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      Female-limited X chromosome evolution reveals that lifespan is mainly modulated by interlocus rather than intralocus sexual conflict

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          Abstract

          Abstract

          Sexual dimorphism in somatic investment may be shaped by two distinct forms of sexual conflict; under intralocus sexual conflict (IASC), males and females have different optimal levels of somatic investment but are constrained from reaching their respective optima by their shared genome, while under interlocus sexual conflict (IRSC), males and females have different optimal sexual strategies, which could have direct or indirect effects on levels of somatic investment. We investigated effects of IASC and IRSC on two aspects of somatic investment, immune defence strategies and longevity, using previously established female-limited experimental evolution lines in Drosophila melanogaster. We found little evidence for any effect of either type of sexual conflict on investment in the immune defence resistance or tolerance. Nor did we find convincing evidence that longevity is subject to IASC in this species. However, we did find evidence that increased female control over mating rate had important and opposite effects on longevity between the sexes. Specifically, females that had adapted to high levels of female control over mating had a longer lifespan when kept in mixed-sex groups, while males had shorter longevity, perhaps due to increased investment in post-copulatory sexual selection. These novel results show that female control over mating rates may have important and unexpected effects on patterns of somatic investment.

          Significance statement

          Sexual conflict occurs between the two sexes over numerous life history traits, and it is complex to disentangle how these traits interact and affect each other. Here we use a long-term evolution experiment to investigate sexual dimorphism in somatic maintenance. We found no effect of feminising the X chromosome on female immune defence. However, we did find that increased female control over mating rate resulted in longer female lifespan, but reduced male lifespan, and that these effects were dependent on social context (isolated or in mixed-sex groups). Unlike previous studies on the effect of sexual conflict on longevity, our experiment did not manipulate environmental conditions nor the adult sex ratio, which is likely to reduce both pre- and post-copulatory sexual selection.

          Supplementary Information

          The online version contains supplementary material available at 10.1007/s00265-022-03231-4.

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          Most cited references55

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          Fitting Linear Mixed-Effects Models Usinglme4

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            Intralocus sexual conflict.

            Intralocus sexual conflict occurs when selection on a shared trait in one sex displaces the other sex from its phenotypic optimum. It arises because many shared traits have a common genetic basis but undergo contrasting selection in the sexes. A recent surge of interest in this evolutionary tug of war has yielded evidence of such conflicts in laboratory and natural populations. Here we highlight outstanding questions about the causes and consequences of intralocus sexual conflict at the genomic level, and its long-term implications for sexual coevolution. Whereas recent thinking has focussed on the role of intralocus sexual conflict as a brake on sexual coevolution, we urge a broader appraisal that also takes account of its potential to drive adaptive evolution and speciation.
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              Sexually antagonistic male adaptation triggered by experimental arrest of female evolution.

              W. Rice (1996)
              Each sex is part of the environment of the other sex. This may lead to perpetual coevolution between the sexes, when adaptation by one sex reduces fitness of the other. Indirect evidence comes from experiments with Drosophila melanogaster indicating that seminal fluid reduces the competitive ability of sperm from other males, thereby increasing male fitness. It also reduces a female's propensity to remate and increase her egg-laying rate. In contrast to these benefits to males, seminal fluid has substantial toxic side effects in females, with increasing quantity leading to decreasing female survival. Here I show that when female D. melanogaster are experimentally prevented from coevolving with males, males rapidly adapt to the static female phenotype. This male adaptation leads to a reduction in female survivorship, which is mediated by an increased rate of remating and increased toxicity of seminal fluid.
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                Author and article information

                Contributors
                Katrine.Lund-Hansen@biol.lu.se
                Journal
                Behav Ecol Sociobiol
                Behav Ecol Sociobiol
                Behavioral Ecology and Sociobiology
                Springer Berlin Heidelberg (Berlin/Heidelberg )
                0340-5443
                1432-0762
                17 August 2022
                17 August 2022
                2022
                : 76
                : 9
                : 120
                Affiliations
                [1 ]GRID grid.4514.4, ISNI 0000 0001 0930 2361, Biology Department, , Lund University, ; Lund, Sweden
                [2 ]GRID grid.4305.2, ISNI 0000 0004 1936 7988, Institute of Evolutionary Biology, , University of Edinburgh, ; Edinburgh, Scotland
                [3 ]GRID grid.14095.39, ISNI 0000 0000 9116 4836, Institute of Biology, , Freie Universität Berlin, ; Berlin, Germany
                Author information
                http://orcid.org/0000-0002-6696-7164
                http://orcid.org/0000-0002-8696-6978
                http://orcid.org/0000-0002-5561-9543
                http://orcid.org/0000-0002-8743-2089
                Article
                3231
                10.1007/s00265-022-03231-4
                9385781
                a5244712-7918-4a1c-b693-ae15845641cd
                © The Author(s) 2022

                Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.

                History
                : 15 May 2022
                : 29 July 2022
                : 8 August 2022
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/501100002805, Carl Tryggers Stiftelse för Vetenskaplig Forskning;
                Award ID: CTS 17:1
                Award Recipient :
                Funded by: European Research Council
                Award ID: ERC-Stg-678148
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100001659, Deutsche Forschungsgemeinschaft;
                Award ID: AR 872/4-1
                Award ID: AR 872/7-1
                Award ID: AR 872/1-1
                Award Recipient :
                Funded by: Lund University
                Categories
                Original Article
                Custom metadata
                © Springer-Verlag GmbH Germany, part of Springer Nature 2022

                Ecology
                resistance,tolerance,drosophila melanogaster,sexual antagonism,experimental evolution,longevity

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