Sex-specific patterns of senescence in artificial insect populations varying in sex-ratio to manipulate reproductive effort

Abstract Background The disposable soma theory of ageing assumes that organisms optimally trade-off limited resources between reproduction and longevity to maximize fitness. Early reproduction should especially trade-off against late reproduction and longevity because of reduced investment into soma...

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Main Authors: Charly Jehan, Manon Chogne, Thierry Rigaud, Yannick Moret
Format: Article
Language:English
Published: BMC 2020-02-01
Series:BMC Evolutionary Biology
Subjects:
Online Access:https://doi.org/10.1186/s12862-020-1586-x
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author Charly Jehan
Manon Chogne
Thierry Rigaud
Yannick Moret
author_facet Charly Jehan
Manon Chogne
Thierry Rigaud
Yannick Moret
author_sort Charly Jehan
collection DOAJ
description Abstract Background The disposable soma theory of ageing assumes that organisms optimally trade-off limited resources between reproduction and longevity to maximize fitness. Early reproduction should especially trade-off against late reproduction and longevity because of reduced investment into somatic protection, including immunity. Moreover, as optimal reproductive strategies of males and females differ, sexually dimorphic patterns of senescence may evolve. In particular, as males gain fitness through mating success, sexual competition should be a major factor accelerating male senescence. In a single experiment, we examined these possibilities by establishing artificial populations of the mealworm beetle, Tenebrio molitor, in which we manipulated the sex-ratio to generate variable levels of investment into reproductive effort and sexual competition in males and females. Results As predicted, variation in sex-ratio affected male and female reproductive efforts, with contrasted sex-specific trade-offs between lifetime reproduction, survival and immunity. High effort of reproduction accelerated mortality in females, without affecting immunity, but high early reproductive success was observed only in balanced sex-ratio condition. Male reproduction was costly on longevity and immunity, mainly because of their investment into copulations rather than in sexual competition. Conclusions Our results suggest that T. molitor males, like females, maximize fitness through enhanced longevity, partly explaining their comparable longevity.
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spelling doaj.art-194ace5c6a0d402ba651dc61873fbcf62022-12-21T18:23:53ZengBMCBMC Evolutionary Biology1471-21482020-02-0120111310.1186/s12862-020-1586-xSex-specific patterns of senescence in artificial insect populations varying in sex-ratio to manipulate reproductive effortCharly Jehan0Manon Chogne1Thierry Rigaud2Yannick Moret3UMR CNRS 6282 BioGéoSciences, Équipe Écologie Évolutive, Université Bourgogne-Franche ComtéUMR CNRS 6282 BioGéoSciences, Équipe Écologie Évolutive, Université Bourgogne-Franche ComtéUMR CNRS 6282 BioGéoSciences, Équipe Écologie Évolutive, Université Bourgogne-Franche ComtéUMR CNRS 6282 BioGéoSciences, Équipe Écologie Évolutive, Université Bourgogne-Franche ComtéAbstract Background The disposable soma theory of ageing assumes that organisms optimally trade-off limited resources between reproduction and longevity to maximize fitness. Early reproduction should especially trade-off against late reproduction and longevity because of reduced investment into somatic protection, including immunity. Moreover, as optimal reproductive strategies of males and females differ, sexually dimorphic patterns of senescence may evolve. In particular, as males gain fitness through mating success, sexual competition should be a major factor accelerating male senescence. In a single experiment, we examined these possibilities by establishing artificial populations of the mealworm beetle, Tenebrio molitor, in which we manipulated the sex-ratio to generate variable levels of investment into reproductive effort and sexual competition in males and females. Results As predicted, variation in sex-ratio affected male and female reproductive efforts, with contrasted sex-specific trade-offs between lifetime reproduction, survival and immunity. High effort of reproduction accelerated mortality in females, without affecting immunity, but high early reproductive success was observed only in balanced sex-ratio condition. Male reproduction was costly on longevity and immunity, mainly because of their investment into copulations rather than in sexual competition. Conclusions Our results suggest that T. molitor males, like females, maximize fitness through enhanced longevity, partly explaining their comparable longevity.https://doi.org/10.1186/s12862-020-1586-xAgeingCost of reproductionDisposable soma theoryImmunityImmuno-senescenceTenebrio molitor
spellingShingle Charly Jehan
Manon Chogne
Thierry Rigaud
Yannick Moret
Sex-specific patterns of senescence in artificial insect populations varying in sex-ratio to manipulate reproductive effort
BMC Evolutionary Biology
Ageing
Cost of reproduction
Disposable soma theory
Immunity
Immuno-senescence
Tenebrio molitor
title Sex-specific patterns of senescence in artificial insect populations varying in sex-ratio to manipulate reproductive effort
title_full Sex-specific patterns of senescence in artificial insect populations varying in sex-ratio to manipulate reproductive effort
title_fullStr Sex-specific patterns of senescence in artificial insect populations varying in sex-ratio to manipulate reproductive effort
title_full_unstemmed Sex-specific patterns of senescence in artificial insect populations varying in sex-ratio to manipulate reproductive effort
title_short Sex-specific patterns of senescence in artificial insect populations varying in sex-ratio to manipulate reproductive effort
title_sort sex specific patterns of senescence in artificial insect populations varying in sex ratio to manipulate reproductive effort
topic Ageing
Cost of reproduction
Disposable soma theory
Immunity
Immuno-senescence
Tenebrio molitor
url https://doi.org/10.1186/s12862-020-1586-x
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AT thierryrigaud sexspecificpatternsofsenescenceinartificialinsectpopulationsvaryinginsexratiotomanipulatereproductiveeffort
AT yannickmoret sexspecificpatternsofsenescenceinartificialinsectpopulationsvaryinginsexratiotomanipulatereproductiveeffort