Signature of sexual conflict is actually conflict resolved

There has been substantial interest of late in using population genetic methods to study sexual conflict, where an allele increases the fitness of one sex at some cost to the other (Mank, 2017). Population genomic scans for sexual conflict offer an important advance given the difficulties of identifying antagonistic alleles from more traditional methods, and could greatly increase our understanding of the extent and loci of sexual conflict. This is particularly true for studies in natural populations, for which obtaining accurate fitness measurements for each sex can be challenging. In this issue of Molecular Ecology, Bissegger, Laurentino, Roesti, and Berner (2019) present a cautionary tale about how to interpret these population genomic data.     

Phenotypic differentiation is associated with divergent sexual selection among closely related barn swallow populations

Sexual selection plays a key role in the diversification of numerous animal clades and may accelerate trait divergence during speciation. However, much of our understanding of this process comes from phylogenetic comparative studies, which rely on surrogate measures such as dimorphism that may not represent selection in wild populations. In this study, we assess sexual selection pressures for multiple male visual signals across four barn swallow (Hirundo rustica) populations. Our sample encompassed 2400 linear km and two described subspecies: European H. r. rustica (in the Czech Republic and Romania) and eastern Mediterranean H. r. transitiva (in Israel), as well as a potential area of contact (in Turkey). We demonstrate significant phenotypic differentiation in four sexual signalling axes, despite very low‐level genomic divergence and no comparable divergence in an ecological trait. Moreover, the direction of phenotypic divergence is consistent with differences in sexual selection pressures among subspecies. Thus, H. r. transitiva, which have the darkest ventral plumage of any population, experience directional selection for darker plumage. Similarly, H. r. rustica, which have the longest tail feathers of any population, experience directional selection for elongated tail feathers and disruptive selection for ventral plumage saturation. These results suggest that sexual selection is the primary driver of phenotypic differentiation in this species. Our findings add to growing evidence of phenotypic divergence with gene flow. However, to our knowledge, this is the first study to relate direct measures of the strength and targets of sexual selection to phenotypic divergence among closely related wild populations.     

Sex-specific trait architecture in a spider with sexual size dimorphism

Sexual dimorphism, or sex-specific trait expression, may evolve when selection favours different optima for the same trait between sexes, that is, under antagonistic selection. Intra-locus sexual conflict exists when the sexually dimorphic trait under antagonistic selection is based on genes shared between sexes. A common assumption is that the presence of sexual-size dimorphism (SSD) indicates that sexual conflict has been, at least partly, resolved via decoupling of the trait architecture between sexes. However, whether and how decoupling of the trait architecture between sexes has been realized often remains unknown. We tested for differences in architecture of adult body size between sexes in a species with extreme SSD, the African hermit spider (Nephilingis cruentata), where adult female body size greatly exceeds that of males. Specifically, we estimated the sex-specific importance of genetic and maternal effects on adult body size among individuals that we laboratory-reared for up to eight generations. Quantitative genetic model estimates indicated that size variation in females is to a larger extent explained by direct genetic effects than by maternal effects, but in males to a larger extent by maternal than by genetic effects. We conclude that this sex-specific body-size architecture enables body-size evolution to proceed much more independently than under a common architecture to both sexes.     

Sex-limited mutations and the evolution of sexual dimorphism

Abstract.— Although the developmental and genetic mechanisms underlying sex differences are being elucidated in great detail in a number of species, there remains a breach between proximate and evolutionary studies of sexual dimorphism. More precisely, the evolution of sex-limited gene expression at autosomal loci has not been well reasoned using either theoretical or empirical methods. Here, I show that a Mendelian genetic model including elementary details of sexual differentiation provides novel insight into the evolution of sex differences via sex limitation. This model indicates that the nature of allelic effects and the pattern of selection must be known in both sexes to predict the evolution of sex differences. That is, selection interacts with genetic variation for sexual dimorphism to produce unanticipated patterns of trait divergence or convergence between the sexes. Ultimately, this model may explain why previous models for the evolution of sexual dimorphism do not predict the erratic behavior of the sex difference during artificial selection experiments.     

Stable linkage disequilibrium owing to sexual antagonism

Linkage disequilibrium (LD) is an association between genetic loci that is typically transient. Here, we identify a previously overlooked cause of stable LD that may be pervasive: sexual antagonism. This form of selection produces unequal allele frequencies in males and females each generation, which upon admixture at fertilization give rise to an excess of haplotypes that couple male-beneficial with male-beneficial and female-beneficial with female-beneficial alleles. Under sexual antagonism, LD is obtained for all recombination frequencies in the absence of epistasis. The extent of LD is highest at low recombination and for stronger selection. We provide a partition of the total LD into distinct components and compare our result for sexual antagonism with Li and Nei''s model of LD owing to population subdivision. Given the frequent observation of sexually antagonistic selection in natural populations and the number of traits that are often involved, these results suggest a major contribution of sexual antagonism to genomic structure.     

性选择与性冲突理论在植物繁殖生态学中的应用与进展

性选择与性冲突是植物繁殖性状多样性及性系统演化的重要动力, 二者密切相关却又有所区别, 理解它们的作用机制及其影响对于植物繁殖生态学的研究具有重要意义。当前, 性选择与性冲突理论在植物繁殖生态学中的运用已取得长足进展, 但国内相关研究较少, 对该领域关注不够。因此, 该文对该领域的基本理论和研究进展进行了综述。首先, 阐述性选择与性冲突理论在植物研究中的发展及其运用基础; 其次, 分别从授粉前和授粉后两个阶段详细介绍性选择与性冲突在有花植物繁殖过程中的作用机制及其影响, 并指出环境因素对它们所产生的影响; 最后, 对当前研究存在的不足及该领域未来的研究方向进行总结和展望。希望以此增强人们对性选择和性冲突理论的认识, 促进其在植物繁殖生态学中的运用与发展。     

The genetic basis of sexual dimorphism in birds

The genetic basis of sexual dimorphisms is an intriguing problem of evolutionary genetics because dimorphic traits are limited to one sex. Such traits can arise genetically in two ways. First, the alleles that cause dimorphisms could be limited in expression to only one sex at their first appearance. Alternatively, dimorphism alleles could initially be expressed in both sexes, but subsequently be repressed or promoted in only one sex by the evolution of modifier genes or regulatory elements. We investigated these alternatives by looking for the expression of sexually dimorphic traits in female hybrids between bird species whose males show different types of ornaments. If modifier alleles or regulatory elements involved in sex-limited traits are not completely dominant, the modification should break down in female hybrids, which might then show dimorphic traits resembling those seen in males. Of 13 interspecific hybridizations examined, we found not a single instance of the expression of male-limited ornaments in female hybrids. This suggests that male ornaments were sex limited from the outset or that those traits became sex limited through the evolution of dominant modifiers -- possibly cis-dominant regulatory elements. Observing hybrid phenotypes is a useful approach to studying the genetics and evolution of dimorphic traits.     

Sexual antagonism leads to a mosaic of X-autosome conflict

Males and females have different optimal values for some traits, such as body size. When the same genes control these traits in both sexes, selection pushes in opposite directions in males and females. Alleles at autosomal loci spend equal amounts of time in males and females, suggesting that the sexually antagonistic selective forces may approximately balance between the opposing optima. Frank and Crespi noted that alleles on the X chromosome spend twice as much time in diploid females as in haploid males. That distinction between the sexes may tend to favor X-linked genes that push more strongly toward the female optimum than the male optimum. The female bias of X-linked genes opposes the intermediate optimum of autosomal genes, potentially creating a difference between the direction of selection on traits favored by X chromosomes and autosomes. Patten has recently argued that explicit genetic assumptions about dominance and the relative magnitude of allelic effects may lead X-linked genes to favor the male rather than the female optimum, contradicting Frank and Crespi. This article combines the insights of those prior analyses into a new, more general theory. We find some parameter combinations for X-linked loci that favor a female bias and other parameter combinations that favor a male bias. We conclude that the X likely contains a mosaic pattern of loci that differ with autosomes over sexually antagonistic traits. The overall tendency for a female or male bias on the X depends on prior assumptions about the distribution of key parameters across X-linked loci. Those parameters include the dominance coefficient and the way in which ploidy influences the magnitude of allelic effects.     

Sexual dimorphism and sexual conflict in the diving beetle Agabus uliginosus (L.) (Coleoptera: Dytiscidae)

Sexual conflict can drive intersexual arms races, with female resistance and male persistence traits coevolving antagonistically. Such arms races are well documented in some diving beetles, although the extent of sexual conflict in this family remains unclear. The European dytiscid Agabus uliginosus has a strikingly dimorphic female; individuals from most regions are smooth and male‐like, whereas those from some populations have a strongly roughened dorsum, a trait that has attracted the name dispar. We demonstrate that rough and smooth females differ consistently in the development of dorsal surface microreticulation, and that these females are associated with males that differ in the development of their persistence traits. These findings extend the occurrence of pre‐insemination sexual conflict and associated intrasexual dimorphism in Dytiscidae, and suggest that such mating systems are relatively widespread in these beetles.     

Intralocus sexual conflict and offspring sex ratio

Males and females frequently have different fitness optima for shared traits, and as a result, genotypes that are high fitness as males are low fitness as females, and vice versa. When this occurs, biasing of offspring sex-ratio to reduce the production of the lower-fitness sex would be advantageous, so that for example, broods produced by high-fitness females should contain fewer sons. We tested for offspring sex-ratio biasing consistent with these predictions in broad-horned flour beetles. We found that in both wild-type beetles and populations subject to artificial selection for high- and low-fitness males, offspring sex ratios were biased in the predicted direction: low-fitness females produced an excess of sons, whereas high-fitness females produced an excess of daughters. Thus, these beetles are able to adaptively bias sex ratio and recoup indirect fitness benefits of mate choice.     

Phenotypic plasticity in female mate choice behavior is mediated by an interaction of direct and indirect genetic effects in Drosophila melanogaster

Female mate choice is a complex decision‐making process that involves many context‐dependent factors. In Drosophila melanogaster, a model species for the study of sexual selection, indirect genetic effects (IGEs) of general social interactions can influence female mate choice behaviors, but the potential impacts of IGEs associated with mating experiences are poorly understood. Here, we examined whether the IGEs associated with a previous mating experience had an effect on subsequent female mate choice behaviors and quantified the degree of additive genetic variation associated with this effect. Females from 21 different genetic backgrounds were housed with males from one of two distinct genetic backgrounds for either a short (3 hr) or long (48 hr) exposure period and their subsequent mate choice behaviors were scored. We found that the genetic identity of a previous mate significantly influenced a female's subsequent interest in males and preference of males. Additionally, a hemiclonal analysis revealed significant additive genetic variation associated with experience‐dependent mate choice behaviors, indicating a genotype‐by‐environment interaction for both of these parameters. We discuss the significance of these results with regard to the evolution of plasticity in female mate choice behaviors and the maintenance of variation in harmful male traits.     

Increased opportunity for sexual conflict promotes harmful males with elevated courtship frequencies

Mating systems have a profound influence on the probability of conflict occurring between the sexes. Promiscuity is predicted to generate sexual conflict, thereby driving the evolution of male traits that harm females, whereas monogamy is expected to foster reproductive cooperation, thus rendering such traits redundant. We tested these predictions using experimentally evolved Drosophila pseudoobscura subject to different mating systems. Female survival was not influenced by the mating system treatment of her partner. However, females continuously housed with males evolving under elevated opportunities for female promiscuity produced fewer total progeny, but a relatively greater number of progeny early in their lives, than females housed with males evolving under obligate monogamy. We also found that promiscuous males courted females more frequently than monogamous males. Variation in male courtship frequency and progeny production patterns among treatments reinforces the critical importance of mating system variation for sexual conflict, during both pre‐ and post‐copulatory interactions.     

Parental sex discrimination and intralocus sexual conflict

Intralocus sexual conflict occurs when populations segregate for alleles with opposing fitness consequences in the two sexes. This form of selection is known to be capable of maintaining genetic and fitness variation in nature, the extent of which is sensitive to the underlying genetics. We present a one-locus model of a haploid maternal effect that has sexually antagonistic consequences for offspring. The evolutionary dynamics of these maternal effects are distinct from those of haploid direct effects under sexual antagonism because the relevant genes are expressed only in females. Despite this, we find the same opportunity for sexually antagonistic polymorphism at the maternal effect locus as at a direct effect locus. Thus, sexually antagonistic maternal effects may underlie some natural genetic variation. The model we present permits alternative interpretations of how the genes are expressed and how the fitness variation is assigned, which invites a theoretical comparison to models of both imprinted genes and sex allocation.     

Predicting the evolution of sexual size dimorphism

11 , Evolution 34 : 292–305) equations for predicting the evolution of sexual size dimorphism (SSD) through frequency‐dependent sexual selection, and frequency‐independent natural selection, were tested against results obtained from a stochastic genetic simulation model. The SSD evolved faster than predicted, due to temporary increases in the genetic variance brought about by directional selection. Predictions for the magnitude of SSD at equilibrium were very accurate for weak sexual selection. With stronger sexual selection the total response was greater than predicted. Large changes in SSD can occur without significant long‐term change in the genetic correlation between the sexes. Our results suggest that genetic correlations constrain both the short‐term and long‐term evolution of SSD less than predicted by the Lande model.     

Intralocus sexual conflict over human height

Intralocus sexual conflict (IASC) occurs when a trait under selection in one sex constrains the other sex from achieving its sex-specific fitness optimum. Selection pressures on body size often differ between the sexes across many species, including humans: among men individuals of average height enjoy the highest reproductive success, while shorter women have the highest reproductive success. Given its high heritability, IASC over human height is likely. Using data from sibling pairs from the Wisconsin Longitudinal Study, we present evidence for IASC over height: in shorter sibling pairs (relatively) more reproductive success (number of children) was obtained through the sister than through the brother of the sibling pair. By contrast, in average height sibling pairs most reproductive success was obtained through the brother relative to the sister. In conclusion, we show that IASC over a heritable, sexually dimorphic physical trait (human height) affects Darwinian fitness in a contemporary human population.     

The evolution from females to hermaphrodites results in a sexual conflict over mating in androdioecious nematode worms and clam shrimp

The nematode worm Caenorhabditis elegans and the clam shrimp Eulimnadia texana are two well‐studied androdioecious species consisting mostly of self‐fertilizing hermaphrodites and few males. To understand how androdioecy can evolve, a simple two‐step mathematical model of the evolutionary pathway from a male–female species to a selfing‐hermaphrodite species is constructed. First, the frequency of mutant females capable of facultative self‐fertilization increases if the benefits of reproductive assurance exceed the cost. Second, hermaphrodites become obligate self‐fertilizers if the fitness of selfed offspring exceeds one‐half the fitness of outcrossed offspring. Genetic considerations specific to C. elegans and E. texana show that males may endure as descendants of the ancestral male–female species. These models combined with an extensive literature review suggest a sexual conflict over mating in these androdioecious species: selection favours hermaphrodites that self and males that outcross. The strength of selection on hermaphrodites and males differs, however. Males that fail to outcross suffer a genetic death. Hermaphrodites may never encounter a rare male, and those that do and outcross only bear less fecund offspring. This asymmetric sexual conflict results in an evolutionary stand‐off: rare, but persistent males occasionally fertilize common, but reluctant hermaphrodites. A consequence of this stand‐off may be an increase in the longevity of the androdioecious mating system.     

Interspecific allometry for sexual shape dimorphism: Macroevolution of multivariate sexual phenotypes with application to Rensch's rule

Allometric trends in the degree of sexual dimorphism with body size have long fascinated evolutionary biologists. Many male-biased clades display more prominent sexual dimorphism in larger taxa (Rensch's rule), with most examples documenting this pattern for body size dimorphism. Although sexual dimorphism in traits other than body size is equally functionally relevant, characterizing allometric patterns of sexual dimorphism in such traits is hampered by lack of an analytical framework that can accommodate multivariate phenotypes. In this article, we derive a multivariate equivalency for investigating trends in sexual dimorphism—relative to overall body size—across taxa and provide a generalized test to determine whether such allometric patterns correspond with Rensch's rule. For univariate linear traits such as body size, our approach yields equivalent results to those from standard procedures, but our test is also capable of detecting trends in multivariate datasets such as shape. Computer simulations reveal that the method displays appropriate statistical properties, and an empirical example in Mediterranean lizards provides the first demonstration of Rensch's rule in a multivariate phenotype (head shape). Our generalized procedure substantially extends the analytical toolkit for investigating macroevolutionary patterns of sexual dimorphism and seeking a better understanding of the processes that underlie them.     

Gene duplication in the evolution of sexual dimorphism

Males and females share most of the same genes, so selection in one sex will typically produce a correlated response in the other sex. Yet, the sexes have evolved to differ in a multitude of behavioral, morphological, and physiological traits. How did this sexual dimorphism evolve despite the presence of a common underlying genome? We investigated the potential role of gene duplication in the evolution of sexual dimorphism. Because duplication events provide extra genetic material, the sexes each might use this redundancy to facilitate sex‐specific gene expression, permitting the evolution of dimorphism. We investigated this hypothesis at the genome‐wide level in Drosophila melanogaster, using the presence of sex‐biased expression as a proxy for the sex‐specific specialization of gene function. We expected that if sexually antagonistic selection is a potent force acting upon individual genes, duplication will result in paralog families whose members differ in sex‐biased expression. Gene members of the same duplicate family can have different expression patterns in males versus females. In particular, duplicate pairs containing a male‐biased gene are found more frequently than expected, in agreement with previous studies. Furthermore, when the singleton ortholog is unbiased, duplication appears to allow one of the paralog copies to acquire male‐biased expression. Conversely, female‐biased expression is not common among duplicates; fewer duplicate genes are expressed in the female‐soma and ovaries than in the male‐soma and testes. Expression divergence exists more in older than in younger duplicates pairs, but expression divergence does not correlate with protein sequence divergence. Finally, genomic proximity may have an effect on whether paralogs differ in sex‐biased expression. We conclude that the data are consistent with a role of gene duplication in fostering male‐biased, but not female‐biased, gene expression, thereby aiding the evolution of sexual dimorphism.     

Inter-genomic sexual conflict drives antagonistic coevolution in harvester ants

The reproductive interests of males and females are not always aligned, leading to sexual conflict over parental investment, rate of reproduction and mate choice. Traits that increase the genetic interests of one sex often occur at the expense of the other, selecting for counter-adaptations leading to antagonistic coevolution. Reproductive conflict is not limited to intraspecific interactions; interspecific hybridization can produce pronounced sexual conflict between males and females of different species, but it is unclear whether such conflict can drive sexually antagonistic coevolution between reproductively isolated genomes. We tested for hybridization-driven sexually antagonistic adaptations in queens and males of the socially hybridogenetic ‘J’ lineages of Pogonomyrmex harvester ants, whose mating system promotes hybridization in queens but selects against it in males. We conducted no-choice mating assays to compare patterns of mating behaviour and sperm transfer between inter- and intra-lineage pairings. There was no evidence for mate discrimination on the basis of pair type, and the total quantity of sperm transferred did not differ between intra- and inter-lineage pairs; however, further dissection of the sperm transfer process into distinct mechanistic components revealed significant, and opposing, cryptic manipulation of copulatory investment by both sexes. Males of both lineages increased their rate of sperm transfer to high-fitness intra-lineage mates, with a stronger response in the rarer lineage for whom mating mistakes are the most likely. By contrast, the total duration of copulation for intra-lineage mating pairs was significantly shorter than for inter-lineage crosses, suggesting that queens respond to prevent excessive sperm loading by prematurely terminating copulation. These findings demonstrate that sexual conflict can lead to antagonistic coevolution in both intra-genomic and inter-genomic contexts. Indeed, the resolution of sexual conflict may be a key determinant of the long-term evolutionary potential of host-dependent reproductive strategies, counteracting the inherent instabilities arising from such systems.