Joint effects of group sex-ratio and Wolbachia infection on female reproductive success in the terrestrial isopod Armadillidium vulgare

Abstract Background In species that reproduce with sexual reproduction, males and females often have opposite strategies to maximize their own fitness. For instance, males are typically expected to maximize their number of mating events, whereas an excessive number of mating events can be costly for...

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Main Authors: Margot Fortin, Joël Meunier, Tiffany Laverré, Catherine Souty-Grosset, Freddie-Jeanne Richard
Format: Article
Language:English
Published: BMC 2019-02-01
Series:BMC Evolutionary Biology
Subjects:
Online Access:http://link.springer.com/article/10.1186/s12862-019-1391-6
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author Margot Fortin
Joël Meunier
Tiffany Laverré
Catherine Souty-Grosset
Freddie-Jeanne Richard
author_facet Margot Fortin
Joël Meunier
Tiffany Laverré
Catherine Souty-Grosset
Freddie-Jeanne Richard
author_sort Margot Fortin
collection DOAJ
description Abstract Background In species that reproduce with sexual reproduction, males and females often have opposite strategies to maximize their own fitness. For instance, males are typically expected to maximize their number of mating events, whereas an excessive number of mating events can be costly for females. Although the risk of sexual harassment by males and resulting costs for females are expected to increase with the proportion of males, it remains unknown whether and how parasitic distorters of a host population’s sex-ratio can shape this effect on the fitness of females. Here, we addressed this question using Armadillidium vulgare and its parasite Wolbachia that alters the sex-ratio of a population. We set up Wolbachia-free and Wolbachia-infected females in experimental groups exhibiting 100, 80, 50% or 20% females for 1 year, during which we measured changes in survival, fertility and fecundity. Results Wolbachia infection shaped the effects of both population sex-ratio and reproductive season on female fecundity. Compared to Wolbachia-free females, Wolbachia-infected females were less likely to be gravid in populations exhibiting an excess of females and did not exhibit the otherwise negative effect of seasons on this likelihood. Group sex-ratio and Wolbachia infection have independent effects on other measured traits. Male-biased populations had females both exhibiting the lowest survival rate after 6 months and producing the smallest number of offspring, independent of Wolbachia infection. Conversely, Wolbachia-infected females had the lowest likelihood of producing at least one offspring, independent of group sex-ratio. Wolbachia infection had no effect on female survival rate. Conclusions We demonstrated that male-biased sex-ratio and the presence of Wolbachia are costly for females due to sexual harassment by males and bacterial infection, respectively. Interestingly, Wolbachia infection triggers another negative effect. This effect does not come from an excess of males and its associated sexual harassment of females but instead from a lack of males and the associated risk for females of remaining unmated. Overall, these findings highlight the importance of social pressures and infection on female fitness and provide insights into our general understanding of the joint and opposite effects of these two parameters in the evolution of reproductive strategies.
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spelling doaj.art-b1f9fe9048bd43fb90f18849e8d0db612022-12-21T21:32:21ZengBMCBMC Evolutionary Biology1471-21482019-02-011911810.1186/s12862-019-1391-6Joint effects of group sex-ratio and Wolbachia infection on female reproductive success in the terrestrial isopod Armadillidium vulgareMargot Fortin0Joël Meunier1Tiffany Laverré2Catherine Souty-Grosset3Freddie-Jeanne Richard4Laboratoire Ecologie et Biologie des Interactions, Equipe “Ecologie, Evolution, Symbiose”, UMR CNRS 7267, Université de PoitiersInstitut de Recherche sur la Biologie de l’Insecte (IRBI), UMR 7261, CNRS, Université de ToursLaboratoire Ecologie et Biologie des Interactions, Equipe “Ecologie, Evolution, Symbiose”, UMR CNRS 7267, Université de PoitiersLaboratoire Ecologie et Biologie des Interactions, Equipe “Ecologie, Evolution, Symbiose”, UMR CNRS 7267, Université de PoitiersLaboratoire Ecologie et Biologie des Interactions, Equipe “Ecologie, Evolution, Symbiose”, UMR CNRS 7267, Université de PoitiersAbstract Background In species that reproduce with sexual reproduction, males and females often have opposite strategies to maximize their own fitness. For instance, males are typically expected to maximize their number of mating events, whereas an excessive number of mating events can be costly for females. Although the risk of sexual harassment by males and resulting costs for females are expected to increase with the proportion of males, it remains unknown whether and how parasitic distorters of a host population’s sex-ratio can shape this effect on the fitness of females. Here, we addressed this question using Armadillidium vulgare and its parasite Wolbachia that alters the sex-ratio of a population. We set up Wolbachia-free and Wolbachia-infected females in experimental groups exhibiting 100, 80, 50% or 20% females for 1 year, during which we measured changes in survival, fertility and fecundity. Results Wolbachia infection shaped the effects of both population sex-ratio and reproductive season on female fecundity. Compared to Wolbachia-free females, Wolbachia-infected females were less likely to be gravid in populations exhibiting an excess of females and did not exhibit the otherwise negative effect of seasons on this likelihood. Group sex-ratio and Wolbachia infection have independent effects on other measured traits. Male-biased populations had females both exhibiting the lowest survival rate after 6 months and producing the smallest number of offspring, independent of Wolbachia infection. Conversely, Wolbachia-infected females had the lowest likelihood of producing at least one offspring, independent of group sex-ratio. Wolbachia infection had no effect on female survival rate. Conclusions We demonstrated that male-biased sex-ratio and the presence of Wolbachia are costly for females due to sexual harassment by males and bacterial infection, respectively. Interestingly, Wolbachia infection triggers another negative effect. This effect does not come from an excess of males and its associated sexual harassment of females but instead from a lack of males and the associated risk for females of remaining unmated. Overall, these findings highlight the importance of social pressures and infection on female fitness and provide insights into our general understanding of the joint and opposite effects of these two parameters in the evolution of reproductive strategies.http://link.springer.com/article/10.1186/s12862-019-1391-6SymbiosisMate choiceMultiple matingBreeding successes
spellingShingle Margot Fortin
Joël Meunier
Tiffany Laverré
Catherine Souty-Grosset
Freddie-Jeanne Richard
Joint effects of group sex-ratio and Wolbachia infection on female reproductive success in the terrestrial isopod Armadillidium vulgare
BMC Evolutionary Biology
Symbiosis
Mate choice
Multiple mating
Breeding successes
title Joint effects of group sex-ratio and Wolbachia infection on female reproductive success in the terrestrial isopod Armadillidium vulgare
title_full Joint effects of group sex-ratio and Wolbachia infection on female reproductive success in the terrestrial isopod Armadillidium vulgare
title_fullStr Joint effects of group sex-ratio and Wolbachia infection on female reproductive success in the terrestrial isopod Armadillidium vulgare
title_full_unstemmed Joint effects of group sex-ratio and Wolbachia infection on female reproductive success in the terrestrial isopod Armadillidium vulgare
title_short Joint effects of group sex-ratio and Wolbachia infection on female reproductive success in the terrestrial isopod Armadillidium vulgare
title_sort joint effects of group sex ratio and wolbachia infection on female reproductive success in the terrestrial isopod armadillidium vulgare
topic Symbiosis
Mate choice
Multiple mating
Breeding successes
url http://link.springer.com/article/10.1186/s12862-019-1391-6
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