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

2020 ◽  
Author(s):  
Basabi Bagchi ◽  
Quentin Corbel ◽  
Imroze Khan ◽  
Ellen Payne ◽  
Devshuvam Banerji ◽  
...  

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.

BMC Biology ◽  
2021 ◽  
Vol 19 (1) ◽  
Author(s):  
Basabi Bagchi ◽  
Quentin Corbel ◽  
Imroze Khan ◽  
Ellen Payne ◽  
Devshuvam Banerji ◽  
...  

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.


2020 ◽  
Vol 40 (6) ◽  
pp. 649-656
Author(s):  
Juan C Azofeifa-Solano ◽  
Jeffrey A Sibaja-Cordero ◽  
Ingo S Wehrtmann

Abstract The sexual selection over traits that favor access to mating partners could promote the emergence of sexual dimorphism when the pressure is different between sexes. Monogamous species are considered to have a low degree of sexual dimorphism. The highly diverse snapping shrimps are usually regarded as monogamous, but the mating system has been studied only in few species. We aimed to provide insights into the mating system and sexual dimorphism of Alpheus colombiensisWicksten, 1988. The adult sex ratio was female biased, and solitary ovigerous females were found, suggesting a temporary mate guarding type of mating system. Our results also revealed sexual dimorphism on the snapping claw, which is larger in males than in females. The male’s snapping claw is probably under sexual selection, which can be mediated by male-male competition or female choice. We also estimated the A. colombiensis female size at maturity at 5.2 ± 0.76 mm. Our results contradict the common idea that snapping shrimps are monogamous species, and support that A. colombiensis probably have a temporary mate guarding (e.g., males can sexually interact with more than one female, in opposition to sexual monogamy). This study also sustains the growing evidence that alpheid shrimps display snapping claw sexual dimorphism.


2019 ◽  
Author(s):  
Nathan William Burke ◽  
Shinichi Nakagawa ◽  
Russell Bonduriansky

ABSTRACTTransgenerational plasticity (TGP) occurs when the environment experienced by parents induces changes in traits of offspring and/or subsequent generations. Such effects can be adaptive or non-adaptive and are increasingly recognised as key determinants of health, cognition, development and performance across a wide range of taxa, including humans. While the conditions that favour maternal TGP are well understood, rapidly accumulating evidence indicates that TGP can be maternal or paternal, and offspring responses can be sex-specific. However, the evolutionary mechanisms that drive this diversity are unknown. We used an individual-based model to investigate the evolution of TGP when the sexes experience different ecologies. We find that adaptive TGP rarely evolves when alleles at loci that determine offspring responses to environmental information originating from the mother and father are subject to sexually antagonistic selection. By contrast, duplication and sex-limitation of such loci can allow for the evolution of a variety of sex-specific responses, including non-adaptive sex-specific TGP when sexual selection is strong. Sexual conflict could therefore help to explain why adaptive TGP evolves in some species but not others, why sons and daughters respond to parental signals in different ways, and why complex patterns of sex-specific TGP may often be non-adaptive.


2019 ◽  
Author(s):  
Åsa Lankinen ◽  
Maria Strandh

AbstractPremise of the ResearchThe wide diversity of floral traits seen among plants is shaped by neutral and selective evolutionary processes. In outcrossing species, sexual selection from competing pollen donors is expected to be important for shaping mating system-related traits but empirical evidence is scarce. In a previous evaluation of experimental evolution lines crossed with either one or two pollen donors (monogamous, M, or polyandrous, P, lines) at early floral stages in mixed-mating Collinsia heterophylla (Plantaginaceae), P showed enhanced pollen competitive ability and reduced maternal seed set compared to M, in accordance with sexually antagonistic evolution of pollen. Here, we asked whether the presence of sexual selection during pollen competition affect mating system-related floral traits in the same lines.MethodologyWe compared flowering start, timing of anther-stigma contact (as an indication of timing of self-pollination), timing of stigma receptivity and first seed set between M and P, and with a source line, S (starting material). The former three traits are later in outcrossers than in selfers of Collinsia. The latter trait was expected to be earlier in P than in M because of sexual selection for early seed siring of pollen.Pivotal ResultsArtificial polyandry for four generations resulted in later flowering start and later anther-stigma contact in P compared to M, and the latter trait was intermediate in S. Thus, P appeared more ‘outcrossing’ than M. Stigma receptivity did not differ between lines. First seed set was earlier in P than in M, as expected from sexual selection.ConclusionsOur results from C. heterophylla experimental evolution lines suggest that a component of sexual selection during outcross pollination could enhance the patterns of floral divergence commonly found between outcrossers and selfers.


2018 ◽  
Vol 373 (1757) ◽  
pp. 20170419 ◽  
Author(s):  
Anna Runemark ◽  
Fabrice Eroukhmanoff ◽  
Angela Nava-Bolaños ◽  
Jo S. Hermansen ◽  
Joana I. Meier

While gene flow can reduce the potential for local adaptation, hybridization may conversely provide genetic variation that increases the potential for local adaptation. Hybridization may also affect adaptation through altering sexual dimorphism and sexual conflict, but this remains largely unstudied. Here, we discuss how hybridization may affect sexual dimorphism and conflict due to differential effects of hybridization on males and females, and then how this, in turn, may affect local adaptation. First, in species with heterochromatic sexes, the lower viability of the heterogametic sex in hybrids could shift the balance in sexual conflict. Second, sex-specific inheritance of the mitochondrial genome in hybrids may lead to cytonuclear mismatches, for example, in the form of ‘mother's curse’, with potential consequences for sex ratio and sex-specific expression. Third, sex-biased introgression and recombination may lead to sex-specific consequences of hybridization. Fourth, transgressive segregation of sexually antagonistic alleles could increase sexual dimorphism in hybrid populations. Sexual dimorphism can reduce sexual conflict and enhance intersexual niche partitioning, increasing the fitness of hybrids. Adaptive introgression of alleles reducing sexual conflict or enhancing intersexual niche partitioning may facilitate local adaptation, and could favour the colonization of novel habitats. We review these consequences of hybridization on sex differences and local adaptation, and discuss how their prevalence and importance could be tested empirically. This article is part of the theme issue ‘Linking local adaptation with the evolution of sex differences'.


2007 ◽  
Vol 19 (2) ◽  
pp. 309-316 ◽  
Author(s):  
Cécile Vanpé ◽  
Petter Kjellander ◽  
Maxime Galan ◽  
Jean-François Cosson ◽  
Stéphane Aulagnier ◽  
...  

2018 ◽  
Author(s):  
Bart P. S. Nieuwenhuis ◽  
Duur K. Aanen

SummaryWhen many gametes compete to fertilize a limited number of compatible gametes, sexual selection will favour traits that increase competitive success during mating. In animals and plants, sperm and pollen competition have yielded many interesting adaptations for improved mating success. In fungi, similar processes have not been shown directly yet. We test the hypothesis that sexual selection can increase competitive fitness during mating, using experimental evolution in the mushroom-forming fungus Schizophyllum commune (Basidiomycota). Mating in mushroom fungi occurs by donation of nuclei to a mycelium. These fertilizing ‘male’ nuclei migrate through the receiving ‘female’ mycelium. In our setup, an evolving population of nuclei was serially mated with a non-evolving female mycelium for 20 sexual generations. From the twelve tested evolved lines, four had increased and one had decreased fitness relative to an unevolved competitor. Even though only two of those five remained significant after correcting for multiple comparisons, for all five lines we found a correlation between the efficiency with which the female mycelium is accessed and fitness, providing additional circumstantial evidence for fitness change in those five lines. In two lines, fitness change was also accompanied by increased spore production. The one line with net reduced competitive fitness had increased spore production, but reduced fertilisation efficiency. We did not find trade-offs between male reproductive success and other fitness components. We compare these findings with examples of sperm and pollen competition and show that many similarities between these systems and nuclear competition in mushrooms exist.


2021 ◽  
Author(s):  
Julian Baur ◽  
Dorian Jagusch ◽  
Piotr Michalak ◽  
Mareike Koppik ◽  
David Berger

1. To mitigate effects of climate change it is important to understand species responses to increasing temperatures. This has often been done by studying survival or activity at temperature extremes. Before such extremes are reached, however, effects on fertility may already be apparent. 2. Sex differences in the thermal sensitivity of fertility (TSF) could impact species persistence under climate warming because female fertility is typically more limiting to population growth than male fertility. However, little is known about sex differences in TSF. 3. Here we first demonstrate that the mating system can strongly influence TSF using the seed beetle Callosobruchus maculatus. We exposed populations carrying artificially induced mutations to two generations of short-term experimental evolution under alternative mating systems, manipulating the opportunity for natural and sexual selection on the mutations. We then measured TSF in males and females subjected to juvenile or adult heat stress. 4. Populations kept under natural and sexual selection had higher fitness, but similar TSF, compared to control populations kept under relaxed selection. However, females had higher TSF than males, and strikingly, this sex difference had increased over only two generations in populations evolving under sexual selection. 5. We hypothesized that an increase in male-induced harm to females during mating had played a central role in driving this evolved sex difference, and indeed, remating under conditions limiting male harassment of females reduced both male and female TSF. Moreover, we show that manipulation of mating system parameters in C. maculatus generates intraspecific variation in the sex difference in TSF equal to that found among a diverse set of studies on insects. 6. Our study provides a causal link between the mating system and TSF. Sexual conflict, (re)mating rates, and genetic responses to sexual selection differ among ecological settings, mating systems and species. Our study therefore also provides mechanistic understanding for the variability in previously reported TSFs which can inform future experimental assays and predictions of species responses to climate warming.


Evolution ◽  
2019 ◽  
Vol 73 (12) ◽  
pp. 2390-2400 ◽  
Author(s):  
Julian Baur ◽  
Jean d'Amour Nsanzimana ◽  
David Berger

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