The Role of Body Size in Mating Interactions of the Sexually Cannibalistic Fishing Spider Dolomedes triton

Some arachnids display extreme sexual size dimorphism (SSD) with adult females being several times larger than adult males. One explanation for SSD in species that exhibit pre‐copulatory sexual cannibalism (female attack, kill and consumption of the male prior to mating) is that smaller males may be less likely victims of predatory attacks by females. However, in some sexually cannibalistic species SSD is relatively moderate (i.e. males are similar in size to females) suggesting benefits of large male body size. Here, I report the results of an experiment designed to explore the ramifications of body size in mating interactions of the sexually cannibalistic, North American fishing spider (Dolomedes triton). Results suggest that male size does not influence courtship behavior, the likelihood of being attacked, or the male's ability to secure a mounting. However, large males were superior at gaining copulations once mounted. Sexual cannibalism may also be predicated on female size. Female condition (mass/cephalothorax area) did not explain any of these behaviors from the copulatory sequence, however, females with a smaller cephalothorax area were more likely to attack courting males. Finally, analysis of the ratio of female size to male size showed that when SSD is weak males are more likely to escape attacks and mate successfully. Results are discussed in light of several hypotheses for sexual cannibalism, and the benefits of large male body size illustrated here are put forth as potential explanations for the relatively moderate extent of SSD found in this sexually cannibalistic species.     

Remote copulation: male adaptation to female cannibalism

Sexual cannibalism by females and associated male behaviours may be driven by sexual conflict. One such male behaviour is the eunuch phenomenon in spiders, caused by total genital emasculation, which is a seemingly maladaptive behaviour. Here, we provide the first empirical testing of an adaptive hypothesis to explain this behaviour, the remote copulation, in a highly sexually cannibalistic orb-web spider Nephilengys malabarensis. We demonstrate that sperm transfer continues from the severed male organ into female genitals after the male has been detached from copula. Remote copulation increases the total amount of sperm transferred, and thus probably enhances paternity. We conclude that the mechanism may have evolved in response to sexual cannibalism and female-controlled short copulation duration.     

Female behaviour and the interaction of male and female genital traits mediate sperm transfer during mating

Natural selection and post‐copulatory sexual selection, including sexual conflict, contribute to genital diversification. Fundamental first steps in understanding how these processes shape the evolution of specific genital traits are to determine their function experimentally and to understand the interactions between female and male genitalia during copulation. Our experimental manipulations of male and female genitalia in red‐sided garter snakes (Thamnophis sirtalis parietalis) reveal that copulation duration and copulatory plug deposition, as well as total and oviductal/vaginal sperm counts, are influenced by the interaction between male and female genital traits and female behaviour during copulation. By mating females with anesthetized cloacae to males with spine‐ablated hemipenes using a fully factorial design, we identified significant female–male copulatory trait interactions and found that females prevent sperm from entering their oviducts by contracting their vaginal pouch. Furthermore, these muscular contractions limit copulatory plug size, whereas the basal spine of the male hemipene aids in sperm and plug transfer. Our results are consistent with a role of sexual conflict in mating interactions and highlight the evolutionary importance of female resistance to reproductive outcomes.     

Genital damage in the orb-web spider Argiope bruennichi (Araneae: Araneidae) increases paternity success

The morphology of male genitalia often suggests functions besidessperm transfer that may have evolved under natural or sexualselection. In several species of sexually cannibalistic spiders,males damage their paired genitalia during mating, limitingthem to one copulation per pedipalp. Using a triple-mating experiment,we tested if genital damage in the orb-web spider Argiope bruennichiincreases male fitness either through facilitating his escapefrom an aggressive female or by obstructing the female's inseminationducts against future copulation attempts from other males. Wefound no survival advantage for males damaging their pedipalps;however, copulations into a previously used insemination ductwere significantly shorter when the previous male had left partsof his genitalia inside the insemination duct. Because copulationduration determines paternity in this species, our result suggeststhat male genital damage in A. bruennichi is sexually selected.By breaking off parts of their intromittent organs inside avirgin female, males can reduce sperm competition and therebyincrease their paternity success.     

Genital morphology and fertilization success in the dung beetle Onthophagus taurus: an example of sexually selected male genitalia

In animals with internal fertilization and promiscuous mating, male genitalia show rapid and divergent evolution. Three hypotheses have been suggested to explain the evolutionary processes responsible for genital evolution: the lock-and-key hypothesis, the pleiotropy hypothesis and the sexual-selection hypothesis. Here, we determine whether variation in male genital morphology influences fertilization success in the dung beetle Onthophagus taurus, as predicted by the sexual-selection hypothesis. Variation in four out of five genital sclerites of the endophallus influenced a male's fertilization success, supporting the general hypothesis that male genitalia can evolve under sexual selection. Furthermore, different genital sclerites were found to enhance first versus second male paternity, indicating that different sclerites serve offensive and defensive roles. Genital-trait variability was comparable to that in other species but was less variable than a non-genital sexually selected trait (head horns). We suggest that directional selection for genital elaboration may be countered by natural selection, which should favour genitalia of a size and shape necessary for efficient coupling and sperm transfer.     

Intraspecific evidence from guppies for correlated patterns of male and female genital trait diversification

The role of sexual selection in fuelling genital evolution is becoming increasingly apparent from comparative studies revealing interspecific divergence in male genitalia and evolutionary associations between male and female genital traits. Despite this, we know little about intraspecific variance in male genital morphology, or how male and female reproductive traits covary among divergent populations. Here we address both topics using natural populations of the guppy, Poecilia reticulata, a livebearing fish that exhibits divergent patterns of male sexual behaviour among populations. Initially, we performed a series of mating trials on a single population to examine the relationship between the morphology of the male's copulatory organ (the gonopodium) and the success of forced matings. Using a combination of linear measurements and geometric morphometrics, we found that variation in the length and shape of the gonopodium predicted the success of forced matings in terms of the rate of genital contacts and insemination success, respectively. We then looked for geographical divergence in these traits, since the relative frequency of forced matings tends to be greater in high-predation populations. We found consistent patterns of variation in male genital size and shape in relation to the level of predation, and corresponding patterns of (co)variation in female genital morphology. Together, these data enable us to draw tentative conclusions about the underlying selective pressures causing correlated patterns of divergence in male and female genital traits, which point to a role for sexually antagonistic selection.     

Challenging the Aggressive Spillover Hypothesis: Is Pre‐Copulatory Sexual Cannibalism a Part of a Behavioural Syndrome?

Pre‐copulatory cannibalism – females devouring males during courtship – may bring no benefit to either sex. The ‘aggressive spillover hypothesis’ (ASH) posits that pre‐copulatory cannibalism represents a spillover of female aggressiveness from the juvenile foraging context, when aggressiveness is advantageous, to the adult mating context, when aggressiveness may be non‐adaptive or maladaptive. The ASH suggests that individuals exhibit limited plasticity in aggressive behaviours because they are genetically canalised for indiscriminate aggressiveness towards prey and conspecifics, including males. Hence, a tendency to employ pre‐copulatory cannibalism is a part of the female aggression syndrome, an assertion generally accepted in the personality field. We here re‐evaluate the previous findings in the light of personality criteria, which we propose for ASH validation: between‐individual differences, repeatability and heritability in tendency for pre‐copulatory attacks (and pre‐copulatory cannibalism) and voracity towards prey, and their correlation. To re‐evaluate ASH and to allow for additional or alternative explanations, we ask whether pre‐copulatory cannibalism depends on female hunger, mating status, size and/or male quality. Finally, we ask whether cannibalistic females have a reduced reproductive success as predicted by the ASH. While repeatability and heritability in voracity towards prey and its correlation with the tendency to engage in pre‐copulatory cannibalism were found in certain systems, we lack any evidence for repeatability and heritability in pre‐copulatory cannibalistic attempts and for its maladaptiveness. Rather than only resorting to the ASH, foraging and mate choice hypotheses may also explain pre‐copulatory cannibalism. We suggest clarifying the use of the terms sexual cannibalism (effect) and female aggressiveness or tendency to attack and devour males (cause), and argue that male strategies to avoid cannibalism should be considered. We propose testing the ASH as the explanation for pre‐copulatory cannibalism in those cases where female tendency to devour males correlates with actual pre‐copulatory cannibalism and when all the above criteria are fulfilled. Finally, we propose future directions for studying the ASH.     

Sexual cannibalism in the fishing spider and a model for the evolution of sexual cannibalism based on genetic constraints

Several hypotheses have been proposed for the evolution of sexual cannibalism by females. Newman and Elgar (1991) suggested that sexual cannibalism prior to mating by virgin female spiders may have evolved as a result of female foraging considerations. According to this model, an adult female's decision to mate or cannibalize a courting male should be based on an assessment of the male's value as a meal versus his value as a mate. The current study provides an empirical test of the assumptions and predictions of this model in the sexually cannibalistic fishing spider. Adult females were subjected to different food treatments, and exposed to adult males in the laboratory. However, only one of the assumptions of the model and none of its five predictions were upheld. We failed to find any effects of female foraging, female mating status, female size, male size or time of the season on females' behaviour towards courting males. Females behaved stereotypically, and many females were left unmated despite numerous mating opportunities. We also demonstrate costs of sexual cannibalism in a natural population. We propose that the act of sexual cannibalism in the fishing spider is non-adaptive, and develop a model for the evolution of premating sexual cannibalism in spiders based on genetic constraints. According to this hypothesis, sexual cannibalism by adult females may have evolved as an indirect result of selection for high and non-discriminate aggression during previous ontogenetic stages. Genetic covariance between different components of aggressive behaviour may constrain the degree to which (1) juvenile and adult aggression and/or (2) aggression towards conspecifics and heterospecifics can vary independently. We briefly review the support for our model, and suggest several critical tests that may be used to assess the assumptions and predictions of the model.     

Frequent Failure of Male Monopolization Strategies as a Cost of Female Choice in the Black Widow Spider Latrodectus tredecimguttatus

In many mating systems, males strive for securing paternity through monopolizing females. As male monopolization attempts often contradict female interests, this conflict may fuel an evolutionary arms race. In the widow spider genus Latrodectus, females are commonly polyandrous, whereas males are monogynous, hence restricted to mate with a single female, making paternity protection particularly important. Potential mating plugs (specialized embolus sclerites of male copulatory organs) have been discovered in the complex female genital tracts of several Latrodectus species. In this study, we investigated mating strategies in the Mediterranean black widow spider Latrodectus tredecimguttatus and tested the adaptive value of female attacks against male monopolization efforts. In a double mating experiment, we manipulated the number of insertions (=copulations) for first and second males to assess female behaviour and male embolus sclerite placement success. Our results indicate that first males′ embolus sclerites inside the females′ sperm stores physically block sclerites of subsequent males. While female attacks did not affect the deposition of potential mating plugs, they significantly reduced copulation duration. Irrespective of female aggression, male sclerite placement failure occurred frequently, but large males were more successful than smaller competitors. We suggest that the complex genital morphology in both sexes may have co‐evolved antagonistically and female morphology could serve to favour large males for fertilization.     

Sexual cannibalism: high incidence in a natural population with benefits to females

Background

Sexual cannibalism may be a form of extreme sexual conflict in which females benefit more from feeding on males than mating with them, and males avoid aggressive, cannibalistic females in order to increase net fitness. A thorough understanding of the adaptive significance of sexual cannibalism is hindered by our ignorance of its prevalence in nature. Furthermore, there are serious doubts about the food value of males, probably because most studies that attempt to document benefits of sexual cannibalism to the female have been conducted in the laboratory with non-natural alternative prey. Thus, to understand more fully the ecology and evolution of sexual cannibalism, field experiments are needed to document the prevalence of sexual cannibalism and its benefits to females.

Methodology/Principal Findings

We conducted field experiments with the Mediterranean tarantula (Lycosa tarantula), a burrowing wolf spider, to address these issues. At natural rates of encounter with males, approximately a third of L. tarantula females cannibalized the male. The rate of sexual cannibalism increased with male availability, and females were more likely to kill and consume an approaching male if they had previously mated with another male. We show that females benefit from feeding on a male by breeding earlier, producing 30% more offspring per egg sac, and producing progeny of higher body condition. Offspring of sexually cannibalistic females dispersed earlier and were larger later in the season than spiderlings of non-cannibalistic females.

Conclusions/Significance

In nature a substantial fraction of female L. tarantula kill and consume approaching males instead of mating with them. This behaviour is more likely to occur if the female has mated previously. Cannibalistic females have higher rates of reproduction, and produce higher-quality offspring, than non-cannibalistic females. Our findings further suggest that female L. tarantula are nutrient-limited in nature and that males are high-quality prey. The results of these field experiments support the hypothesis that sexual cannibalism is adaptive to females.     

A non-sperm transferring genital trait under sexual selection: an experimental approach

Male genitalia are among the fastest evolving morphological characters, and at a general level sexual selection seems to be involved. But experimental determination of the functions of many remarkable genitalic elaborations is very rare. Here we present the first study to address experimentally the adaptive function of a male genital structure that is not involved in sperm transfer. Females of the orb-weaving spider Argiope bruennichi are sexually cannibalistic and polyandrous. The male increases his paternity by obstructing the female's insemination duct with a fragment of his complex genitalia (embolus tip). We manipulated males by detaching another species-specific structure, the median apophysis spur, and found that the spur promotes breakage of the embolus tip inside the female duct, but does not affect the probability and duration of copulation. These data are novel in that they suggest that a genitalic structure which does not transfer sperm nevertheless evolved in the context of sperm competition.     

Female genital morphology and mating behavior of Orchestina (Arachnida: Araneae: Oonopidae)

The unusual reproductive biology of many spider species makes them compelling targets for evolutionary investigations. Mating behavior studies combined with genital morphological investigations help to understand complex spider reproductive systems and explain their function in the context of sexual selection. Oonopidae are a diverse spider family comprising a variety of species with complex internal female genitalia. Data on oonopid phylogeny are preliminary and especially studies on their mating behavior are very rare. The present investigation reports on the copulatory behavior of an Orchestina species for the first time. The female genitalia are described by means of serial semi-thin sections and scanning electron microscopy. Females of Orchestina sp. mate with multiple males. On average, copulations last between 15.4 and 23.54 min. During copulation, the spiders are in a position taken by most theraphosids and certain members of the subfamily Oonopinae: the male pushes the female back and is situated under her facing the female's sternum. Males of Orchestina sp. possibly display post-copulatory mate-guarding behavior. The female genitalia are complex. The genital opening leads into the uterus externus from which a single receptaculum emerges. The dorsal wall of the receptaculum forms a sclerite serving as muscle attachment. A sclerotized plate with attached muscles lies in the posterior wall of the uterus externus. The plate might be used to lock the uterus during copulation. The present study gives no direct evidence for cryptic female choice in Orchestina sp. but suggests that sexual selection occurs in the form of sperm competition through sperm mixing.     

Safer sex with feeding females: sexual conflict in a cannibalistic spider

Mating strategies are to a large degree shaped by conflictsbetween the sexes, causing a rapid antagonistic coevolutionof traits involved in reproduction. The view that sexual cannibalismrepresents a form of sexual conflict leads to the predictionof male traits that facilitate escape from cannibalistic females.A variety of traits have been suggested to serve this functionin spiders, where sexual cannibalism is comparatively common.Empirical evidence, however, is virtually absent. Here we showexperimentally that opportunistic mating with feeding females,which has been reported from several species of orb-weavingspiders, greatly reduces the risk of cannibalism and injuryfor males in the spider Nephila fenestrata. This has directconsequences for a male's fertilization success because survivingmales can reduce the female's remating probability by guardingher against rivals. Although copulation with previously matedfemales sometimes appears to be mechanically impossible, secondmales that do copulate can expect to fertilize on average 64%of a female's eggs. Our results support the view that opportunisticmating may have evolved as a male tactic in a context of sexualconflict over sexual cannibalism.     

Does Female Personality Determine Mate Choice Through Sexual Cannibalism?

Animal personalities (e.g. consistent across‐context behavioural differences between individuals) can lead to differences in mate choice. However, evidence for this link remains limited. Pre‐mating sexual cannibalism can be a behavioural syndrome (i.e. a suboptimal personality) in which adaptive female aggression towards heterospecific prey spills over on non‐adaptive aggression towards courting males, independently of the female mating or feeding status (i.e. the ‘aggressive spillover hypothesis’, ASH). On the other hand, sexual cannibalism can also be a form of mate choice by which females selectively kill or mate with males depending on the male phenotype. We introduce the hypothesis that the most aggressive females in the population will not only attack males more frequently, but will be less likely to impose sexual selection on males through sexual cannibalism. Assuming that in a field common garden experiment in which females were fed ad libitum the rate of weight gain by a female may reflect her voracity or aggressiveness, we show that in the cannibalistic burrowing wolf spider Lycosa hispanica (formerly L. tarantula), voracity towards heterospecific prey predicts a female's tendency towards sexual cannibalism. Unmated females with higher weight gains were more cannibalistic and attacked males regardless of the male phenotype. On the other hand, females that were less voracious tended to be less cannibalistic, and when they did kill a male, they were selective, killing males in poorer condition and mating with those in better condition. Our results demonstrate that females with different phenotypes (growth rates) differently imposed selection on male condition, tentatively supporting the hypothesis that female aggression levels can spill over on sexual selection through sexual cannibalism.     

Behavioral response of male mantid Tenodera aridifolia (Mantodea: Mantidae) to windy conditions as a female approach strategy

When sexual cannibalism presents a sexual conflict, one expects to find male traits that reduce the risk of cannibalism. In sexually cannibalistic species, selection is thought to have favored the evolution of male approach behaviors that reduce the probability that the female will kill the male. We tested the hypothesis that male mantids change their approach behavior in response to wind to reduce the risk of being noticed by females. Time between detection of the female by the male and mating was shorter under windy than windless conditions. Sexual approach behavior was observed more frequently under windy than windless conditions. Moreover, this behavior was observed more frequently when the female was walking than when the female was not walking under windy conditions. The detection rate of male mantids by females was significantly lower on swaying leaves than on fixed leaves. Our results thus indicate that male mantids were more active in response to wind. Therefore, we suggest that the male's quick approach strategy toward females when the wind is blowing at short range is adaptive in reducing the risk of detection by females.     

Evolution of male and female genitalia following release from sexual selection

Despite the key functions of the genitalia in sexual interactions and fertilization, the role of sexual selection and conflict in shaping genital traits remains poorly understood. Seed beetle (Callosobruchus maculatus) males possess spines on the intromittent organ, and females possess a thickened reproductive tract wall that also bears spines. We investigated the role of sexual selection and conflict by imposing monogamous mating on eight replicate populations of this naturally polygamous insect, while maintaining eight other populations under polygamy. To establish whether responses to mating system manipulation were robust to ecological context, we simultaneously manipulated life-history selection (early/late reproduction). Over 18-21 generations, male genital spines evolved relatively reduced length in large males (i.e., shallower static allometry) in monogamous populations. Two nonintromittent male genital appendages also evolved in response to the interaction of mating system and ecology. In contrast, no detectable evolution occurred in female genitalia, consistent with the expectation of a delayed response in defensive traits. Our results support a sexually antagonistic role for the male genital spines, and demonstrate the evolution of static allometry in response to variation in sexual selection opportunity. We argue that further advances in the study of genital coevolution will require a much more detailed understanding of the functions of male and female genital traits.     

Benefits of size dimorphism and copulatory silk wrapping in the sexually cannibalistic nursery web spider,Pisaurina mira

In sexually cannibalistic animals, male fitness is influenced not only by successful mate acquisition and egg fertilization, but also by avoiding being eaten. In the cannibalistic nursery web spider, Pisaurina mira, the legs of mature males are longer in relation to their body size than those of females, and males use these legs to aid in wrapping a female''s legs with silk prior to and during copulation. We hypothesized that elongated male legs and silk wrapping provide benefits to males, in part through a reduced likelihood of sexual cannibalism. To test this, we paired females of random size with males from one of two treatment groups—those capable of silk wrapping versus those incapable of silk wrapping. We found that males with relatively longer legs and larger body size were more likely to mate and were less likely to be cannibalized prior to copulation. Regardless of relative size, males capable of silk wrapping were less likely to be cannibalized during or following copulation and had more opportunities for sperm transfer (i.e. pedipalpal insertions). Our results suggest that male size and copulatory silk wrapping are sexually selected traits benefiting male reproductive success.     

Mate plugging via genital mutilation in nephilid spiders: an evolutionary hypothesis

Nephilid spiders are known for gigantic females and tiny males. Such extreme sexual dimorphism and male-biased sex ratios result in fierce male–male competition for mates. Intense sperm competition may be responsible for behaviors such as mate guarding, mate binding, opportunistic mating, genital mutilation, mating plugs and male castration (eunuchs). We studied the mating biology of two phylogenetically, behaviorally and morphologically distinct south-east Asian nephilid spider species ( Herennia multipuncta, Nephila pilipes ) in nature and in the laboratory. Specifically, we established the frequencies and effectiveness of plugging (a plug is part of the male copulatory organ), and tested for male and female copulatory organ reuse. Both in nature and in the laboratory, plug frequencies were higher in H. multipuncta (75–80% females plugged) compared with N. pilipes (45–47.4%), but the differences were not significant. Plugs were single and effective (no remating) in H. multipuncta but multiple and ineffective (remating possible) in N. pilipes . In Herennia , the males plugged when the female was aggressive and in Nephila plugging was more likely when mating with previously mated and larger females. Further differences in sexual biology are complete palpal removal and higher sexual aggressiveness in Herennia (sexual cannibalism recorded for the first time), and mate binding in Nephila . Thus, we propose the following evolutionary hypothesis: nephilid plugging was ancestrally successful and enabled males to monopolize females, but plugging became ineffective in the phylogenetically derived Nephila . If the evolution of nephilid sexual mechanisms is driven by sexual conflict, then the male mechanism to monopolize females prevailed in a part of the phylogeny, but the female resistance to evade monopolization ultimately won the arms race.     

Death feigning in the face of sexual cannibalism

Pre-copulatory sexual cannibalism by females affects male and female reproductive success in profoundly different ways, with the females benefiting from a meal and the male facing the risk of not reproducing at all. This sexual conflict predicts evolution of traits to avoid cannibalism and ensure male reproductive success. We show that males of the nuptial gift-giving spider Pisaura mirabilis display a remarkable death feigning behaviour--thanatosis--as part of the courtship prior to mating with potentially cannibalistic females. Thanatosis is a widespread anti-predator strategy; however, it is exceptional in the context of sexual selection. When the female approached a gift-displaying male, she usually showed interest in the gift but would sometimes attack the male, and at this potentially dangerous moment the male could 'drop dead'. When entering thanatosis, the male would collapse and remain completely motionless while retaining hold of the gift so it was held simultaneously by both mates. When the female initiated consumption of the gift, the male cautiously 'came to life' and initiated copulation. Death feigning males were more successful in gaining copulations, but did not have prolonged copulations. We propose that death feigning evolved as an adaptive male mating strategy in conjunction with nuptial gift giving under the risk of being victimized by females.     

The evolution of male genitalia: patterns of genetic variation and covariation in the genital sclerites of the dung beetle Onthophagus taurus

Three main hypotheses, have been invoked to explain divergent genital evolution, the lock and key, pleiotropy, and sexual selection hypotheses, each of which make different predictions about how genital traits are inherited. Here we used a half-sib breeding design to examine the patterns of genetic variation and covariation between male genital sclerites, and their covariance with general body morphology in the dung beetle Onthophagus taurus. We found CV(A)'s and CV(P)'s were similar for both genital and general morphological traits and that CV(R)'s were large for both trait types. We found that male genital sclerites were negatively genetically correlated with general morphological traits. Variation in male genital morphology has direct implications for a male's fertilization success and the resulting sexual selection acting on male genitalia is predicted to maintain high levels of additive genetic variance. Contrary to this prediction, we found that individual genital sclerites all had low levels of additive genetic variance and large maternal and environmental sources of variation. Our data suggest that the genital sclerites in O. taurus are not inherited independently but as a genetically integrated unit. More importantly, the way the different sclerites function to influence male fertilization success reflects this genetic integration. Even though levels of V(A) in individual genital sclerites may be low, there may still be sufficient V(A) in multivariate trait space for selection to generate evolutionary change in the overall morphology of male genitalia.