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Interactions with ectoparasitic mites induce host metabolic and immune responses in flies at the expense of reproduction-associated factors

Published online by Cambridge University Press:  05 June 2020

Joshua B. Benoit Open the ORCID record for Joshua B. Benoit [Opens in a new window] ,
Joy Bose ,
Samuel T. Bailey  and
Michal Polak
Joshua B. Benoit*
Affiliation:
Department of Biological Sciences, University of Cincinnati, Cincinnati, OH45221, USA
Joy Bose
Affiliation:
Department of Biological Sciences, University of Cincinnati, Cincinnati, OH45221, USA
Samuel T. Bailey
Affiliation:
Department of Biological Sciences, University of Cincinnati, Cincinnati, OH45221, USA
Michal Polak
Affiliation:
Department of Biological Sciences, University of Cincinnati, Cincinnati, OH45221, USA
*
Author for correspondence: Joshua B. Benoit, E-mail: joshua.benoit@uc.edu
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Abstract

Parasites cause harm to their hosts and represent pervasive causal agents of natural selection. Understanding host proximate responses during interactions with parasites can help predict which genes and molecular pathways are targets of this selection. In the current study, we examined transcriptional changes arising from interactions between Drosophila melanogaster and their naturally occurring ectoparasitic mite, Gamasodes queenslandicus. Shifts in host transcript levels associated with behavioural avoidance revealed the involvement of genes underlying nutrient metabolism. These genetic responses were reflected in altered body lipid and glycogen levels in the flies. Mite infestation triggered a striking immune response, while male accessory gland protein transcript levels were simultaneously reduced, suggesting a trade-off between host immune responses to parasite challenge and reproduction. Comparison of transcriptional analyses during mite infestation to those during nematode and parasitoid attack identified host genes similarly expressed in flies during these interactions. Validation of the involvement of specific genes with RNA interference lines revealed candidates that may directly mediate fly–ectoparasite interactions. Our physiological and molecular characterization of the Drosophila–Gamasodes interface reveals new proximate mechanisms underlying host–parasite interactions, specifically host transcriptional shifts associated with behavioural avoidance and infestation. The results identify potential general mechanisms underlying host resistance and evolutionarily relevant trade-offs.

Keywords

DrosophilaectoparasiteGamasodesmitesnutrient levelsparasite resistanceRNA-seqtrade-offs
Type
Research Article
Information
Parasitology , Volume 147 , Issue 11 , September 2020 , pp. 1196 - 1205
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Copyright
Copyright © The Author(s) 2020. Published by Cambridge University Press

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