Pre-copulatory Sexual Cannibalism Research Articles

Males discriminate between substrate-borne cues of conspecific females based on age and mating status in the jumping spider, Habronattus brunneus.

Sexual selection is often studied with a focus on female mate choice, wherein females evaluate male signals to select an optimal mate. However, in some systems, males should also make careful decisions about the females they choose to court, particularly when faced with the risk of precopulatory sexual cannibalism. Here, we explore the idea that male jumping spiders (Habronattus brunneus) may mitigate this risk by responding to female cues probably associated with female aggression and/or receptivity. We tested mature male spiders' ability to discriminate between substrate-borne cues (i.e. silk and excreta) produced by conspecific females of different ages and mating statuses. We found that males spent more time exploring cues produced by mature, non-mated females compared with either immature females or mated females. Heightened interest in cues produced by females that are sexually mature but not yet mated may allow males to reduce cannibalism risk, reduce wasted courtship effort and increase their reproductive success. The use of chemical and/or tactile cues in jumping spider courtship behaviour has been vastly understudied compared with the ways they use vision; this study provides the groundwork for understanding how these sensory modalities interact.

Impact of pre-copulatory sexual cannibalism on genetic diversity and efficacy of selection.

Factors that increase reproductive variance among individuals act to reduce effective population size (Ne), which accelerates the loss of genetic diversity and decreases the efficacy of purifying selection. These factors include sexual cannibalism, offspring investment and mating system. Pre-copulatory sexual cannibalism, where the female consumes the male prior to mating, exacerbates this effect. We performed comparative transcriptomics in two spider species, the cannibalistic Trechaleoides biocellata and the non-cannibalistic T. keyserlingi, to generate genomic evidence to support these predictions. First, we estimated heterozygosity and found that genetic diversity is relatively lower in the cannibalistic species. Second, we calculated dN/dS ratios as a measure of purifying selection; a higher dN/dS ratio indicated relaxed purifying selection in the cannibalistic species. These results are consistent with the hypothesis that sexual cannibalism impacts operational sex ratio and demographic processes, which interact with evolutionary forces to shape the genetic structure of populations. However, other factors such as the mating system and life-history traits contribute to shaping Ne. Comparative analyses across multiple contrasting species pairs would be required to disentangle these effects. Our study highlights that extreme behaviours such as pre-copulatory cannibalism may have profound eco-evolutionary effects.

Male coercion and female injury in a sexually cannibalistic mantis.

Sexual conflict can generate coercive traits in males that enhance mating success at the expense of female fitness. Pre-copulatory sexual cannibalism-where females consume males without mating-typically favours cautious rather than coercive mating tactics, and few examples of the latter are known. Here, we show that males of the highly cannibalistic springbok mantis, Miomantis caffra, wrestle females during pre-mating interactions. We find that most initial contacts between males and females involve a violent struggle whereby each sex tries be the first to grasp hold of the other with their raptorial forelegs. When females win the struggle, they always cannibalize males. However, when males grasp females first, they dramatically increase the chance of mating. We also find striking evidence that, on some occasions, males wound females with their fore-tibial claws during struggles, resulting in haemolymph loss and scar tissue formation. Taken together, our results show how males can overcome the threat of cannibalism by coercively wrestling females. We argue that pre-copulatory injury in this species is likely to be a negative pleiotropic side-effect of coercive mating behaviour and foraging morphology.

Behavioural correlations and aggression in praying mantids

Distinct behaviours can co-vary within individuals. As such, the magnitude of certain behaviours may be partly predicted by other behaviours, rather than the environment. This can constrain behaviours, potentially reducing behavioural variability. Pre-copulatory sexual cannibalism, the consumption of potential mates before copulation, can lead to females remaining unmated, particularly if males are rare. One possible explanation for the persistence of pre-copulatory cannibalism is that sexual cannibalism is correlated with high levels of aggression towards prey. Here, we test this in two species of praying mantis: the highly cannibalistic Miomantis caffra and the less cannibalistic Orthodera novaezealandiae. If cannibalism in M. caffra is linked to aggression towards prey, we predicted that (1) M. caffra would be more aggressive towards prey than O. novaezealandiae, (2) female M. caffra would be more aggressive than males, (3) aggression towards prey would be correlated across juvenile and adult instars for M. caffra but not O. novaezealandiae, and (4) aggression towards prey would be associated with a propensity for sexual cannibalism among individual M. caffra. We found evidence supporting predictions one and two, but not predictions three and four. Surprisingly, aggression was shown to be repeatable and correlated across instars for O. novaezealandiae but not M. caffra. Our results suggest sexual cannibalism is not a product of behavioural co-variation, even in clades where sexual cannibalism is common. This suggests that sexual cannibalism evolves due to the direct benefits it brings to females, rather than being a by-product of high aggression towards heterospecific prey.Significance statementIn some animals, different behaviours co-vary within individuals. This may lead to the emergence of costly behaviours and reduce behavioural plasticity. It is theorized that pre-copulatory cannibalism is a costly behavioural by-product of selection for high levels of aggression towards prey. However, there are very few studies that explicitly test this. Here, we provide a behavioural comparison between two species of praying mantis that vary in their propensity to cannibalize and tested whether general aggression is linked cannibalism. We found that aggression towards prey in adults can be linked to juvenile aggression but not a propensity for cannibalism. Although cannibalism rates were higher in the species that was more aggressive towards prey, aggression towards prey was not linked to cannibalism within individuals. This suggests that pre-copulatory cannibalism is not a behavioural by-product but a result of direct selection.

Short and fast vs long and slow: age changes courtship in male orb-web spiders (Argiope keyserlingi).

Male reproductive performance can vary with condition, age and future reproductive opportunities. Web-building spiders are ideal models to examine the effects of senescence on fitness-related behaviours due to strong selection on male courtship to reduce pre-copulatory sexual cannibalism. Argiope keyserlingi spiders generate courtship vibrations, or 'shudders', that reduce female aggression. We found that male A. keyserlingi courtship slowed with chronological age. Older males took longer to travel across the courtship thread, and overall number of shudders increased. Males retained some ability to modulate courtship quality (shudder duration and number of rocks within each shudder) in response to female quality. A change in courtship performance over time, despite strong selection for repeatability, indicates that ageing in male A. keyserlingi may have direct impacts on reproductive performance.

Feeding regime, adult age and sexual size dimorphism as determinants of pre-copulatory sexual cannibalism in virgin wolf spiders

Pre-copulatory sexual cannibalism (Pre-SC), where females attack and consume courting males, is considered an extreme case of sexual conflict. Different ultimate causes underlying this phenomenon have been proposed for more than a century and still remain unclear. The main objective of this research was to test the ‘adaptive foraging hypothesis’ in females of the non-burrowing wolf spider Lycosa fasciiventris. We exposed virgin adult females to either rich or poor diet treatments (differing in prey quality and availability) and offered them males at different adult female ages (a proxy of mate availability during adulthood). The analysis of correlative data served to evaluate other hypotheses/predictions. In order to test the ‘mate choice hypothesis’ and the ‘sexual size dimorphism hypothesis’, we tested how male absolute and relative (to the female) body size, respectively, affected the probability of Pre-SC. Finally, we asked if the female body size predicts the rate of Pre-SC as proposed by the ‘aggressive spillover hypothesis’. Females from the poor diet treatment and females that were offered a mate shortly after reaching maturity more likely engaged in Pre-SC than females from the rich diet treatment and females that were deprived of males for longer periods. While females more likely cannibalized courting males of relatively or absolutely smaller body size, female absolute body size did not predict Pre-SC. Thus, our results support the ‘adaptive foraging hypothesis’, the ‘mate choice hypothesis’ and the ‘sexual size dimorphism hypothesis’ and failed to find support for one of the predictions of the ‘aggressive spillover hypothesis’. Pre-copulatory sexual cannibalism, where females kill and devour courting males, may be costly for both sexes raising questions about its adaptive aspects and evolution. We used wolf spider Lycosa fasciiventris to test several existing hypotheses aiming to explain the phenomenon. Pre-copulatory cannibalism in virgin females was predicted by their food availability during adulthood, age at first male encounter and the relative body size of the courting male. Females more likely engaged in pre-copulatory cannibalism if they were poorly fed, young at first male encounter and relatively larger than their courting males. Thus, our data may simultaneously support the ‘adaptive foraging’, the ‘sexual size dimorphism’ and the ‘mate choice’ hypotheses as the explanations for pre-copulatory cannibalism occurrences in L. fasciiventris.

The shield effect: nuptial gifts protect males against pre-copulatory sexual cannibalism.

Several not mutually exclusive functions have been ascribed to nuptial gifts across different taxa. Although the idea that a nuptial prey gift may protect the male from pre-copulatory sexual cannibalism is attractive, it has previously been considered of no importance based on indirect evidence and rejected by experimental tests. We reinvestigated whether nuptial gifts may function as a shield against female attacks during mating encounters in the spider Pisaura mirabilis and whether female hunger influences the likelihood of cannibalistic attacks. The results showed that pre-copulatory sexual cannibalism was enhanced when males courted without a gift and this was independent of female hunger. We propose that the nuptial gift trait has evolved partly as a counteradaptation to female aggression in this spider species.

The risk of sexual cannibalism and its effect on male approach and mating behaviour in a praying mantid

Precopulatory sexual cannibalism is an extreme form of sexual conflict because it has the potential to eliminate current and future reproductive success for males. Several female factors such as body condition, mating status and orientation are predicted to impact the likelihood of cannibalism, and males are expected to respond to these factors by altering their approach behaviours in ways that minimize the chance of being attacked (i.e. slower approach and greater distance at mounting). We used the sexually cannibalistic praying mantid Pseudomantis albofimbriata to test whether and how certain female risk factors affect male approach and mating behaviour. We created three different risk treatments by manipulating female body condition, mating status and orientation, and recorded the frequency of cannibalism, male mating success, male approach behaviours and copulation duration. As predicted, female body condition and mating status had an effect on the frequency of sexual cannibalism, and cannibalized males had significantly lower mating success than noncannibalized males. Female orientation was the least important factor in determining the rate of sexual cannibalism in this system, with no significant difference between front- and rear-facing females. Contrary to what we predicted, male P. albofimbriata did not alter/shape their approach or mating behaviours relative to any of the proposed female risk factors of sexual cannibalism. There was also no difference in copulation duration between cannibalized and noncannibalized males. Future studies that investigate the effect of sexual cannibalism on postcopulatory male mating strategies will provide better clarification of the costs and benefits of sexual cannibalism in this system and will also be useful in understanding why males do not respond to the risk of sexual cannibalism in a precopulatory scenario.

Precopulatory Sexual Cannibalism Causes Increase Egg Case Production, Hatching Success, and Female Attractiveness to Males

AbstractPrecopulatory sexual cannibalism is an extreme form of sexual conflict that can entail significant costs to the cannibalized individual and a variety of costs and benefits to the cannibal itself. Characterizing these costs and benefits is fundamental to our understanding of how this behavior evolves. Using the spider Agelenopsis pennsylvanica, we tested the reproductive consequences of precopulatory sexual cannibalism by staging cannibalization events and comparing the performance of experimental cannibals against natural cannibals (i.e., those that cannibalized on their own) and non‐cannibals. We found two performance benefits associated with precopulatory sexual cannibalism: first, experimental cannibals were more likely to produce egg cases than non‐cannibals, and second, egg cases from experimental cannibals and natural cannibals were significantly more likely to hatch than those produced by non‐cannibals. We then tested whether males were more likely to approach the webs of experimental cannibals vs. non‐cannibalistic control females. Our data demonstrate that sexual cannibalism increases female attractiveness to males. Although this result seems counterintuitive, in fact, rates of precopulatory sexual cannibalism were much lower in females that had already cannibalized their first male: 38% of sexually naïve females engaged in precopulatory sexual cannibalism, whereas only 5% of females engaged in cannibalism a second time. Thus, males that approach cannibals receive two benefits: they are less likely to be cannibalized precopula, and they have the possibility of mating with females that have a higher probability of producing viable egg cases. Taken together, our data suggest that precopulatory sexual cannibalism affords females numerous benefits and may have a hand in shaping male mate choice decisions.

Debates: The Aggressive Spillover Hypothesis: Existing Ailments and Putative Remedies

AbstractThe aggressive spillover hypothesis posits that precopulatory sexual cannibalism could evolve as a byproduct of directional selection on aggressiveness in a foraging context. In this debates piece we consider the critique of Kralj‐Fišer and collaborators on the existing evidence in favor of the aggressive spillover hypothesis. Like Kralj‐Fišer et al., we are of the opinion that the evidence in favor of the aggressive spillover hypothesis is still fairly weak. Despite this fact, the hypothesis remains one of the most widely celebrated examples of how behavioral syndromes can generate adaptive trade‐offs. We describe herein several opportunities to build upon the existing data in favor of the aggressive spillover hypothesis and more critically evaluate its assumptions and predictions.

Sexual cannibalism is associated with female behavioural type, hunger state and increased hatching success

Precopulatory sexual cannibalism may represent the most extreme form of sexual conflict because it necessarily truncates the reproductive potential of the victim. Three of the most prominent mechanisms invoked to explain incidence of precopulatory sexual cannibalism are the ‘adaptive foraging’, ‘aggressive spillover’ and ‘mate choice’ hypotheses. These hypotheses argue that sexual cannibalism is either (1) the result of female choice, where females gauge the benefits of suitors as perspective mates versus prey, (2) a neutral (or deleterious) by-product of selection on aggressiveness in nonreproductive contexts, or (3) a mechanism by which females express their mating preferences, respectively. We tested the predictions of these hypotheses in the funnel-web spider Agelenopsis pennsylvanica using staged laboratory encounters. We then tracked numerous fitness proxies of cannibalistic versus noncannibalistic females to determine whether cannibalism was associated with increased female performance. We found that more aggressive females and those deprived of food were more likely to engage in precopulatory cannibalism. Cannibalism was not associated with male condition, male body size or female body size, nor with the mass of females' egg cases, the number of eggs therein, or the mass of individual eggs. In contrast, there was a positive association between the mass of the egg case and the number of offspring that emerged in cannibalistic females, but not in noncannibalistic females. Thus, offspring of cannibalistic mothers appear to have increased hatching success in heavier egg cases. This may represent a novel advantage associated with sexual cannibalism.

Multimodal mate assessment by male praying mantids in a sexually cannibalistic mating system

The traditional view of sexual selection has been that of competing males and choosy females; however, more recently it has been recognized that males mayexhibit mate choice when females vary in quality and when males suffer costs associated with mating. Sexually cannibalistic mating systems provide an opportunitytoexaminemalematechoicefurther:thehighcostspotentiallyinvolvedinthematingprocess for males, as well as variation in female quality, predict male mate choice. We used the praying mantid Pseudomantis albo! mbriata to determine the effect of female body condition on male mate choice in a system with frequent precopulatory sexual cannibalism. Female body condition is positively correlated with fecundity and negatively correlated with the propensity to cannibalize, so we predicted males would strongly prefer females in good condition to maximize their reproductive potential. Results of our simultaneouschoicetestsshowedthatmalesusechemicalandvisualcuesformatelocationandassessment,and that theycan use eitherof these sensory modalities to distinguish and choose between females differing in body condition, with a signi! cant preference for good-condition females. However, surprisingly, males rarely rejected poor-condition females in the more ecologically relevant scenario of only one immediate potential mate and both sensory modes available to them, which may be explained by the strong scramble competition known for praying mantid systems. These results show that even when female quality varies and the cost of mating for males is substantial, male mate rejection does not always evolve. Crown Copyright ! 2010. Published on behalf of The Association for the Study of Animal Behaviour by Elsevier Ltd. All rights reserved.

Male mating preference is associated with risk of pre-copulatory cannibalism in a socially polymorphic spider

We performed male attraction experiments and staged courtship sequences to test for non-random mating with respect to social behavioral phenotype in the comb-footed spider, Anelosimus studiosus. While asocial behavior is the dominant phenotype in all A. studiosus populations examined to date, a social phenotype approaches a frequency of 15% in colder environments. We collected test subjects from higher latitude polymorphic populations and scored all individuals as to their behavioral phenotype prior to their use in these trials. Males of both phenotypes differentially approached and courted social females over asocial females and no-spider controls. By offering males different numbers of females of one type vs. the other in subsequent trials, we determined that the difference in attractiveness between the two phenotypes social/asocial is 1.5/1. Both the web produced by a female and a female that has been removed from its web attract males. We suggest that the male attracting pheromone is present on females and is also attached to silk threads. Staged encounters completed between males and females of the respective phenotypes demonstrated that courting males suffer significantly less pre-copulatory sexual cannibalism with social females than with asocial ones, and thus, female social tendency is phenotypically linked to sexual aggression. We propose that the male preference for social females is adaptive because of the observed asymmetry in courtship success.

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.

Precopulatory sexual cannibalism in fishing spiders (Dolomedes triton): a role for behavioral syndromes

Precopulatory sexual cannibalism (predation of a potential mate prior to copulation) offers an extreme example of intersexual conflict, a current focus in behavioral ecology. The ‘aggressive-spillover’ hypothesis, posits that precopulatory sexual cannibalism may be a nonadaptive by-product of a general syndrome of voracity (aggression towards prey) that is expressed in multiple behavioral contexts. In this view, selection favoring high levels of voracity throughout ontogeny spills over to cause sexual cannibalism in adult females even when it is not necessarily beneficial. Using the North American fishing spider, Dolomedes triton, we present the first in depth test of this hypothesis. We found support for three aspects of the spillover hypothesis. First, voracity towards hetero-specific prey results in high feeding rates, large adult size, and increased fecundity. Second, juvenile and adult voracity are positively correlated (i.e., voracity is a consistent trait over ontogeny). Third, voracity towards hetero-specific prey is indeed positively correlated with precopulatory sexual cannibalism. Assays of antipredator behavior further revealed positive correlations between boldness towards predators, voracity and precopulatory sexual cannibalism. Overall, our results support the notion that precopulatory sexual cannibalism in D. triton is part of a behavioral syndrome spanning at least three major contexts: foraging, predator avoidance, and mating.

Cohabitation of juvenile females with mature males promotes sexual cannibalism in fishing spiders

Precopulatory sexual cannibalism, or female predation of a potential mate before mating, illustrates an extreme intersexual conflict. Unlike sexual cannibalism occurring after mating, precopulatory sexual cannibalism cannot be construed as a male strategy. Thus, research on the adaptive significance of this phenomenon has focused on female benefits. In the present study, I test the idea that precopulatory sexual cannibalism represents an adaptive female trade-off between the material costs and benefits of mating with a male (forgoing food, securing sperm) and preying on a male (forgoing sperm, securing food). I pay particular attention to the rarely tested prediction that precopulatory sexual cannibalism by virgin females should increase as each female’s expectation of future mating opportunities increases. I use the phenomenon of cohabitation between adult males and juvenile females nearing sexual maturity as a means to manipulate female expectation of future mate availability. Results indicate that feeding on a male has significant positive effects on several measures of female fecundity. However, the likelihood of precopulatory attacks was not explained by a female’s recent feeding history. Finally, as predicted, juvenile female cohabitation with mature males (expectation of future mating opportunities) heightens the prevalence of precopulatory attacks by virgin females, suggesting that juvenile experience can alter a female’s propensity for sexual cannibalism. This is the first study to suggest that juvenile experience can alter a female’s propensity for sexual cannibalism. This finding emphasizes the point that studies of sexual selection and mating systems need to consider the effects of juvenile experience on adult behavior. Key words: adaptive foraging, fishing spiders, juvenile experience, male-female cohabitation, precopulatory sexual cannibalism. [Behav Ecol]

Sexual cannibalism in fishing spiders (Dolomedes triton): an evaluation of two explanations for female aggression towards potential mates

I manipulated food availability in juvenile and adult fishing spiders (Dolomedes triton) to test two hypotheses for sexual cannibalism. The adaptive foraging hypothesis posits that sexual cannibalism is an economic, adaptive foraging strategy on the part of the adult female. In contrast, the aggressive-spillover hypothesis suggests that precopulatory sexual cannibalism is misplaced aggression favoured in previous life-history phases. Several results indicated support for the adaptive foraging hypothesis. First, increased adult food availability produced marginally nonsignificant fecundity benefits in female's first egg sacs and highly significant fecundity benefits in female's second egg sacs. Second, while consumption of a male did not result in more offspring in either egg sac, it did significantly increase the probability a female would successfully hatch an egg sac. Finally, mating trials revealed mixed support for the adaptive foraging hypothesis as, for the most part, female mating behaviour (attack or mate) was not determined by the adaptive value a male represented (food item or sperm donor). Specifically, the likelihood of a precopulatory attack was not determined by male size, date (an indirect estimate of male availability) or female nutrient load. However, mated females did tend to attack courting males more often than virgin females. The aggressive-spillover hypothesis was supported by several findings. For juveniles, food availability had a significant positive effect on fixed female size (cephalothorax area at final moult) which, in turn, had a significant positive effect on fecundity. Thus, the spillover hypothesis' assertion that strong fecundity selection acts on juvenile feeding and fixed adult size was supported. The possibility that the spillover and adaptive foraging hypotheses are not mutually exclusive is discussed, especially in light of the presence of high levels of sexual cannibalism both before and after mating.