Evidence That the Microbiota Counteracts Male Outbreeding Strategy by Inhibiting Sexual Signaling in Females

The microbiota is increasingly being recognized as having important impacts on many host biological processes. However, evidence of its effects on animal communication and breeding strategy is lacking. In this three-factorial study, we show that females were more willing to mate with related males,...

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Main Authors: Chloe Heys, Anne Lizé, Hervé Colinet, Thomas A. R. Price, Mark Prescott, Fiona Ingleby, Zenobia Lewis
Format: Article
Language:English
Published: Frontiers Media S.A. 2018-03-01
Series:Frontiers in Ecology and Evolution
Subjects:
Online Access:http://journal.frontiersin.org/article/10.3389/fevo.2018.00029/full
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author Chloe Heys
Anne Lizé
Anne Lizé
Hervé Colinet
Thomas A. R. Price
Mark Prescott
Fiona Ingleby
Zenobia Lewis
author_facet Chloe Heys
Anne Lizé
Anne Lizé
Hervé Colinet
Thomas A. R. Price
Mark Prescott
Fiona Ingleby
Zenobia Lewis
author_sort Chloe Heys
collection DOAJ
description The microbiota is increasingly being recognized as having important impacts on many host biological processes. However, evidence of its effects on animal communication and breeding strategy is lacking. In this three-factorial study, we show that females were more willing to mate with related males, with relatedness likely being assessed through the microbiota. By contrast, male mating investment is concurrently determined by both the relatedness and microbiota status of the female. When the microbiota in female Drosophila melanogaster is altered by an antibiotic, male investment in sperm number increased when mating with unrelated females compared to related ones. Contrastingly, the presence of an intact microbiota in females canceled this male outbreeding strategy. As a consequence, the microbiota, when intact, decreased the fitness of the mating couple. Furthermore, we showed that female sexual signaling (cuticular hydrocarbons), with regards to kin recognition, significantly interacts with microbiota. Interestingly, the interaction is significant for hydrocarbons expressed by both sexes, but not for female-specific compounds. Taken together, our results suggest that microbiota can influence kin recognition by disfavoring male outbreeding strategies, likely by inhibiting key olfactory sexual signaling. This represents the first evidence of a host outbreeding strategy counteracted by their microbiota.
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spelling doaj.art-14204dbed0294229b60ee4dfdfbe1f112022-12-21T17:31:04ZengFrontiers Media S.A.Frontiers in Ecology and Evolution2296-701X2018-03-01610.3389/fevo.2018.00029336961Evidence That the Microbiota Counteracts Male Outbreeding Strategy by Inhibiting Sexual Signaling in FemalesChloe Heys0Anne Lizé1Anne Lizé2Hervé Colinet3Thomas A. R. Price4Mark Prescott5Fiona Ingleby6Zenobia Lewis7Institute of Integrative Biology, University of Liverpool, Liverpool, United KingdomInstitute of Integrative Biology, University of Liverpool, Liverpool, United KingdomUMR 6553 ECOBIO, University of Rennes 1, Rennes, FranceUMR 6553 ECOBIO, University of Rennes 1, Rennes, FranceInstitute of Integrative Biology, University of Liverpool, Liverpool, United KingdomInstitute of Integrative Biology, University of Liverpool, Liverpool, United KingdomEvolution, Behavior and Environment Group, University of Sussex, Brighton, United KingdomInstitute of Integrative Biology, University of Liverpool, Liverpool, United KingdomThe microbiota is increasingly being recognized as having important impacts on many host biological processes. However, evidence of its effects on animal communication and breeding strategy is lacking. In this three-factorial study, we show that females were more willing to mate with related males, with relatedness likely being assessed through the microbiota. By contrast, male mating investment is concurrently determined by both the relatedness and microbiota status of the female. When the microbiota in female Drosophila melanogaster is altered by an antibiotic, male investment in sperm number increased when mating with unrelated females compared to related ones. Contrastingly, the presence of an intact microbiota in females canceled this male outbreeding strategy. As a consequence, the microbiota, when intact, decreased the fitness of the mating couple. Furthermore, we showed that female sexual signaling (cuticular hydrocarbons), with regards to kin recognition, significantly interacts with microbiota. Interestingly, the interaction is significant for hydrocarbons expressed by both sexes, but not for female-specific compounds. Taken together, our results suggest that microbiota can influence kin recognition by disfavoring male outbreeding strategies, likely by inhibiting key olfactory sexual signaling. This represents the first evidence of a host outbreeding strategy counteracted by their microbiota.http://journal.frontiersin.org/article/10.3389/fevo.2018.00029/fullmicrobiotasexual signalingchemical communicationkin recognitionmating behavioroutbreeding strategy
spellingShingle Chloe Heys
Anne Lizé
Anne Lizé
Hervé Colinet
Thomas A. R. Price
Mark Prescott
Fiona Ingleby
Zenobia Lewis
Evidence That the Microbiota Counteracts Male Outbreeding Strategy by Inhibiting Sexual Signaling in Females
Frontiers in Ecology and Evolution
microbiota
sexual signaling
chemical communication
kin recognition
mating behavior
outbreeding strategy
title Evidence That the Microbiota Counteracts Male Outbreeding Strategy by Inhibiting Sexual Signaling in Females
title_full Evidence That the Microbiota Counteracts Male Outbreeding Strategy by Inhibiting Sexual Signaling in Females
title_fullStr Evidence That the Microbiota Counteracts Male Outbreeding Strategy by Inhibiting Sexual Signaling in Females
title_full_unstemmed Evidence That the Microbiota Counteracts Male Outbreeding Strategy by Inhibiting Sexual Signaling in Females
title_short Evidence That the Microbiota Counteracts Male Outbreeding Strategy by Inhibiting Sexual Signaling in Females
title_sort evidence that the microbiota counteracts male outbreeding strategy by inhibiting sexual signaling in females
topic microbiota
sexual signaling
chemical communication
kin recognition
mating behavior
outbreeding strategy
url http://journal.frontiersin.org/article/10.3389/fevo.2018.00029/full
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