Sexual conflict and the gender load: correlated evolution between population fitness and sexual dimorphism in seed beetles

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

10.1101/2020.12.20.423717 ◽

2020 ◽

Author(s):

Basabi Bagchi ◽

Quentin Corbel ◽

Imroze Khan ◽

Ellen Payne ◽

Devshuvam Banerji ◽

...

Keyword(s):

Sex Differences ◽

Sexual Selection ◽

Sexual Dimorphism ◽

Mating System ◽

Sexual Conflict ◽

Experimental Evolution ◽

Parasitic Infections ◽

Expression Of Genes ◽

Trade Offs ◽

Seed Beetles

AbstractSexual 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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Sexual dimorphism explains residual variance around the survival‐reproduction tradeoff in lizards: Implications for sexual conflict over life‐history evolution*

Evolution ◽

10.1111/evo.13799 ◽

2019 ◽

Vol 73 (11) ◽

pp. 2324-2332 ◽

Cited By ~ 2

Author(s):

Aaron M. Reedy ◽

William J. Evans ◽

Robert M. Cox

Keyword(s):

Life History ◽

Sexual Dimorphism ◽

Sexual Conflict ◽

Life History Evolution ◽

Residual Variance ◽

History Evolution

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Genome size correlates with reproductive fitness in seed beetles

Proceedings of The Royal Society B Biological Sciences ◽

10.1098/rspb.2015.1421 ◽

2015 ◽

Vol 282 (1815) ◽

pp. 20151421 ◽

Cited By ~ 14

Author(s):

Göran Arnqvist ◽

Ahmed Sayadi ◽

Elina Immonen ◽

Cosima Hotzy ◽

Daniel Rankin ◽

...

Keyword(s):

Life History ◽

Natural Selection ◽

Genome Size ◽

Evolutionary Biology ◽

Large Scale ◽

Life History Traits ◽

Single Species ◽

Reproductive Fitness ◽

Correlated Evolution ◽

Seed Beetles

The ultimate cause of genome size (GS) evolution in eukaryotes remains a major and unresolved puzzle in evolutionary biology. Large-scale comparative studies have failed to find consistent correlations between GS and organismal properties, resulting in the ‘ C -value paradox’. Current hypotheses for the evolution of GS are based either on the balance between mutational events and drift or on natural selection acting upon standing genetic variation in GS. It is, however, currently very difficult to evaluate the role of selection because within-species studies that relate variation in life-history traits to variation in GS are very rare. Here, we report phylogenetic comparative analyses of GS evolution in seed beetles at two distinct taxonomic scales, which combines replicated estimation of GS with experimental assays of life-history traits and reproductive fitness. GS showed rapid and bidirectional evolution across species, but did not show correlated evolution with any of several indices of the relative importance of genetic drift. Within a single species, GS varied by 4–5% across populations and showed positive correlated evolution with independent estimates of male and female reproductive fitness. Collectively, the phylogenetic pattern of GS diversification across and within species in conjunction with the pattern of correlated evolution between GS and fitness provide novel support for the tenet that natural selection plays a key role in shaping GS evolution.

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Correlated evolution between male ejaculate allocation and female remating behaviour in seed beetles (Bruchidae)

Journal of Evolutionary Biology ◽

10.1111/j.1420-9101.2007.01494.x ◽

2008 ◽

Vol 21 (2) ◽

pp. 471-479 ◽

Cited By ~ 28

Author(s):

M. KATVALA ◽

J. L. RÖNN ◽

G. ARNQVIST

Keyword(s):

Correlated Evolution ◽

Female Remating ◽

Seed Beetles

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Phenotypic sexual dimorphism is associated with genomic signatures of resolved sexual conflict

Molecular Ecology ◽

10.1111/mec.15115 ◽

2019 ◽

Vol 28 (11) ◽

pp. 2860-2871 ◽

Cited By ~ 6

Author(s):

Alison E. Wright ◽

Thea F. Rogers ◽

Matteo Fumagalli ◽

Christopher R. Cooney ◽

Judith E. Mank

Keyword(s):

Sexual Dimorphism ◽

Sexual Conflict ◽

Genomic Signatures

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Sexual conflict and correlated evolution between male persistence and female resistance traits in the seed beetle Callosobruchus maculatus

Proceedings of The Royal Society B Biological Sciences ◽

10.1098/rspb.2017.0132 ◽

2017 ◽

Vol 284 (1855) ◽

pp. 20170132 ◽

Cited By ~ 34

Author(s):

Liam R. Dougherty ◽

Emile van Lieshout ◽

Kathryn B. McNamara ◽

Joe A. Moschilla ◽

Göran Arnqvist ◽

...

Keyword(s):

Sexual Conflict ◽

Male Genitalia ◽

Callosobruchus Maculatus ◽

Negative Relationship ◽

Female Reproductive Tract ◽

Female Resistance ◽

Correlated Evolution ◽

Male And Female ◽

Seed Beetle ◽

Trade Offs

Traumatic mating (or copulatory wounding) is an extreme form of sexual conflict whereby male genitalia physically harm females during mating. In such species females are expected to evolve counter-adaptations to reduce male-induced harm. Importantly, female counter-adaptations may include both genital and non-genital traits. In this study, we examine evolutionary associations between harmful male genital morphology and female reproductive tract morphology and immune function across 13 populations of the seed beetle Callosobruchus maculatus . We detected positive correlated evolution between the injuriousness of male genitalia and putative female resistance adaptations across populations. Moreover, we found evidence for a negative relationship between female immunity and population productivity, which suggests that investment in female resistance may be costly due to the resource trade-offs that are predicted between immunity and reproduction. Finally, the degree of female tract scarring (harm to females) was greater in those populations with both longer aedeagal spines and a thinner female tract lining. Our results are thus consistent with a sexual arms race, which is only apparent when both male and female traits are taken into account. Importantly, our study provides rare evidence for sexually antagonistic coevolution of male and female traits at the within-species level.

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Sensory exploitation and sexual conflict

Philosophical Transactions of the Royal Society B Biological Sciences ◽

10.1098/rstb.2005.1790 ◽

2006 ◽

Vol 361 (1466) ◽

pp. 375-386 ◽

Cited By ~ 117

Author(s):

Göran Arnqvist

Keyword(s):

Sexual Dimorphism ◽

Sexual Conflict ◽

Theoretical Models ◽

Sensory Exploitation ◽

Subsequent Evolution ◽

Female Preferences ◽

General Importance ◽

Evolution Of Resistance ◽

Sexual Traits ◽

Sexually Antagonistic Coevolution

Much of the literature on male–female coevolution concerns the processes by which male traits and female preferences for these can coevolve and be maintained by selection. There has been less explicit focus on the origin of male traits and female preferences. Here, I argue that it is important to distinguish origin from subsequent coevolution and that insights into the origin can help us appreciate the relative roles of various coevolutionary processes for the evolution of diversity in sexual dimorphism. I delineate four distinct scenarios for the origin of male traits and female preferences that build on past contributions, two of which are based on pre-existing variation in quality indicators among males and two on exploitation of pre-existing sensory biases among females. Recent empirical research, and theoretical models, suggest that origin by sensory exploitation has been widespread. I argue that this points to a key, but perhaps transient, role for sexually antagonistic coevolution (SAC) in the subsequent evolutionary elaboration of sexual traits, because (i) sensory exploitation is often likely to be initially costly for individuals of the exploited sex and (ii) the subsequent evolution of resistance to sensory exploitation should often be associated with costs due to selective constraints. A review of a few case studies is used to illustrate these points. Empirical data directly relevant to the costs of being sensory exploited and the costs of evolving resistance is largely lacking, and I stress that such data would help determining the general importance of sexual conflict and SAC for the evolution of sexual dimorphism.

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Kin but less than kind: within-group male relatedness does not increase female fitness in seed beetles

Proceedings of The Royal Society B Biological Sciences ◽

10.1098/rspb.2019.1664 ◽

2019 ◽

Vol 286 (1910) ◽

pp. 20191664 ◽

Cited By ~ 1

Author(s):

Elena C. Berg ◽

Martin I. Lind ◽

Shannon Monahan ◽

Sophie Bricout ◽

Alexei A. Maklakov

Keyword(s):

Sexual Conflict ◽

Callosobruchus Maculatus ◽

Lifetime Reproductive Success ◽

Cognitive Error ◽

Individual Fitness ◽

Adaptive Mechanisms ◽

Female Survival ◽

Reproductive Part ◽

Seed Beetles

Theory maintains within-group male relatedness can mediate sexual conflict by reducing male–male competition and collateral harm to females. We tested whether male relatedness can lessen female harm in the seed beetle Callosobruchus maculatus . Male relatedness did not influence female lifetime reproductive success or individual fitness across two different ecologically relevant scenarios of mating competition. However, male relatedness marginally improved female survival. Because male relatedness improved female survival in late life when C. maculatus females are no longer producing offspring, our results do not provide support for the role of within-group male relatedness in mediating sexual conflict. The fact that male relatedness improves the post-reproductive part of the female life cycle strongly suggests that the effect is non-adaptive. We discuss adaptive and non-adaptive mechanisms that could result in reduced female harm in this and previous studies, and suggest that cognitive error is a likely explanation.

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