Male harassment drives females to alter habitat use and leads to segregation of the sexes

Sexual conflict is ubiquitous across taxa. It often results in male harassment of females for mating opportunities that are costly for females, in some cases reducing reproductive success and increasing mortality. One strategy that females may employ to avoid sexual harassment is to segregate spatially from males. In fact, we do find sexual segregation in habitat use in species that have high levels of sexual conflict; however, the role of sexual harassment in driving such segregation remains poorly understood. Here, we demonstrate experimentally in a population of wild Trinidadian guppies Poecilia reticulata that male sexual harassment drives females into habitats that they otherwise do not prefer to occupy. In support of the social factors hypothesis for sexual segregation, which states that social factors such as harassment drive sexual segregation, this female behaviour leads to segregation of the sexes. In the presence of males, females actively select areas of high predation risk, but low male presence, and thus trade off increased predation risk against reduced sexual harassment.     

Male sexual harassment alters female social behaviour towards other females

Male harassment of females to gain mating opportunities is a consequence of an evolutionary conflict of interest between the sexes over reproduction and is common among sexually reproducing species. Male Trinidadian guppies Poecilia reticulata spend a large proportion of their time harassing females for copulations and their presence in female social groups has been shown to disrupt female-female social networks and the propensity for females to develop social recognition based on familiarity. In this study, we investigate the behavioural mechanisms that may lead to this disruption of female sociality. Using two experiments, we test the hypothesis that male presence will directly affect social behaviours expressed by females towards other females in the population. In experiment one, we tested for an effect of male presence on female shoaling behaviour and found that, in the presence of a free-swimming male guppy, females spent shorter amounts of time with other females than when in the presence of a free-swimming female guppy. In experiment two, we tested for an effect of male presence on the incidence of aggressive behaviour among female guppies. When males were present in a shoal, females exhibited increased levels of overall aggression towards other females compared with female only shoals. Our work provides direct evidence that the presence of sexually harassing males alters female-female social behaviour, an effect that we expect will be recurrent across taxonomic groups.     

Social preferences based on sexual attractiveness: a female strategy to reduce male sexual attention

Male sexual harassment of females is common across sexually reproducing species and can result in fitness costs to females. We hypothesized that females can reduce unwanted male attention by constructing a social niche where their female associates are more sexually attractive than themselves, thus influencing the decision-making of males to their advantage. We tested this hypothesis in the Trinidadian guppy (Poecilia reticulata), a species with high levels of male sexual harassment. First, we confirmed that non-receptive females were harassed less when they were paired with a more sexually attractive (receptive) female than with another non-receptive female. We then found that, indeed, females exploit this as a strategy to reduce sexual harassment; non-receptive females actively preferred to associate with receptive over non-receptive females. Importantly, when given access only to chemosensory cues, non-receptive females still showed this preference, suggesting that they use information from chemical cues to assess the sexual attractiveness of potential female partners. Receptive females in contrast showed no such preferences. Our results demonstrate that females can decrease male harassment by associating with females that are more sexually attractive than themselves and that they perform active partner choices based on this relative attractiveness. We propose that this strategy is likely to represent an important pathway by which females can construct social niches that influence the decision-making of others to their advantage; in this case, to reduce the sexual harassment they experience.     

Female and male genetic contributions to post-mating immune defence in female Drosophila melanogaster

Post-mating reduction in immune defence is common in female insects, and a trade-off between mating and immunity could affect the evolution of immunity. In this work, we tested the capacity of virgin and mated female Drosophila melanogaster to defend against infection by four bacterial pathogens. We found that female D. melanogaster suffer post-mating immunosuppression in a pathogen-dependent manner. The effect of mating was seen after infection with two bacterial pathogens (Providencia rettgeri and Providencia alcalifaciens), though not after infection with two other bacteria (Enterococcus faecalis and Pseudomonas aeruginosa). We then asked whether the evolution of post-mating immunosuppression is primarily a ‘female’ or ‘male’ trait by assaying for genetic variation among females for the degree of post-mating immune suppression they experience and among males for the level of post-mating immunosuppression they elicit in their mates. We also assayed for an interaction between male and female genotypes to test the specific hypothesis that the evolution of a trade-off between mating and immune defence in females might be being driven by sexual conflict. We found that females, but not males, harbour significant genetic variation for post-mating immunosuppression, and we did not detect an interaction between female and male genotypes. We thus conclude that post-mating immune depression is predominantly a ‘female’ trait, and find no evidence that it is evolving under sexual conflict.     

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.     

Sexual interference in the Golden snub-nosed monkey (Rhinopithecus roxellana): a test of the sexual competition hypothesis in a polygynous species

Sexual interference (SI), which is defined as any disturbance directed to a mating pair by other individuals, has been reported in several primate species. It is widely suggested that successful harassers experience improved mating success by increasing their access to reproductive partners as well as by reducing the mating success of rivals. Although theories of primate sexual conflict highlight male intra-sexual mating competition, females also are reported to actively disrupt copulations between mating partners. In this study, we investigated SI in a multilevel troop of Golden snub-nosed monkeys (Rhinopithecus roxellana) inhabiting the Qinling Mountains, China. Behavioral observations of 11 one-male units (OMU) that comprised the multilevel troop were conducted from September 2007 to May 2008. During this period 17.1% of 652 documented intra-OMU sexual encounters were characterized either by mild or aggressive forms of harassment. Sexual harassment was typically performed by a single individual (91.9%), and in 75.7% of cases the harasser was an adult or sub-adult female. The frequency of female harassment was positively correlated with the number of adult and sub-adult females residing in an OMU, and resulted in a significant decrease in matings ending in ejaculation. We found that the amount of SI a female received was not a significant predictor of her reproductive success. However, females who conceived during the mating season directed higher levels of harassment at other females than females who did not conceive. We evaluate the strength of the sexual competition hypothesis and the hormonally modulated aggression hypothesis in explaining patterns of SI in female Golden snub-nosed monkeys.     

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.     

Polyandry: the history of a revolution

We give a historic overview and critical perspective of polyandry in the context of sexual selection. Early approaches tended to obfuscate the fact that the total matings (copulations) by the two sexes is equal, neglecting female interests and that females often mate with (or receive ejaculates from) more than one male (polyandry). In recent years, we have gained much more insight into adaptive reasons for polyandry, particularly from the female perspective. However, costs and benefits of multiple mating are unlikely to be equal for males and females. These must be assessed for each partner at each potential mating between male i and female j, and will often be highly asymmetric. Interests of i and j may be in conflict, with (typically, ultimately because of primordial sex differences) i benefitting and j losing from mating, although theoretically the reverse can also obtain. Polyandry reduces the sex difference in Bateman gradients, and the probability of sexual conflict over mating by: (i) reducing the potential expected value of each mating to males in inverse proportion to the number of mates per female per clutch, and also often by (ii) increasing ejaculate costs through increased sperm allocation. It can nevertheless create conflict over fertilization and increase conflict over parental investment. The observed mean mating frequency for the population (and hence the degree of polyandry) is likely, at least in part, to reflect a resolution of sexual conflict. Immense diversity exists across and within taxa in the extent of polyandry, and views on its significance have changed radically, as we illustrate using avian polyandry as a case study. Despite recent criticisms, the contribution of the early pioneers of sexual selection, Darwin and Bateman, remains generally valid, and should not, therefore, be negated; as with much in science, pioneering advances are more often amplified and refined, rather than replaced with entirely new paradigms.     

Sex-specific chemical cues from immatures facilitate the evolution of mate guarding in Heliconius butterflies

Competition for mates has substantial effects on sensory systems and often leads to the evolution of extraordinary mating behaviours in nature. The ability of males to find sexually immature females and associate with them until mating is a remarkable example. Although several aspects of such pre-copulatory mate guarding have been investigated, little is known about the mechanisms used by males to locate immature females and assess their maturity. These are not only key components of the origin and maintenance of this mating strategy, but are also necessary for inferring the level to which females cooperate and thus the incidence of sexual conflict. We investigated the cues involved in recognition of immature females in Heliconius charithonia, a butterfly that exhibits mate guarding by perching on pupae. We found that males recognized female pupae using sex-specific volatile monoterpenes produced by them towards the end of pupal development. Considering the presumed biosynthetic pathways of such compounds and the reproductive biology of Heliconius, we propose that these monoterpenes are coevolved signals and not just sex-specific cues exploited by males. Their maintenance, despite lack of female mate choice, may be explained by variation in cost that females pay with this male behaviour under heterogeneous ecological conditions.     

A model of sexual selection and female use of refuge in a coercive mating system

In many non-monogamous systems, males invest less in progeny than do females. This leaves males with higher potential rates of reproduction, and a likelihood of sexual conflict, including, in some systems, coercive matings. If coercive matings are costly, the best female strategy may be to avoid male interaction. We present a model that demonstrates female movement in response to male harassment as a mechanism to lower the costs associated with male coercion, and the effect that female movement has on selection in males for male harassment. We found that, when females can move from a habitat patch to a refuge to which males do not have access, there may be a selection for either high, or low harassment male phenotype, or both, depending on the relationship between the harassment level of male types in the population and a threshold level of male harassment. This threshold harassment level depends on the relative number of males and females in the population, and the relative resource values of the habitat; the threshold increases as the sex ratio favours females, and decreases with the value of the refuge patch or total population. Our model predicts that selection will favour the harassment level that lies closest to this threshold level of harassment, and differing harassment levels will coexist within the population only if they lie on the opposite sides of the threshold harassment. Our model is consistent with empirical results suggesting that an intermediate harassment level provides maximum reproductive fitness to males when females are mobile.     

Fitness consequences of divorce in the azure-winged magpie depends on the breeding experience of a new mate

Sexual conflict in producing and raising offspring is a critical issue in evolutionary ecology research.Individual experience affects their breeding performance,as measured by such traits of provisioning of offspring and engagement in extra-pair copulations,and may cause an imbalance in sexual conflict.Thus,divorce is hypothesized to occur within aged social pairs,irrespective of current reproductive success.This concept was explored in the azure-winged magpie Cyanopica cyanus by investigating the divorce of a social pair and its relationship to their changes in breeding performance with prior experience.Females engaging in extra-pair copulation may intensify sexual conflicts and may be the main reason for divorce.Once divorced,females repairing with an inexperienced male realized higher reproductive success than that repairing with an experienced male;males repairing with an experienced female realized higher reproductive success than that repairing with an inexperienced female.This finding indicates that the fitness consequence of divorce depends on the breeding experience of new mates.Divorced females can obtain more extra-pair copulations,whereas divorced males cannot,when they repair with inexperienced breeders.Divorced females provisioned a brood at lower rates than inexperienced females whereas divorced males had no such difference.It appears that divorced females can obtain an advantage in sexual conflicts with inexperienced mates in future reproduction.Consequently,females are probably more active than males in divorcing their aged mates so as to select an inexperienced male as a new mate.Azure-winged magpies thus provide novel insights into the implicaticns of sexual conflict in birds.     

Convenience polyandry or convenience polygyny? Costly sex under female control in a promiscuous primate

Classic sex roles depict females as choosy, but polyandry is widespread. Empirical attempts to understand the evolution of polyandry have often focused on its adaptive value to females, whereas 'convenience polyandry' might simply decrease the costs of sexual harassment. We tested whether constraint-free female strategies favour promiscuity over mating selectivity through an original experimental design. We investigated variation in mating behaviour in response to a reversible alteration of sexual dimorphism in body mass in the grey mouse lemur, a small primate where female brief sexual receptivity allows quantifying polyandry. We manipulated body condition in captive females, predicting that convenience polyandry would increase when females are weaker than males, thus less likely to resist their solicitations. Our results rather support the alternative hypothesis of 'adaptive polyandry': females in better condition are more polyandrous. Furthermore, we reveal that multiple mating incurs significant energetic costs, which are strikingly symmetrical between the sexes. Our study shows that mouse lemur females exert tight control over mating and actively seek multiple mates. The benefits of remating are nevertheless not offset by its costs in low-condition females, suggesting that polyandry is a flexible strategy yielding moderate fitness benefits in this small mammal.     

Field crickets change mating preferences using remembered social information

Plasticity in female mate choice can fundamentally alter selection on male ornaments, but surprisingly few studies have examined the role of social learning in shaping female mating decisions in invertebrates. We used the field cricket Teleogryllus oceanicus to show that females retain information about the attractiveness of available males based on previous social experience, compare that information with incoming signals and then dramatically reverse their preferences to produce final, predictable, mating decisions. Male ornament evolution in the wild may depend much more on the social environment and behavioural flexibility through learning than was previously thought for non-social invertebrates. The predictive power of these results points to a pressing need for theoretical models of sexual selection that incorporate effects of social experience.     

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.     

Why are female color polymorphisms rare in territorial damselflies?

In nonterritorial damselflies, females often come in multiple color morphs, perhaps because females with rare colors experience reduced sexual harassment, and thus have a frequency‐dependent fitness advantage, compared to females of the most common color morph, but such polymorphisms are rare in territorial species. We consider three hypotheses to explain the rarity of female color polymorphisms in territorial species: (a) misdirected male aggression, (b) poor male mate recognition, and (c) low mating harassment rates. The first hypothesis has some empirical support, and can account for the absence of andromorphs (i.e., females that resemble males), but does not explain the absence of multiple heteromorphs. We tested the second hypothesis by presenting females of two novel color morphs (green‐ or red‐banded abdomens) to territorial male Hetaerina capitalis. Females of both novel color morphs elicited fewer sexual responses than control females, and the red morph occasionally elicited aggressive responses. These results indicate that novel female color morphs would experience reduced mating harassment in this species, contradicting the hypothesis that male mate recognition is too poorly developed to reduce harassment of novel female morphs. By process of elimination, the third hypothesis, that harassment rates are too low in territorial species to provide rare female morphs a fitness advantage, is favored, but remains untested. Our findings also suggest that the common practice of color‐marking odonates for behavioral research is likely to interfere with mate choice, as has long been known to be the case in birds.     

Acoustic experience shapes female mate choice in field crickets

Female choice can drive the evolution of extravagant male traits. In invertebrates, the influence of prior social experience on female choice has only recently been considered. To better understand the evolutionary implications of experience-mediated plasticity in female choice, we investigated the effect of acoustic experience during rearing on female responsiveness to male song in the field cricket Teleogryllus oceanicus. Acoustic experience has unique biological relevance in this species: a morphological mutation has rendered over 90 per cent of males on the Hawaiian island of Kauai silent in fewer than 20 generations, impeding females' abilities to locate potential mates. Females reared in silent conditions mimicking Kauai were less discriminating of male calling song and more responsive to playbacks, compared with females that experienced song during rearing. Our results to our knowledge, are the first demonstration of long-term effects of acoustic experience in an arthropod, and suggest that female T. oceanicus may be able to compensate for the reduced availability of long-range male sexual signals by increasing their responsiveness to the few remaining signallers. Understanding the adaptive significance of experience-mediated plasticity in female choice provides insight into processes that facilitate rapid evolutionary change and shape sexual selection pressure in natural populations.     

Temperature drives pre‐reproductive selection and shapes the biogeography of a female polymorphism

Conflicts of interests between males and females over reproduction is a universal feature of sexually reproducing organisms and has driven the evolution of intersexual mimicry, mating behaviours and reproductive polymorphisms. Here, we show how temperature drives pre‐reproductive selection in a female colour polymorphic insect that is subject to strong sexual conflict. These species have three female colour morphs, one of which is a male mimic. This polymorphism is maintained by frequency‐dependent sexual conflict caused by male mating harassment. The frequency of female morphs varies geographically, with higher frequency of the male mimic at higher latitudes. We show that differential temperature sensitivity of the female morphs and faster sexual maturation of the male mimic increases the frequency of this morph in the north. These results suggest that sexual conflict during the adult stage is shaped by abiotic factors and frequency‐independent pre‐reproductive selection that operate earlier during ontogeny of these female morphs.     

Using video playback to study the effect of an audience on male mating behavior in the Sailfin molly (Poecilia latipinna)

Sexual conflict in poeciliid fishes is well-documented, particularly male sexual harassment and its effects on females. For instance, male attempts to force copulations influence female feeding, energy allocation, and preference for shoaling partners. However, there has been little research conducted to determine how the social environment shapes the occurrence and intensity of sexual harassment. In this study we ask whether an audience male influences the sexual behaviors of a focal male, the correlated feeding time reduction of female Poecilia latipinna, and if the size of the audience male (larger or smaller than the focal male) influences these behaviors. We presented a video of a male, either smaller or larger than the focal male, or an empty tank (control) to a female interacting with a male or female partner and measured feeding times and sexual behaviors. We found that male sexual behaviors increased in the presence of an audience male, especially if the audience male was larger than the focal male. Females fed more in the presence of a partner female than in the presence of a male, which was independent of the audience (i.e., video treatment). Focal female aggression towards the partner female increased with the size of the audience male. The present study shows that an audience male has multiple interacting influences on both male and female behavior.     

Kin selection and the evolution of sexual conflict

Males and females do not always share the same evolutionary interests. This is particularly true in the case of multiple mating, where male–male competition can often lead to adaptations that are harmful to the female, and females can evolve counter adaptations to reduce the benefits males gain from such traits. Although social evolution has made substantial progress from kin selection theory, most studies of sexual conflict have ignored the effects of genetic relatedness. Here, I use a model of male harm and female resistance to investigate how kin selection affects the evolution of sexual conflict. Building on models of social evolution, I show that relatedness inhibits sexual conflict, in terms of male harm, whereas it has no effect on the evolution female resistance. This study examines a previously neglected mechanism that can potentially help to resolve sexual conflict over mating and highlights the potential importance of considering relatedness in empirical studies of 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.