Resolution Of Sexual Conflict Research Articles

On the resolution of sexual conflict over shared traits.

Anisogamy, different-sized male and female gametes, sits at the heart of sexual selection and conflict between the sexes. Sperm producers (males) and egg producers (females) of the same species generally share most, if not all, of the same genome, but selection frequently favours different trait values in each sex for traits common to both. The extent to which this conflict might be resolved, and the potential mechanisms by which this can occur, have been widely debated. Here, we summarize recent findings and emphasize that once the sexes evolve, sexual selection is ongoing, and therefore new conflict is always possible. In addition, sexual conflict is largely a multivariate problem, involving trait combinations underpinned by networks of interconnected genes. Although these complexities can hinder conflict resolution, they also provide multiple possible routes to decouple male and female phenotypes and permit sex-specific evolution. Finally, we highlight difficulty in the study of sexual conflict over shared traits and promising directions for future research.

Sex ratios and gender norms: why both are needed to understand sexual conflict in humans.

Sexual conflict theory has been successfully applied to predict how in non-human animal populations, sex ratios can lead to conflicting reproductive interests of females and males and affect their bargaining positions in resolving such conflicts of interests. Recently this theory has been extended to understand the resolution of sexual conflict in humans, but with mixed success. We argue that an underappreciation of the complex relationship between gender norms and sex ratios has hampered a successful understanding of sexual conflict in humans. In this paper, we review and expand upon existing theory to increase its applicability to humans, where gender norms regulate sex ratio effects on sexual conflict. Gender norms constrain who is on the marriage market and how they are valued, and may affect reproductive decision-making power. Gender norms can also directly affect sex ratios, and we hypothesize that they structure how individuals respond to market value gained or lost through biased sex ratios. Importantly, gender norms are in part a product of women's and men's sometimes conflicting reproductive interests, but these norms are also subject to other evolutionary processes. An integration of sexual conflict theory and cultural evolutionary theory is required to allow for a full understanding of sexual conflict in humans.

Unisexual flowers as a resolution to intralocus sexual conflict in hermaphrodites.

In dioecious populations, males and females may evolve different trait values to increase fitness through their respective sexual functions. Because hermaphrodites express both sexual functions, resolving sexual conflict is potentially more difficult for them. Here, we show that hermaphrodite plants can partially resolve sexual conflict by expressing different trait values in different male and female modules (e.g. different flowers, inflorescences, branches etc.). We analysed the flowering phenology, sex allocation and selection gradients on floral traits of flowers of the andromonoecious plant Pulsatilla alpina, which produces both bisexual and male flowers. Our results indicate that strong protogyny prevents early bisexual flowers from profiting from high siring opportunities early in the reproductive season at a time when male flowers could achieve high siring success. The production of unisexual male flowers thus resolves this sexual conflict because it allows the flowers to express their male function without waiting until after the female function has been performed. Our study illustrates the resolution of sexual conflict arising from phenological constraints via modular divergence in sex allocation. We discuss the extent to which modular variation in sex allocation in the context of other sexual systems may be similarly explained.

CHANGES IN DIFFERENTIAL GENE EXPRESSION PATTERN IN FLY HEADS AS THE RESPONSE TO AN EXPERIMENTALLY EVOLVED X CHROMOSOME

Sexually antagonistic (SA) mutations that increase fitness in one sex and decrease it in the other sex (also known as intralocus sexual conflict) are central to the sexual antagonism hypothesis of sex chromosome evolution. It was suggested long ago (by Fisher, in 1931) that tight linkage to a sex-determining locus facilitates the accumulation of SA mutations even when their detrimental effect in one sex exceeds its benefit in the other. Due to the difficulties in detecting SA alleles directly, we know very little about the nature of X-linked SA mutations and their role in the evolution of differential gene expression between sexes. To investigate how X-linked SA mutations affect the transcriptome profile in both sexes, we analyzed changes in genome-wide gene expression pattern in Drosophila melanogaster head tissue that had undergone 95 generations of a female-limited X-chromosome experimental evolution. We found an evidence of change in gene expression towards to the female optimum, which we interpret as the result of resolution of sexual conflict over X-linked SA mutations. In addition, we also found a potential unknown gene expression effect of the balancer chromosome on gene expression (that was necessary to use to limit the inheritance of target X chromosome to the female line). All these findings indicate that a highly polymorphic nature of the X chromosome with an important role in genome-wide gene expression profile.

A novel function of egg burial: burying material prevents eggs rolling out of wind-swayed nests

Egg burial behaviour, that is, when parents bury the eggs with a layer of nest material during the egg-laying stage, has been described in various egg-laying animals. Several functions of egg burial have been described in animals with different life histories and breeding traits, but rarely reveal distinctive functions between sister species. In the polygamous Eurasian penduline tit, Remiz pendulinus , sexual conflict over care has been proposed to drive egg burial since, during egg laying, females hide eggs from males to prevent them abandoning the nest. Females then have the option to desert the clutch themselves and leave parenting to the male. However, in a congeneric species, the Chinese penduline tit, Remiz consobrinus , males have been seen with females in the nest at night, which indicates males know of the eggs’ existence. In this study, we investigated egg burial function in Chinese penduline tits and experimentally tested four hypothesized functions of egg-burying behaviour. (1) We found that egg burial is unlikely to play a role in sexual conflict resolution, as both males and females appeared to bury eggs during egg laying and both freely entered and roosted in the nests with eggs exposed at night. (2) Egg burial does not prevent nest parasitism, as no egg rejection or clutch abandonment was observed in clutches with model parasitic eggs. (3) Our results do not support the temperature regulation hypothesis since the temperature difference between buried and experimentally unburied eggs did not affect hatching success. (4) Notably, our results support the novel egg protection against wind hypothesis since the burying layer efficiently prevented the eggs from rolling out of wind-swayed nests. The difference our study found between the two Remiz species highlights that one behaviour, egg burial, can serve different evolutionary functions between closely related species. • We experimentally tested four functions of egg burial in wild Remiz consobrinus . • Egg burial did not function against brood parasitism or in resolving sexual conflict. • Burying layer regulates egg temperature, but this did not improve hatching success. • Burying material efficiently stops eggs from being blown out of wind-swayed nest. • One behaviour can fulfil different functions even in closely related species.

Sex-biased gene expression and recent sex chromosome turnover.

Cichlids are well known for their propensity to radiate generating arrays of morphologically and ecologically diverse species in short evolutionary time. Following this rapid evolutionary pace, cichlids show high rates of sex chromosome turnover. We here studied the evolution of sex-biased gene (SBG) expression in 14 recently diverged taxa of the Lake Tanganyika Tropheini cichlids, which show different XY sex chromosomes. Across species, sex chromosome sequence divergence predates divergence in expression between the sexes. Only one sex chromosome, the oldest, showed signs of demasculinization in gene expression and potentially contribution to the resolution of sexual conflict. SBGs in general showed high rates of turnovers and evolved mostly under drift. Sexual selection did not shape the rapid evolutionary changes of SBGs. Male-biased genes evolved faster than female-biased genes, which seem to be under more phylogenetic constraint. We found a relationship between the degree of sex bias and sequence evolution driven by sequence differences among the sexes. Consistent with other species, strong sex bias towards sex-limited expression contributes to resolving sexual conflict in cichlids.This article is part of the theme issue ‘Challenging the paradigm in sex chromosome evolution: empirical and theoretical insights with a focus on vertebrates (Part II)’.

Animal personality can modulate sexual conflict over offspring provisioning

Sexual conflict over parental investment is widespread among species with biparental care. Studies have indicated that a high degree of behavioural similarity between the two parents can increase offspring survival; however, it remains unclear how sexual conflict over parental care is resolved. In this study, we examined whether similarity of personality traits between the two parents plays an important role in affecting the provisioning behaviour of each sex in a wild population of the chestnut thrush, Turdus rubrocanus . First, as expected, the mating pairs with more similar personality traits had higher provisioning rates than those pairs with dissimilar traits. Moreover, we found that the similarity of personality traits can modulate the sexual conflict over provisioning in this species, as both parents with more similar partners had relatively higher and less divergent provisioning rates. A partner removal experiment revealed how the sole female or male parent responded when the level of conflict over care increased (the removed partner does not provide any care). The majority of males always reduced their provisioning investment, while females’ decisions depended on the degree of similarity with their partners. Females compensated by provisioning more frequently in pairs of similar personality traits (i.e. accepting a high level of conflict), but reduced their provisioning investment in extremely dissimilar pairs. Our results promote a better understanding of the resolution of sexual conflict over provisioning and highlight the evolutionary significance of mating with similar partners based on certain personality traits. • We studied personality and sexual conflict over provisioning in chestnut thrushes. • Pairs with more similar activity provisioned chicks at higher rates. • Pairs with more similar activity had less divergent provisioning rates. • Activity similarity affected provisioning rate of parent after partner removed.

Genetic basis of susceptibility to low-dose paraquat and variation between the sexes in Drosophila melanogaster.

Toxicant resistance is a complex trait, affected both by genetics and the environment. Like most complex traits, it can exhibit sexual dimorphism, yet sex is often overlooked as a factor in studies of toxicant resistance. Paraquat, one such toxicant, is a commonly used herbicide and is known to produce mitochondrial oxidative stress, decrease dopaminergic neurons and dopamine (DA) levels, and decrease motor ability. While the main effects of paraquat are well-characterized, less is known about the naturally occurring variation in paraquat susceptibility. The purpose of this study was to map the genes contributing to low-dose paraquat susceptibility in Drosophila melanogaster, and to determine if susceptibility differs between the sexes. One hundred of the Drosophila Genetic Reference Panel (DGRP) lines were scored for susceptibility via climbing ability and used in a genome-wide association study (GWAS). Variation in seventeen genes in females and thirty-five genes in males associated with paraquat susceptibility. Only two candidate genes overlapped between the sexes despite a significant positive correlation between male and female susceptibilities. Many associated polymorphisms had significant interactions with sex, with most having conditionally neutral effects. Conditional neutrality between the sexes probably stems from sex-biased expression which may result from partial resolution of sexual conflict. Candidate genes were verified with RNAi knockdowns, gene expression analyses, and DA quantification. Several of these genes are novel associations with paraquat susceptibility. This research highlights the importance of assessing both sexes when studying toxicant susceptibility.

Genomic signatures of globally enhanced gene duplicate accumulation in the megadiverse higher Diptera fueling intralocus sexual conflict resolution.

Gene duplication is an important source of evolutionary innovation. To explore the relative impact of gene duplication during the diversification of major insect model system lineages, we performed a comparative analysis of lineage-specific gene duplications in the fruit fly Drosophila melanogaster (Diptera: Brachycera), the mosquito Anopheles gambiae (Diptera: Culicomorpha), the red flour beetle Tribolium castaneum (Coleoptera), and the honeybee Apis mellifera (Hymenoptera). Focusing on close to 6,000 insect core gene families containing maximally six paralogs, we detected a conspicuously higher number of lineage-specific duplications in Drosophila (689) compared to Anopheles (315), Tribolium (386), and Apis (223). Based on analyses of sequence divergence, phylogenetic distribution, and gene ontology information, we present evidence that an increased background rate of gene duplicate accumulation played an exceptional role during the diversification of the higher Diptera (Brachycera), in part by providing enriched opportunities for intralocus sexual conflict resolution, which may have boosted speciation rates during the early radiation of the megadiverse brachyceran subclade Schizophora.

Differences in the contributions of sex linkage and androgen regulation to sex-biased gene expression in juvenile and adult sticklebacks.

Different evolutionary interests between males and females can lead to the evolution of sexual dimorphism. However, intersex genetic correlations due to the shared genome can constrain the evolution of sexual dimorphism, resulting in intra-locus sexual conflict. One of the mechanisms resolving this conflict is sex linkage, which allows males and females to carry different alleles on sex chromosomes. Another is a regulatory mutation causing sex-biased gene expression, which is often mediated by gonadal steroids in vertebrates. How do these two mechanisms differ in the contributions to the resolution of intra-locus sexual conflict? The magnitude of sexual conflict often varies between the juvenile and adult stages. Because gonadal steroids change in titre during development, we hypothesized that gonadal steroids play a role in sexual dimorphism expression only at certain developmental stages, whereas sex linkage is more important for sexual dimorphism expressed throughout life. Our brain transcriptome analysis of juvenile and adult threespine sticklebacks showed that the majority of genes that were sex-biased in both stages were sex-linked. The relative contribution of androgen-dependent regulation to the sex-biased transcriptome increased and that of sex linkage declined in adults compared to juveniles. The magnitude of the sex differences was greater in sex-linked genes than androgen-responsive genes, suggesting that sex linkage is more effective than androgen regulation in the production of large sex differences in gene expression. Overall, our data are consistent with the hypothesis that sex linkage is effective in resolving sexual conflict throughout life, whereas androgen-dependent regulation can contribute to temporary resolution of sexual conflict.

Sex-dependent dominance maintains migration supergene in rainbow trout

Males and females often differ in their fitness optima for shared traits that have a shared genetic basis, leading to sexual conflict. Morphologically differentiated sex chromosomes can resolve this conflict and protect sexually antagonistic variation, but they accumulate deleterious mutations. However, how sexual conflict is resolved in species that lack differentiated sex chromosomes is largely unknown. Here we present a chromosome-anchored genome assembly for rainbow trout (Oncorhynchus mykiss) and characterize a 55-Mb double-inversion supergene that mediates sex-specific migratory tendency through sex-dependent dominance reversal, an alternative mechanism for resolving sexual conflict. The double inversion contains key photosensory, circadian rhythm, adiposity and sex-related genes and displays a latitudinal frequency cline, indicating environmentally dependent selection. Our results show sex-dependent dominance reversal across a large autosomal supergene, a mechanism for sexual conflict resolution capable of protecting sexually antagonistic variation while avoiding the homozygous lethality and deleterious mutations associated with typical heteromorphic sex chromosomes.

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

Intralocus sexual conflict, where an allele benefits one sex at the expense of the other, has an important role in shaping genetic diversity of populations through balancing selection. However, the potential for mating systems to exert balancing selection through sexual conflict on the genome remains unclear. Furthermore, the nature and potential for resolution of sexual conflict across the genome has been hotly debated. To address this, we analysed de novo transcriptomes from six avian species, chosen to reflect the full range of sexual dimorphism and mating systems. Our analyses combine expression and population genomic statistics across reproductive and somatic tissue, with measures of sperm competition and promiscuity. Our results reveal that balancing selection is weakest in the gonad, consistent with the resolution of sexual conflict and evolutionary theory that phenotypic sex differences are associated with lower levels of ongoing conflict. We also demonstrate a clear link between variation in sexual conflict and levels of genetic variation across phylogenetic space in a comparative framework. Our observations suggest that this conflict is short‐lived, and is resolved via the decoupling of male and female gene expression patterns, with important implications for the role of sexual selection in adaptive potential and role of dimorphism in facilitating sex‐specific fitness optima.

Genome-wide sexually antagonistic variants reveal long-standing constraints on sexual dimorphism in fruit flies.

The evolution of sexual dimorphism is constrained by a shared genome, leading to ‘sexual antagonism’, in which different alleles at given loci are favoured by selection in males and females. Despite its wide taxonomic incidence, we know little about the identity, genomic location, and evolutionary dynamics of antagonistic genetic variants. To address these deficits, we use sex-specific fitness data from 202 fully sequenced hemiclonal Drosophila melanogaster fly lines to perform a genome-wide association study (GWAS) of sexual antagonism. We identify approximately 230 chromosomal clusters of candidate antagonistic single nucleotide polymorphisms (SNPs). In contradiction to classic theory, we find no clear evidence that the X chromosome is a hot spot for sexually antagonistic variation. Characterising antagonistic SNPs functionally, we find a large excess of missense variants but little enrichment in terms of gene function. We also assess the evolutionary persistence of antagonistic variants by examining extant polymorphism in wild D. melanogaster populations and closely related species. Remarkably, antagonistic variants are associated with multiple signatures of balancing selection across the D. melanogaster distribution range and in their sister species D. simulans, indicating widespread and evolutionarily persistent (about 1 million years) genomic constraints on the evolution of sexual dimorphism. Based on our results, we propose that antagonistic variation accumulates because of constraints on the resolution of sexual conflict over protein coding sequences, thus contributing to the long-term maintenance of heritable fitness variation.

Male-biased gene expression resolves sexual conflict through the evolution of sex-specific genetic architecture.

Many genes are subject to contradictory selection pressures in males and females, and balancing selection resulting from sexual conflict has the potential to substantially increase standing genetic diversity in populations and thereby act as an important force in adaptation. However, the underlying causes of sexual conflict, and the potential for resolution, remains hotly debated. Using transcriptome‐resequencing data from male and female guppies, we use a novel approach, combining patterns of genetic diversity and intersexual divergence in allele frequency, to distinguish the different scenarios that give rise to sexual conflict, and how this conflict may be resolved through regulatory evolution. We show that reproductive fitness is the main source of sexual conflict, and this is resolved via the evolution of male‐biased expression. Furthermore, resolution of sexual conflict produces significant differences in genetic architecture between males and females, which in turn lead to specific alleles influencing sex‐specific viability. Together, our findings suggest an important role for sexual conflict in shaping broad patterns of genome diversity, and show that regulatory evolution is a rapid and efficient route to the resolution of conflict.

The resolution of conflict in families.

The emergence of family groups is associated with conflict over the allocation of food or other limited resources. Understanding the mechanisms mediating the resolution of such conflict is a major aim in behavioral ecology. Most empirical work on familial conflict has focused on birds. Here, we highlight how recent work on insects provides new and exciting insights into how such conflict is resolved. This work shows that conflict resolution can be more complex than traditionally envisioned, often involving multiple mechanisms. For example, it shows that the resolution of sexual conflict involves a combination of behavioral negotiation, direct assessment of partner's state, and manipulation using anti-aphrodisiacs or prenatal maternal effects. Furthermore, it highlights that there is a shift from the traditional emphasis on conflict (and competition) to a greater emphasis on the balance between conflict on the one hand and cooperation on the other.

Faking death to avoid male coercion: extreme sexual conflict resolution in a dragonfly.

Faking death to avoid male coercion: extreme sexual conflict resolution in a dragonfly.

Acoustic communication in zebra finches signals when mates will take turns with parental duties

Bi-parental care may involve both cooperation and conflict between parents. Parents adjust their workload to that of their partner and this ability is likely to affect reproductive success. Whether mates communicate, either to resolve the sexual conflict or to coordinate their joint investment in parental care is a largely unaddressed question which we examined by recording wild zebra finches at the nest during incubation. Zebra finch (Taeniopygia guttata) partners produce vocal exchanges at the nest that can be characterized as duets. Some duets end in nest-relief (when birds take turns incubating and foraging) but some do not (when the foraging mate vocally interacts with its incubating partner by coming inside or in the vicinity of the nest). Our data indicate that the structure of the duet predicted its outcome (relief or not), with a parent calling differently before leaving or staying in the nest by modifying its vocal repertoire as well as the acoustic structure of one particular call type which is typically used inside the nest. Zebra finch partners may thus exchange on the time to take turns with parental duties. Our results show that acoustic communication between partners might be of importance in the organization of parental care and could help in understanding sexual conflict resolution or cooperation phenomena in future studies.

The Evolution of Sex Chromosomes and Dosage Compensation in Plants.

Plant sex chromosomes can be vastly different from those of the few historical animal model organisms from which most of our understanding of sex chromosome evolution is derived. Recently, we have seen several advancements from studies on green algae, brown algae, and land plants that are providing a broader understanding of the variable ways in which sex chromosomes can evolve in distant eukaryotic groups. Plant sex-determining genes are being identified and, as expected, are completely different from those in animals. Species with varying levels of differentiation between the X and Y have been found in plants, and these are hypothesized to be representing different stages of sex chromosome evolution. However, we are also finding that sex chromosomes can remain morphologically unchanged over extended periods of time. Where degeneration of the Y occurs, it appears to proceed similarly in plants and animals. Dosage compensation (a phenomenon that compensates for the consequent loss of expression from the Y) has now been documented in a plant system, its mechanism, however, remains unknown. Research has also begun on the role of sex chromosomes in sexual conflict resolution, and it appears that sex-biased genes evolve similarly in plants and animals, although the functions of these genes remain poorly studied. Because the difficulty in obtaining sex chromosome sequences is increasingly being overcome by methodological developments, there is great potential for further discovery within the field of plant sex chromosome evolution.

Selection on an antagonistic behavioral trait can drive rapid genital coevolution in the burying beetle, Nicrophorus vespilloides.

Male and female genital morphology varies widely across many taxa, and even among populations. Disentangling potential sources of selection on genital morphology is problematic because each sex is predicted to respond to adaptations in the other due to reproductive conflicts of interest. To test how variation in this sexual conflict trait relates to variation in genital morphology we used our previously developed artificial selection lines for high and low repeated mating rates. We selected for high and low repeated mating rates using monogamous pairings to eliminate contemporaneous female choice and male–male competition. Male and female genital shape responded rapidly to selection on repeated mating rate. High and low mating rate lines diverged from control lines after only 10 generations of selection. We also detected significant patterns of male and female genital shape coevolution among selection regimes. We argue that because our selection lines differ in sexual conflict, these results support the hypothesis that sexually antagonistic coevolution can drive the rapid divergence of genital morphology. The greatest divergence in morphology corresponded with lines in which the resolution of sexual conflict over mating rate was biased in favor of male interests.

If you eat, I eat: resolution of sexual conflict over consumption from a shared resource

Sexual conflict arises whenever males and females have divergent reproductive interests. The mechanisms mediating the resolution of sexual conflict have been studied extensively in the context of parental care, where each parent adjusts its decision about how much care to provide based on its partner's workload. However, there is currently no information on the mechanisms mediating the resolution of sexual conflict over personal consumption from a shared resource. We address this gap in the burying beetle Nicrophorus vespilloides, which breeds on small vertebrate carcasses. The carcass serves as a source of food for both the developing larvae and the caring parents, and parents feed from the carcass for self-maintenance. To study the mechanisms mediating conflict resolution, we experimentally varied the two parents' body size to create variation in carcass consumption. We then assessed whether each parent adjusted its consumption based on its own size, its partner's size and its partner's consumption. As expected, large parents gained more mass than small parents. Furthermore, males paired to large females gained more mass than males paired to small females, and females responded to their partner's mass change, gaining more mass when their partner did. Our study provides insights into the resolution of a new form of sexual conflict, showing that it is mediated through both matching and sealed-bid responses. Our findings also suggest that the resolution models developed in the context of sexual conflict over biparental care may apply more generally than previously thought.