Receptive females mitigate costs of sexual conflict

Males typically gain fitness from multiple mating, whereas females often lose fitness from numerous mating, potentially leading to sexual conflict over mating. This conflict is expected to favour the evolution of female resistance to mating. However, females may incur male harassment if they refuse to copulate; thus, greater female resistance may increase costs imposed by males. Here, I show that the evolution of resistance to mating raises fitness disadvantages of interacting with males when mating is harmful in female adzuki bean beetles, Callosobruchus chinensis. Females that were artificially selected for higher and lower remating propensity evolved to accept and resist remating, respectively. Compared with females that evolved to accept remating, females that evolved to resist it suffered higher fitness costs from continuous exposure to males. The costs of a single mating measured by the effect on longevity did not differ among selection line females. This study indicates that receptive rather than resistant females mitigate the fitness loss resulting from sexual conflict, suggesting that even though mating is harmful, females can evolve to accept additional mating.     

Female resistance to sexual coercion can evolve to preserve the indirect benefits of mate choice

Sexual conflict over the indirect benefits of mate choice may arise when traits in one sex limit the ability of the other sex to freely choose mates but when these coercive traits are not necessarily directly harmful (i.e. forced fertilization per se). Although we might hypothesize that females can evolve resistance in order to retain the indirect, genetic benefits (reflected in offspring attractiveness) of mating with attractive males, up to now it has been difficult to evaluate potential underlying mechanisms. Traditional theoretical approaches do not usually conceptually distinguish between female preference for male mating display and female resistance to forced fertilization, yet sexual conflict over indirect benefits implies the simultaneous action of all of these traits. Here, we present an integrative theoretical framework that draws together concepts from both sexual selection and sexual conflict traditions, allowing for the simultaneous coevolution of displays and preferences, and of coercion and resistance. We demonstrate that it is possible for resistance to coercion to evolve in the absence of direct costs of mating to preserve the indirect benefits of mate choice. We find that resistance traits that improve the efficacy of female mating preference can evolve as long as females are able to attain some indirect benefits of mating with attractive males, even when both attractive and unattractive males can coerce. These results reveal new evolutionary outcomes that were not predicted by prior theories of indirect benefits or sexual conflict.     

Sexual conflict and the tragedy of the commons

It is widely understood that the costs and benefits of mating can affect the fecundity and survival of individuals. Sexual conflict may have profound consequences for populations as a result of the negative effects it causes males and females to have on one another's fitness. Here we present a model describing the evolution of sexual conflict, in which males inflict a direct cost on female fitness. We show that these costs can drive the entire population to extinction. To males, females are an essential but finite resource over which they have to compete. Population extinction owing to sexual conflict can therefore be seen as an evolutionary tragedy of the commons. Our model shows that a positive feedback between harassment and the operational sex ratio is responsible for the demise of females and, thus, for population extinction. We further show that the evolution of female resistance to counter harassment can prevent a tragedy of the commons. Our findings not only demonstrate that sexual conflict can drive a population to extinction but also highlight how simple mechanisms, such as harassment costs to males and females and the coevolution between harassment and resistance, can help avert a tragedy of the commons caused by sexual conflict.     

Lifetime Number of Mates Interacts with Female Age to Determine Reproductive Success in Female Guppies

In many species, mating with multiple males confers benefits to females, but these benefits may be offset by the direct and indirect costs associated with elevated mating frequency. Although mating frequency (number of mating events) is often positively associated with the degree of multiple mating (actual number of males mated), most studies have experimentally separated these effects when exploring their implications for female fitness. In this paper I describe an alternative approach using the guppy Poecilia reticulata, a livebearing freshwater fish in which females benefit directly and indirectly from mating with multiple males via consensual matings but incur direct and indirect costs of mating as a consequence of male sexual harassment. In the present study, females were experimentally assigned different numbers of mates throughout their lives in order to explore how elevated mating frequency and multiple mating combine to influence lifetime reproductive success (LRS) and survival (i.e. direct components of female fitness). Under this mating design, survival and LRS were not significantly affected by mating treatment, but there was a significant interaction between brood size and reproductive cycle (a correlate of female age) because females assigned to the high mating treatment produced significantly fewer offspring later in life compared to their low-mating counterparts. This negative effect of mating treatment later in life may be important in these relatively long-lived fishes, and this effect may be further exacerbated by the known cross-generational fitness costs of sexual harassment in guppies.     

The effect of mating on starvation resistance in natural populations of Drosophila melanogaster

In nature, behavioural and physiological processes involved in mating may entail different costs and benefits for males and females. However, it has been hypothesized that sexual interactions may have additional costs for Drosophila females like decrease in receptivity to remating and shortening of lifespan. During mating, males transfer seminal fluid proteins to females that exert severe physiological changes that may compromise female’s lifespan and reproductive success. However, under specific stressful environmental conditions that organisms usually face in nature, mating may also confer benefits to females. In the present work, we examine the effect of mating on starvation resistance in wild Drosophila melanogaster. We demonstrate that mated females derived from different geographic locations have the benefit of a greater starvation resistance as compared to virgin females. Even though mating status did not affect mean starvation resistance, we detected a strong genotype-specific effect in males. Beyond the obvious advantage of mating, our study reveals that mating might not be perilous for females, as envisaged by sexual conflict theories, but advantageous for flies exposed to shifts in environmental conditions. Thus, our results highlight the importance of studying other ecologically relevant traits that may contribute to the evolution of male–female interactions.     

Mate sampling and the sexual conflict over mating in seaweed flies

The order in which females encounter, or sample, males in apopulation may have important consequences for mate choice,with the information gathered about males influencing boththe preference function and degree of choosiness of females.Sexual selection may be affected as a result. Sampling of particularsubsets of males may be a crucial component of individual variation in mate preferences within populations. However, the sequencein which males are sampled may also be important in specieswithout traditional, active mate choice, such as when sexualselection involves sexual conflict over mating. This wouldoccur if the likelihood of a female mating with a male of acertain phenotype changes as a result of previous encounters.We examined the effects of encountering males differing inbody size, a sexually selected phenotype, in the seaweed flyCoelopa frigida. Sexual selection occurs in this species asa result of a sexual conflict over mating. We show that theoutcome of the sexual conflict is independent of the orderin which males are encountered by female seaweed flies, withthe overall mating advantage to large males being unaffected.In addition, we explored female preference functions and evaluatethe heterogeneity in female willingness to mate. We suggestthat consideration of mate sampling theory is valuable whenexamining mate choice in species in which sexual selectionis driven by sexual conflict.     

The evolution of female mate choice by sexual conflict

Although empirical evidence has shown that many male traits have evolved via sexual selection by female mate choice, our understanding of the adaptive value of female mating preferences is still very incomplete. It has recently been suggested that female mate choice may result from females evolving resistance rather than attraction to males, but this has been disputed. Here, we develop a quantitative genetic model showing that sexual conflict over mating indeed results in the joint evolution of costly female mate choice and exaggerated male traits under a wide range of circumstances. In contrast to tradition explanations of costly female mate choice, which rely on indirect genetic benefits, our model shows that mate choice can be generated as a side-effect of females evolving to reduce the direct costs of mating.     

Polyandry in Bicyclus anynana Butterflies Results from Sexual Conflict over Mating

Although only one or just a few matings are considered sufficient to maximise a female's reproductive success, polyandry is a common mating system in insects and other animals. Female polyandry may either result from direct or indirect benefits of mating multiply, or from male harassment and thus sexual conflict over mating. Here, we test whether the latter is involved in determining female mating frequency in the butterfly Bicyclus anynana. We used a full‐factorial design with three different sex ratios and densities each, resulting in a total of nine treatment groups. Sex ratio but not density affected female mating frequency, which increased with an increasingly male‐biased sex ratio. Our results thus suggest that female polyandry in B. anynana results from sexual conflict, although females seem to be able to reject courting males at least to some extent. Therefore, polyandry in this species may occur in the first place from convenience, as the costs of resisting male harassment may be higher than mating repeatedly.     

Cross-generational effects of sexual harassment on female fitness in the guppy

Sexual harassment is a common outcome of sexual conflict over mating rate. A large number of studies have identified several direct costs to females of sexual harassment including energy expenditure and reduced foraging ability. However, the fitness consequences of sexual harassment for descendants have rarely been investigated. Here, we manipulated the level of sexual harassment and mating rate in two groups of female guppies, Poecilia reticulata, a live-bearing fish in which sexual conflict over mating rate is particularly pronounced. Each female was allowed to interact with three males for one day (low sexual harassment, LSH) or for eight days (high sexual harassment, HSH) during each breeding cycle throughout their life. Female lifetime fecundity did not differ between the groups, but we found a strong effect on offspring fitness. HSH females produced (1) daughters with smaller bodies and (2) sons with shorter gonopodia, which were less attractive to females and less successful in coercive matings than their LSH counterparts. Although these results may be influenced by the indirect effects of sex ratio differences between treatments, they suggest that sexual harassment and elevated mating rate can have negative cross-generational fitness effects and more profound evolutionary consequences than currently thought.     

Sperm‐limited fecundity and polyandry‐induced mortality in female nematodes Caenorhabditis remanei

In many sexually reproducing species, females are sperm limited and actively mate more than once which can lead to sperm competition between males. However, the costs and benefits of multiple matings may differ for males and females leading to different optimal mating frequencies and consequent sexual conflict. Under these circumstances, male traits that reduce females' re‐mating rates are likely to evolve. However, the same traits can also reduce, directly or indirectly, female survival and/or manipulate female fecundity. Evidence of this sexual conflict is common across several taxa. Here, we examine the evidence for this form of conflict in the free‐living nematodes of the Caenorhabditis genus. Members of this group are extensively used to describe developmental and physiological processes. Despite this, we understand little about the evolution of selfing, maintenance of males and sexual conflict in these species, particularly those with gonochoristic mating strategies. In this study, we demonstrate experimentally sexual conflict in the gonochoristic of C. remanei cultured under laboratory conditions. In our first experiment, we found that female fecundity increased with the number of males present which suggests that females' reproduction may be sperm limited. However, increasing the number of males present also reduced female survival. A second experiment ruled out the alternative explanation of density‐dependent reduction in female survival when more males were present as increasing female density correspondingly did not affect female survival. © 2009 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 99 , 362–369.     

Behavioural Consistency in Female Resistance to Male Harassment in a Water Strider Species

Sexual conflict over mating rate often implies that males persist at frequently harassing females to gain matings while females resist mating attempts. In water striders, females can resist by engaging in vigorous pre‐copulatory struggles to dislodge males, but alternative means of resistance have seldom been investigated. Contrary to males, female resistance has not been investigated as a repeatable behaviour. We used Gerris buenoi to investigate the capacity to abbreviate struggles and the tendency to hide off the water as two potential female resistance traits. Specifically, we asked whether these behaviours are repeatable and whether they vary according to sexual conflict intensity and past mating experience. Also, we studied the possible connections between these behaviours and traits linked to fitness, namely endured harassment and mating activity. The capacity to abbreviate struggles was poorly repeatable and decreased with sexual conflict intensity and endured harassment. It seems to be mainly determined by the social environment and by recent events related to sexual conflict. The tendency to hide off the water was significantly repeatable across sexual conflict intensities and can be considered as a repeatable behaviour. Hiding frequently off the water allowed females to decrease the harassment endured by females and may enhance female fitness. In nature, hiding is more readily and more frequently observed than pre‐copulatory struggles. Directly associating hiding off water with female fitness would confirm that this consistent phenotype contributes to sexually antagonistic female resistance.     

Female resistance to male harm evolves in response to manipulation of sexual conflict

The interests of males and females over reproduction rarely coincide and conflicts between the sexes over mate choice, mating frequency, reproductive investment, and parental care are common in many taxa. In Drosophila melanogaster, the optimum mating frequency is higher for males than it is for females. Furthermore, females that mate at high frequencies suffer significant mating costs due to the actions of male seminal fluid proteins. Sexual conflict is predicted to lead to sexually antagonistic coevolution, in which selection for adaptations that benefit males but harm females is balanced by counterselection in females to minimize the extent of male-induced harm. We tested the prediction that elevated sexual conflict should select for increased female resistance to male-induced harm and vice versa. We manipulated the intensity of sexual conflict by experimentally altering adult sex ratio. We created replicated lines of D. melanogaster in which the adult sex ratio was male biased (high conflict lines), equal (intermediate conflict lines), or female biased (low conflict lines). As predicted, females from high sexual conflict lines lived significantly longer in the presence of males than did females from low conflict lines. Our conclusion that the evolutionary response in females was to the level of male-induced harm is supported by the finding that there were no female longevity differences in the absence of males. Differences between males in female harming ability were not detected. This suggests that the response in females was to differences between selection treatments in mating frequency, and not to differences in male harmfulness.     

No Effect of Male Courtship Intensity on Female Remating in the Butterfly <Emphasis Type="Italic">Pieris napi</Emphasis>

In Pieris napi, female fitness increases with number of matings, but wild females mate at an unexpectedly low rate. From a sexual conflict perspective this could be because males manipulate female remating, or alternatively, because wild females experience costs associated with remating which are not applicable under laboratory conditions. To get an indication which sex controls remating and/or the different sexes’ relative costs and benefits of remating, we here test whether female mating frequency is affected by male courtship intensity. We found no effect on female mating frequency or lifespan. This indicates that (i) females control remating and their optimal mating frequency is lower compared to males, or (ii) males can manipulate female remating. We argue that both these alternatives may apply simultaneously to P. napiand that they are inseparable.     

The limits of sexual conflict in the narrow sense: new insights from waterfowl biology

Sexual conflict occurs when the evolutionary interests of the sexes differ and it broadly applies to decisions over mating, fertilization and parental investment. Recently, a narrower view of sexual conflict has emerged in which direct selection on females to avoid male-imposed costs during mating is considered the distinguishing feature of conflict, while indirect selection is considered negligible. In this view, intersexual selection via sensory bias is seen as the most relevant mechanism by which male traits that harm females evolve, with antagonistic coevolution between female preferences and male manipulation following. Under this narrower framework, female preference and resistance have been synonymized because both result in a mating bias, and similarly male display and coercion are not distinguished. Our recent work on genital evolution in waterfowl has highlighted problems with this approach. In waterfowl, preference and resistance are distinct components of female phenotype, and display and coercion are independent male strategies. Female preference for male displays result in mate choice, while forced copulations by unpreferred males result in resistance to prevent these males from achieving matings and fertilizations. Genital elaborations in female waterfowl appear to function in reinforcing female preference to maintain the indirect benefits of choice rather than to reduce the direct costs of coercive mating. We propose a return to a broader view of conflict where indirect selection and intrasexual selection are considered important in the evolution of conflict.     

Sexual conflict over mating and fertilization: an overview

Sexual conflict is a conflict between the evolutionary interests of individuals of the two sexes. The sexes can have different trait optima but this need not imply conflict if their optima can be attained simultaneously. Conflict requires an interaction between males and females (e.g. mating or parental care), such that the optimal outcomes for each sex cannot be achieved simultaneously. It is important to distinguish between battleground models, which define the parameter space for conflict and resolution models, which seek solutions for how conflicts are resolved. Overt behavioural conflict may or may not be manifest at resolution. Following Fisherian principles, an immediate (i.e. direct) benefit to a male that has a direct cost to his female partner can have an indirect benefit to the female via her male progeny. Female resistance to mating has been claimed to represent concurrence rather than conflict, due to female benefits via sons (males with low mating advantage are screened out by resistance). However, the weight of current evidence (both theoretical and empirical) supports sexual conflict for many cases. I review (i) conflicts over mate quality, encounters between males and females of genetically diverged subpopulations, mating rate and inbreeding, (ii) the special features of postcopulatory sexual conflict and (iii) some general features of importance for conflict resolution.     

Why Do Female Callosobruchus maculatus Kick Their Mates?

Sexual conflict is now recognised as an important driver of sexual trait evolution. However, due to their variable outcomes and effects on other fitness components, the detection of sexual conflicts on individual traits can be complicated. This difficulty is exemplified in the beetle Callosobruchus maculatus, where longer matings increase the size of nutritious ejaculates but simultaneously reduce female future receptivity. While previous studies show that females gain direct benefits from extended mating duration, females show conspicuous copulatory kicking behaviour, apparently to dislodge mating males prematurely. We explore the potential for sexual conflict by comparing several fitness components and remating propensity in pairs of full sibling females where each female mated with a male from an unrelated pair of full sibling males. For one female, matings were terminated at the onset of kicking, whereas the other’s matings remained uninterrupted. While fecundity (number of eggs) was similar between treatments, uninterrupted matings enhanced adult offspring numbers and fractionally also longevity. However, females whose matings were interrupted at the onset of kicking exhibited an increased propensity to remate. Since polyandry can benefit female fitness in this species, we argue that kicking, rather than being maladaptive, may indicate that females prefer remating over increased ejaculate size. It may thus be difficult to assess the presence of sexual conflict over contested traits such as mating duration when females face a trade off between direct benefits gained from one mating and indirect benefits from additional matings.     

The evolution of optimal female mating rate changes the coevolutionary dynamics of female resistance and male persistence

Mating decisions usually involve conflict of interests between sexes. Accordingly, males benefit from increased number of matings, whereas costs of mating favour a lower mating rate for females. The resulting sexual conflict underlies the coevolution of male traits that affect male mating success ('persistence') and female traits that affect female mating patterns ('resistance'). Theoretical studies on the coevolutionary dynamics of male persistence and female resistance assumed that costs of mating and, consequently, the optimal female mating rate are evolutionarily constant. Costs of mating, however, are often caused by male 'persistence' traits that determine mating success. Here, we present a model where the magnitude of costs of mating depend on, and evolve with, male persistence. We find that allowing costs of mating to depend on male persistence results in qualitatively different coevolutionary dynamics. Specifically, we find that male traits such as penis spikes that harm females are not predicted to exhibit runaway selection with female resistance, in contrast to previous theory that predicts indefinite escalation. We argue that it is essential to determine when and to what extent costs of mating are caused by male persistence in order to understand and accurately predict coevolutionary dynamics of traits involved in mating decisions.     

Sexual conflict and cooperation under naturally occurring male enforced monogamy

An evolutionary conflict often exists between the sexes in regard to female mating patterns. Females can benefit from polyandry, whereas males mating with polyandrous females lose reproductive opportunities because of sperm competition. Where this conflict occurs, the evolution of mechanisms whereby males can control female remating, often at a fitness cost to the female, are expected to evolve. The fitness cost to the female will be increased in systems where a few high status males monopolise mating opportunities and thus have limited sperm supplies. Here we show that in the cockroach Nauphoeta cinerea, a species where males enforce female monogamy in the first reproductive cycle, males that have become sperm depleted continue to be able to manipulate female remating behaviour. Although the manipulation severely decreases fecundity in females mated to sperm-depleted males, males benefit, increasing their relative fitness by preventing other males from reproducing. Our results suggest that there is selection on maintaining the mechanism of manipulation rather than maintaining sperm numbers. Taken with previous research on sexual conflict in N. cinerea, this study suggests that the causes and consequences of sexual conflict are complex and can change across the life history of an individual.     

Sexual conflict over mating in Gnatocerus cornutus? Females prefer lovers not fighters

Female mate choice and male–male competition are the typical mechanisms of sexual selection. However, these two mechanisms do not always favour the same males. Furthermore, it has recently become clear that female choice can sometimes benefit males that reduce female fitness. So whether male–male competition and female choice favour the same or different males, and whether or not females benefit from mate choice, remain open questions. In the horned beetle, Gnatocerus cornutus, males have enlarged mandibles used to fight rivals, and larger mandibles provide a mating advantage when there is direct male–male competition for mates. However, it is not clear whether females prefer these highly competitive males. Here, we show that female choice targets male courtship rather than mandible size, and these two characters are not phenotypically or genetically correlated. Mating with attractive, highly courting males provided indirect benefits to females but only via the heritability of male attractiveness. However, mating with attractive males avoids the indirect costs to daughters that are generated by mating with competitive males. Our results suggest that male–male competition may constrain female mate choice, possibly reducing female fitness and generating sexual conflict over mating.     

Immune system activation affects male sexual signal and reproductive potential in crickets

Parasite-mediated sexual selection theory posits that individuals(usually females) choose mates by assessing the expression ofcostly secondary sexual signals, which provide reliable indicationsof parasite resistance. If these signals are indeed reliable,then immune-compromised males are predicted to exhibit changesin the sexual signal that are discernable by the female. Moreover,the mating pair is predicted to exhibit some reduction in reproductivefitness if the male is immune compromised. Here, we addressedthese predictions in the ground cricket, Allonemobius socius,by injecting juvenile males with lipopolysaccarides, which allowedus to activate the immune system without the introduction ofa metabolically active pathogen. As a consequence, we were ableto disentangle the cost of immune system activation from thecost of infection. We found that immune activation had a long-termeffect on male calling song and the males' ability to providepaternal resources, which can constrain male and female reproductivepotential. We also found that song interpulse interval variedsignificantly with the male's immune treatment and may thereforeprovide choosy females with a way to avoid mating with immune-compromisedmales. In short, our data support the parasite-mediated theoryof sexual selection, suggesting that female's gain direct benefitsby mating with males who are immune competent.