Genotypes and their interaction effects on reproduction and mating‐induced immune activation in <i>Drosophila melanogaster</i>

Fricke, Claudia; Ávila‐Calero, Sergio; Armitage, Sophie A. O.

doi:10.1111/jeb.13625

Cited by 6 publications

(5 citation statements)

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“… (a) There were significant differences in PO activity throughout development, with levels near zero detected in male (blue) and female (red) pupae and virgin adult males, but detectable levels in (unsexed = black) larvae and high levels in virgin adult females. (b) PO activity measured on day 3 in females mated only on day one (100), day one and two (110), day one and three (101), or on all days (111) (open symbols). A second experiment measured PO activity for a random set of females assigned to treatments 100 and 001 (mated only on day three) (filled symbols).…”

Section: Resultsmentioning

confidence: 99%

“…While previous studies have quantified female immune responses post mating (5,5,22,23,45,50,53,99,100), it often remains unclear whether male harm via genitalia or ejaculatory compounds (i.e. sexual antagonism) drive such responses, or whether they represent independent female optimization of the trade-off between current and future reproduction (5,22,23,27,49,101).…”

Section: Discussionmentioning

confidence: 99%

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Sexual conflict drives micro- and macroevolution of sexual dimorphism in immunity

Bagchi

Corbel

Khan

et al. 2020

Preprint

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Sexual dimorphism in immunity is believed to reflect sex-differences in trade-offs between competing life history demands. Sexual selection can have major effects on mating rates and sex-specific costs of mating and may thereby influence sex-differences in immunity as well as associated host-pathogen dynamics. Yet, experimental data linking the mating system to evolved sexual dimorphism in immunity are scarce and the direct effects of mating rate on immunity are not well established. Here, we use transcriptomic analyses, experimental evolution and phylogenetic comparative methods to study the association between the mating system and sexual dimorphism in immunity in seed beetles, where mating causes internal injuries in females. We demonstrate that female phenoloxidase (PO) activity, involved in wound healing and defence against parasitic infections, is elevated relative to males as a result of sex-biased expression of genes in the proPO activating cascade. We document substantial phenotypic plasticity in female PO activity in response to mating and show that experimental evolution under enforced monogamy (relative to natural polygamy) rapidly decreases female (but not male) PO activity. The evolution of decreased PO in monogamous females was accompanied by increased tolerance to bacterial infection unrelated to mating. This implies that female responses to costly mating may trade off with other aspects of immune defence. Finally, female (but not male) PO activity show correlated evolution with the perceived harmfulness of male genitalia across 12 species of seed beetles, suggesting that sexual conflict has a significant influence on sexual dimorphisms in immunity in this group of insects. Our results thus provide a proximate and ultimate understanding of the links between sexual selection and sexual dimorphism in immunity.

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Section: Resultsmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Sexual conflict drives micro- and macroevolution of sexual dimorphism in immunity

Bagchi

Corbel

Khan

et al. 2020

Preprint

View full text Add to dashboard Cite

show abstract

“…While previous studies have quantified female immune responses post mating [ 5 , 22 , 23 , 45 , 50 , 53 , 100 , 101 ], it often remains unclear whether male harm via genitalia or ejaculatory compounds (i.e. sexual antagonism) drive such responses, or whether they represent independent female optimization of the trade-off between current and future reproduction [ 5 , 22 , 23 , 27 , 49 , 102 ].…”

Section: Discussionmentioning

confidence: 99%

Sexual conflict drives micro- and macroevolution of sexual dimorphism in immunity

et al. 2021

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Background Sexual dimorphism in immunity is believed to reflect sex differences in reproductive strategies and trade-offs between competing life history demands. Sexual selection can have major effects on mating rates and sex-specific costs of mating and may thereby influence sex differences in immunity as well as associated host–pathogen dynamics. Yet, experimental evidence linking the mating system to evolved sexual dimorphism in immunity are scarce and the direct effects of mating rate on immunity are not well established. Here, we use transcriptomic analyses, experimental evolution and phylogenetic comparative methods to study the association between the mating system and sexual dimorphism in immunity in seed beetles, where mating causes internal injuries in females. Results We demonstrate that female phenoloxidase (PO) activity, involved in wound healing and defence against parasitic infections, is elevated relative to males. This difference is accompanied by concomitant sex differences in the expression of genes in the prophenoloxidase activating cascade. We document substantial phenotypic plasticity in female PO activity in response to mating and show that experimental evolution under enforced monogamy (resulting in low remating rates and reduced sexual conflict relative to natural polygamy) rapidly decreases female (but not male) PO activity. Moreover, monogamous females had evolved increased tolerance to bacterial infection unrelated to mating, implying that female responses to costly mating may trade off with other aspects of immune defence, an hypothesis which broadly accords with the documented sex differences in gene expression. Finally, female (but not male) PO activity shows correlated evolution with the perceived harmfulness of male genitalia across 12 species of seed beetles, suggesting that sexual conflict has a significant influence on sexual dimorphisms in immunity in this group of insects. Conclusions Our study provides insights into the links between sexual conflict and sexual dimorphism in immunity and suggests that selection pressures moulded by mating interactions can lead to a sex-specific mosaic of immune responses with important implications for host–pathogen dynamics in sexually reproducing organisms.

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“…Immune responses can be sexually dimorphic in this species (McKean and Nunney 2005 ; Siva-Jothy and Vale 2021 ; Vincent and Dionne 2021 ), and there is some evidence that immune defence can be subject to IASC (Vincent and Sharp 2014 ). In addition, upregulation of immune genes after mating Fricke et al ( 2020 ) suggests that IRSC could be a contributing factor to the evolution of this sexual dimorphism (Fedorka et al 2007 ; Innocenti and Morrow 2009 , but see Short and Lazzaro 2010 ). Similarly, longevity is also sexually dimorphic and has been found to be subject to ongoing IRSC in Drosophila (Wigby and Chapman 2004 ; Nandy et al 2013 ; Arbuthnott et al 2014 ; Duxbury et al 2017 ), and results from other species suggest that it could potentially be subject to IASC as well (e.g.…”

Section: Introductionmentioning

confidence: 99%

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

Lund-Hansen

Kutzer

Armitage

et al. 2022

Behav Ecol Sociobiol

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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.

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Genotypes and their interaction effects on reproduction and mating‐induced immune activation in Drosophila melanogaster

Abstract: This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

Cited by 6 publications

References 49 publications

Sexual conflict drives micro- and macroevolution of sexual dimorphism in immunity

Sexual conflict drives micro- and macroevolution of sexual dimorphism in immunity

Sexual conflict drives micro- and macroevolution of sexual dimorphism in immunity

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

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