Plasticity of the mate choice mind: courtship evokes choice‐like brain responses in females from a coercive mating system

Female mate choice is fundamental to sexual selection, and determining molecular underpinnings of female preference variation is important for understanding mating character evolution. Previously it was shown that whole‐brain expression of a synaptic plasticity marker, neuroserpin, positively correlates with mating bias in the female choice poeciliid, Xiphophorus nigrensis, when exposed to conspecific courting males, whereas this relationship is reversed in Gambusia affinis, a mate coercive poeciliid with no courting males. Here we explore whether species‐level differences in female behavioral and brain molecular responses represent ‘canalized’ or ‘plastic’ traits. We expose female G. affinis to conspecific males and females, as well as coercive and courting male Poecilia latipinna, for preference assays followed by whole‐brain gene expression analyses of neuroserpin, egr‐1 and early B. We find positive correlations between gene expression and female preference strength during exposure to courting heterospecific males, but a reversed pattern following exposure to coercive heterospecific males. This suggests that the neuromolecular processes associated with female preference behavior are plastic and responsive to different male phenotypes (courting or coercive) rather than a canalized response linked to mating system. Further, we propose that female behavioral plasticity may involve learning because female association patterns shifted with experience. Compared to younger females, we found larger, more experienced females spend less time near coercive males but associate more with males in the presence of courters. We thus suggest a conserved learning‐based neuromolecular process underlying the diversity of female mate preference across the mate choice and coercion‐driven mating systems.     

Sexual harassment in a live-bearing fish (<Emphasis Type="Italic">Poecilia mexicana</Emphasis>): influence of population-specific male mating behaviour

We investigated male sexual behaviour and the cost of sexual harassment, as measured by the reduction of female feeding time in the presence of a male, in a cave-dwelling population of Poecilia mexicana, in which sexual harassment does not occur naturally. We asked whether the lack of sexual harassment in this population is due to low sexual activity of the males, or low feeding motivation of the females. We experimentally increased the sexual activity of males or the females feeding motivation, or we used a combination of both treatments. Female feeding time was not lower in the presence of a male than in the presence of a female after sexual deprivation of the males or food deprivation of the females. Only in the combined experiment was female feeding time lower in the presence of a large male than in the presence of a small male, indicating a weak effect of sexual harassment by large males. Virgin females did not suffer a cost of sexual harassment, indicating that sexual experience does not cause the lack of sexual harassment in cave mollies. Males from a surface population, where sexual harassment occurs, significantly reduced the feeding time of cave-dwelling females even though these males exhibited surprisingly little sexual behaviour. The sexual activity of cave mollies did not correlate with male body size in any experiment, indicating that even after sexual deprivation, small cave molly males do not switch to the alternative mating behaviour known in surface-dwelling P. mexicana, where sexual activity is correlated negatively with male body size.     

Size-dependent male mating behaviour and sexual harassment in a population of Atlantic mollies (Poecilia mexicana) from a sulphur creek

The Atlantic molly Poecilia mexicana inhabits a variety of habitats. In previous studies, small males from clear-water populations showed considerably more sexual behaviours than large males. Males from a sulphur creek, the El Azufre, or from a sulphur cave (cave molly) showed comparatively low sexual activity, and typical size-dependent mating behaviour was either absent or large males showed even more sexual behaviour than smaller ones. Sexually deprived cave molly males increased their sexual activity, but small males still did not show more sexual behaviour than large ones, suggesting that the genetic basis for typical size-dependent mating behaviour has been lost. Likely, the extreme abiotic conditions (hypoxia and toxic hydrogen sulphide) have selected against energetically costly behaviours. In this paper, we examined how El Azufre males would respond to sexual deprivation. We found these males to also increase their sexual activity after sexual deprivation but, unlike cave mollies, small males now showed more sexual behaviour than large ones, suggesting that the genetic basis for this behaviour is not lost in this population. Differences between populations may be due to the less harsh characteristics of El Azufre (e.g. less H₂S), resulting in weaker selection against energy-consuming behaviours. Furthermore, we tested for potential costs of male sexual harassment for females in terms of reduced feeding efficiency in the presence of a male, as was shown for P. mexicana from a clear-water population, but was not found in cave mollies or the El Azufre fish. Test females were either starved for 1 week to increase hunger levels or male sexual deprivation and female starvation were combined; however, we found no evidence for male sexual harassment even after these treatments. Our results parallel previous findings in the cave molly and suggest that El Azufre males have lost specific behavioural traits that cause sexual harassment.     

An experimental test for body size‐dependent effects of male harassment and an elevated copulation rate on female lifetime fecundity and offspring performance

Many studies investigate the benefits of polyandry, but repeated interactions with males can lower female reproductive success. Interacting with males might even decrease offspring performance if it reduces a female's ability to transfer maternal resources. Male presence can be detrimental for females in two ways: by forcing females to mate at a higher rate and through costs associated with resisting male mating attempts. Teasing apart the relative costs of elevated mating rates from those of greater male harassment is critical to understand the evolution of mating strategies. Furthermore, it is important to test whether a male's phenotype, notably body size, has differential effects on female reproductive success versus the performance of offspring, and whether this is due to male body size affecting the costs of harassment or the actual mating rate. In the eastern mosquitofish Gambusia holbrooki, males vary greatly in body size and continually attempt to inseminate females. We experimentally manipulated male presence (i.e., harassment), male body size and whether males could copulate. Exposure to males had strong detrimental effects on female reproductive output, growth and immune response, independent of male size or whether males could copulate. In contrast, there was a little evidence of a cross‐generational effect of male harassment or mating rate on offspring performance. Our results suggest that females housed with males pay direct costs due to reduced condition and offspring production and that these costs are not a consequence of increased mating rates. Furthermore, exposure to males does not affect offspring reproductive traits.     

Sex differences in the trade-off between feeding and mating in the guppy

Male guppies Poecilia reticulata court almost continuously and often indulge in sneaky mating attempts. Female guppies, on the other hand, devote much of their time to foraging. This paper demonstrates that both sexes reduce their feeding rate in mixed-sex groups relative to single sex ones and suggests that the decrease is less pronounced for females than for males. Thus males make feeding and mating decisions that are dependent on hunger while female foraging behaviour is constrained by sexual harassment. The observed sex differences in behaviour are a consequence of asymmetrical mating costs in males and females.     

Male mating strategies under predation risk: do females call the shots?

Many authors have reported that, under elevated risk of predation,male guppies (Poecilia reticulata) alter their behavior fromcourtship to forced copulation (gonopodial thrusts not precededby sigmoid displays). This shift is presumed to benefit thebrightly colored male, whose intense courting activity mightotherwise increase his risk of detection and attack by predators.However, there is some evidence that females engaged in reproductiveactivity with males may be even more vulnerable to predatorsthan the males themselves, which suggests an alternative hypothesis:females in high-risk situations are less receptive to male courtship,and this leads males to change their behavior. We tested thishypothesis by providing either males and females separately,or both sexes concurrently, with information about elevatedpredation risk from a cichlid (Crenicichla sp.). We found thatwhen only females were provided with information about increased risk,males performed fewer courtship displays and fewer thrusts.They did not perform more forced copulations in any treatmentgroup. Nonetheless, our results suggest that the female's perceptionof predation risk can be at least as important as the male'sin changing male mating behavior.     

Effects of size and sex on the courting success and foraging behaviour of Embiotoca jacksoni

To test life-history theory that body size and sex should influence how animals allocate time to foraging versus reproductive activities, we measured the effects of size and sex on courting success and foraging behaviour of black surfperch Embiotoca jacksoni off Santa Catalina Island, southern California. Observations of focal fish were made while snorkelling, during which the length of each fish (estimated to the nearest cm), total duration of courting encounters and foraging rates were recorded. We made observations during and outside the mating season. Courtship occurred only between pairs and its duration increased with the size of both the male and female. Although males would court females that were smaller or larger than themselves, pairs that were closely matched in size had long courting sessions, whereas those that differed considerably in size courted only briefly. Small fish foraged more than larger fish, both during and outside the mating season. Males and females foraged at similar rates outside of the mating season, but during the mating season males reduced their foraging rates to less than half that seen outside of the mating season, whereas females continued to forage at the same rate. This decrease in foraging rate of males during the mating season was seen in all sizes of males but was proportionally greatest in the largest males. These observations indicate that males trade off time spent on foraging for time spent courting during the mating season, whereas females do not.     

Influence of male competition on male mating behaviour in the cave molly, Poecilia mexicana

In many species, male mating behaviour is correlated with male body size, with large males often being preferred by females. Small surface-dwelling Poecilia mexicana males compensate for this disadvantage by being more sexually active and using sneaky copulations. In a cave-dwelling population, however, small males do not show this behaviour. Do small males alter their behaviour in the presence of a large rival? Here, we investigated the influence of male competition on male mating behaviour in the cave form. Two males of different sizes were mated with a female either alone or together with the other male. No aggressive interactions were observed between either fish. There was no statistically significant difference in the frequency of sexual behaviours between the two treatments. In both treatments, large males were more sexually active than small males. Thus, small cave molly males do not switch to an alternative mating behaviour in the presence of a larger rival. Possibly, the extreme environmental conditions in the cave (e.g. low oxygen content and high levels of hydrogen sulphide) favour saving energetic costs, resulting in the absence of alternative mating behaviour in small males.     

Mechanisms and consequences of sexual conflict in garter snakes (Thamnophis sirtalis, Colubridae)

Red-sided garter snakes (Thamnophis sirtalis parietalis) courtand mate in early spring around large communal overwinteringdens in central Manitoba. Emerging females are immediately coveredby dozens or hundreds of vigorously-courting males, potentiallyimposing significant costs to the female. By manipulating numbersof courting males (both directly and by applying anticourtshippheromones), we quantified the degree to which female dispersalfrom the den is hindered by courtship. Courted females dispersedonly about half as fast as did solitary females. Blood lactatelevels were higher in mating than in courting or noncourtingsnakes of both sexes; the high levels of lactate in mating femalessupport the idea that courtship is physiologically stressfulto these animals, perhaps via constraints to female respiration.In arena trials, females that were exercised to exhaustion beforecourtship mated with smaller males than did control females.The spatial distribution of snakes around the den exhibits substantialheterogeneity, with densities often varying markedly betweenadjacent areas. Arena trials mimicking this heterogeneity showedthat unmated females avoided parts of the enclosure containingscent cues from males. Our data support the hypothesis thatcourtship in T. s. parietalis confers significant costs to females,and that female behaviors have evolved to reduce those costs.     

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.     

Looking for sexual selection in the female brain

Female mate choice behaviour has significant evolutionary consequences, yet its mechanistic origins are not fully understood. Recent studies of female sensory systems have made great strides in identifying internal mechanisms governing female preferences. Only recently, however, have we begun to identify the dynamic genomic response associated with mate choice behaviour. Poeciliids provide a powerful comparative system to examine genomic responses governing mate choice and female preference behaviour, given the great range of mating systems: from female mate choice taxa with ornamental courting males to species lacking male ornamentation and exhibiting only male coercion. Furthermore, they exhibit laboratory-tractable preference responses without sexual contact that are decoupled from reproductive state, allowing investigators to isolate mechanisms in the brain without physiological confounds. Early investigations with poeciliid species (Xiphophorus nigrensis and Gambusia affinis) have identified putative candidate genes associated with female preference response and highlight a possible genomic pathway underlying female social interactions with males linked functionally with synaptic plasticity and learning processes. This network is positively correlated with female preference behaviour in the female mate choice species, but appears inhibited in the male coercive species. This behavioural genomics approach provides opportunity to elucidate the fundamental building blocks, and evolutionary dynamics, of sexual selection.     

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.     

Effect of parasitic infection on male color pattern and female choice in guppies

We infected male guppies Poecilia reticulata with a naturallyoccurring monogenean parasite, Gyrodactylus turnbulli, in orderto examine effects of parasitism on the expression of colorpatterns and on attractiveness to females. The color of carotenoidspots and ability to attract females were compared between experimentallyinfected fish and a control group of their fullsib brothers,which had identical color patterns and were treated identicallyexcept for actual exposure to parasites. The orange spots ofmales that had been infected for 9 days followed by treatmentwith medication to remove parasites became significandy palerand less saturated. Control males (also treated widi medication)showed no significant changes in their orange spots. Femalesin a divided aquarium choice-apparatus showed no preferencebetween control and infection-treatment males initially, butshowed significant discrimination after the infectiondisinfectiontreatment. Females spent less time near males that had beeninfected and responded to a smaller fraction of their courtshipdisplays relative to control males. There were slight differencesin courting rates of males between treatments. Parasitic infectionappears to reduce the degree of expression of carotenoid colorsin guppies, and females are able to discriminate against recentlyinfected males, probably on the basis of the color change. Byavoiding infected males, females may be able to avoid becominginfected themselves, or they may be able to identify mates basedon "good genes" for parasite resistance diat can be passed onto their offspring.     

Persistent courtship reduces male and female longevity in captive tsetse flies Glossina morsitans morsitans Westwood (Diptera: Glossinidae)

Where males can increase their mating success by harassing femalesuntil they accept copulation, harassing tactics can be expectedto evolve to a point where they have costs to the longevityof both sexes. By experimentally manipulating the sex ratioin captive groups of tsetse flies Glossina morsitans morsitans,we demonstrated that the longevity of females declines wheresex ratios are biased toward males, while the longevity of malesdeclines where the sex ratio is biased toward females. Neitherirradiation of males nor prevention of copulation by blockingor damaging the external male genitalia increased the longevityof females caged with them, suggesting that female longevitywas reduced by the physical aspects of male harassment ratherthan by components of the ejaculate     

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.     

Interacting effects of predation risk and male and female density on male/female conflicts and mating dynamics of stream water striders

We used a factorial experiment to examine interacting effectsof male density, female density, and sunfish (predation risk)on mating dynamics of the stream water strider (Aquarius remigis).Many of our results corroborated earlier studies on the isolatedeffects of each factor on mating behavior. The effect of eachfactor, however, depended on the other factors. For example,in low density pools, predation risk decreased male generalactivity, male/female harassment rates, mating activity, andmating duration and increased the large male mating advantage.At higher densities, however, water striders apparently enjoyed"safety in numbers" and did not alter their mating dynamicsin response to the presence of predators. Female activity showeda particularly complex response to male density and fish. Whenmales were scarce, fish caused females to reduce their activity.However, when males were abundant, fish increased female activity,probably because fish decreased male activity thus releasingfemales from harassment by males. The three treatment factorsalso had interacting effects on male mating success. In theabsence of fish, when females were scarce, increased male densityresulted in a decrease in mean male mating success; however,when females were abundant, increased male density enhancedmean male mating success. In contrast, in the presence of fish,male density had little effect on male mating success. Manyof the observed mating patterns can be explained by the effectsof ecological and social factors on male/female conflicts; thatis, on male harassment of females and female reluctance to mate.     

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.     

Divergent female mating preference in a clonal fish

In asexual all-female species, such as the Amazon molly, Poecilia formosa, that depend on sperm from “host males” only to trigger embryogenesis, mate choice does not provide any indirect, genetic benefits to the choosing female, although direct benefits are possible. Asexual species are thought to have a low evolutionary potential or evolvability due to the absence of meiotic recombination. Hence, theory predicts that mating preferences in P. formosa for male ornaments—if existent—should resemble those of females of the two parental species (Poecilia latipinna and Poecilia mexicana) involved in the natural hybridization that gave rise to the asexual P. formosa. When examining the female preference for dummy males with or without black vertical bars in the two parental species and in two lineages of P. formosa, a preference was detected in P. latipinna, but not in P. mexicana females. Interestingly, P. formosa living syntopic with P. latipinna also preferred striped males, while others living syntopic with P. mexicana preferred non-striped males. The evolutionary significance of this phenomenon remains largely unexplained, but it might indicate the evolution of mating preferences in a species with low evolutionary potential. Possible mechanisms include introgression and mitotic gene conversion. Females might use male coloration as indicator mechanisms for male traits that matter in terms of direct benefits.     

Alternative reproductive tactics in male freshwater fish influence the accuracy of species recognition

Sexual conflict can result in coercive mating. Because males bear low costs of heterospecific mating, coercive males may engage in misdirected mating attempts toward heterospecific females. In contrast, sexual selection through consensual mate choice can cause mate recognition cues among species to diverge, leading to more accurate species recognition. Some species show both coercive mating and mate choice‐associated courtship behaviors as male alternative reproductive tactics. We hypothesized that if the selection pressures on each tactic differ, then the accuracy of species recognition would also change depending on the mating tactic adopted. We tested this hypothesis in the guppy (Poecilia reticulata) and mosquitofish (Gambusia affinis) by a series of choice experiments. Poecilia reticulata and G. affinis males both showed imperfect species recognition and directed all components of mating behavior toward heterospecific females. They tended to direct courtship displays more frequently toward conspecific than heterospecific females. With male P. reticulata, however, accurate species recognition disappeared when they attempted coercive copulation: they directed coercions more frequently toward heterospecific females. We also found that heterospecific sexual interaction had little effect on the fecundity of gravid females, which suggests that prepregnancy interactions likely underpin the exclusion of G. affinis by P. reticulata in our region.     

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.