyahyperparasitoid
AT lievensbart parasitismcauseschangesincaterpillarodoursandassociatedbacterialcommunitieswithconsequencesforhostlocationbyahyperparasitoid
AT jacquemynhans parasitismcauseschangesincaterpillarodoursandassociatedbacterialcommunitieswithconsequencesforhostlocationbyahyperparasitoid
AT dickemarcel parasitismcauseschangesincaterpillarodoursandassociatedbacterialcommunitieswithconsequencesforhostlocationbyahyperparasitoid
AT poelmanerikh parasitismcauseschangesincaterpillarodoursandassociatedbacterialcommunitieswithconsequencesforhostlocationbyahyperparasitoid