Pre-copulatory Cannibalism Research Articles

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.

Increased male mating success in the presence of prey and rivals in a sexually cannibalistic mantis

Abstract Precopulatory sexual cannibalism—or cannibalism without mating—is expected to promote the evolution of male strategies that enhance mating success and reduce the risk of cannibalism, such as preferentially approaching feeding females. Sexual selection on male competitiveness has the potential to alter male mating decisions in the face of cannibalism risk, but such effects are poorly understood. We investigated the effect of prey availability and male–male competition on mating incidence in the highly cannibalistic Springbok mantis, Miomantis caffra. We found that matings were initiated more rapidly and more often in the presence of prey, suggesting that females distracted with foraging may be less of a threat. Competition between males also hastened the onset of copulation and led to higher mating success, with very large effects occurring in the presence of both prey and competitors, indicating that intrasexual competition may intensify attraction to foraging females. Taken together, our results suggest that precopulatory cannibalism has selected for male preference for foraging females and that males adjust their mating strategy to both the risk of competition and the threat of cannibalism.

Black widows as plastic wallflowers: female choosiness increases with indicators of high mate availability in a natural population

Female choice is an important driver of sexual selection, but can be costly, particularly when choosy females risk remaining unmated or experience delays to reproduction. Thus, females should reduce choosiness when mate encounter rates are low. We asked whether choosiness is affected by social context, which may provide reliable information about the local availability of mates. This has been demonstrated in the lab, but rarely under natural conditions. We studied western black widow spiders (Latrodectus hesperus) in the field, placing experimental final-instar immature females so they were either ‘isolated’ or ‘clustered’ near naturally occurring conspecifics (≥10 m or ≤1 m, respectively, from a microhabitat occupied by at least one other female). Upon maturity, females in both treatments were visited by similar numbers of males, but clustered females were visited by males earlier and in more rapid succession than isolated females, confirming that proximity to conspecifics reduces the risk of remaining unmated. As predicted, isolated females were less choosy in staged mating trials, neither rejecting males nor engaging in pre-copulatory cannibalism, in contrast to clustered females. These results demonstrate that exposure of females to natural variation in demography in the field can alter choosiness of adults. Thus, female behaviour in response to cues of local population density can affect the intensity of sexual selection on males in the wild.

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.

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.

Male courtship vibrations delay predatory behaviour in female spiders

During courtship, individuals transfer information about identity, mating status and quality. However, male web-building spiders face a significant problem: how to begin courting female spiders without being mistaken for prey? Male Argiope spiders generate distinctive courtship vibrations (shudders) when entering a female's web. We tested whether courtship shudders delay female predatory behaviour, even when live prey is present in the web. We presented a live cricket to females during playbacks of shudder vibrations, or white noise, and compared female responses to a control in which we presented a live cricket with no playback vibrations. Females were much slower to respond to crickets during playback of shudder vibrations. Shudder vibrations also delayed female predatory behaviour in a related spider species, showing that these vibrations do not simply function for species identity. These results suggest that male web-building spiders employ a phylogenetically conserved vibratory signal to ameliorate the risk of pre-copulatory cannibalism.

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.

Trade-off between pre- and postcopulatory sexual cannibalism in a wolf spider (Araneae, Lycosidae)

Sexual cannibalism can occur before, during or after mating. Relatively few experimental studies have examined why there is variation in the timing of sexual cannibalism. We examined the latency and number of attacks required for female spiders to capture male spiders pre- vs. postcopulation. We also examined the effects of female mating status and hunger level on the occurrence of pre- and postcopulatory cannibalism, which reflects the contribution of both relative capture success and female motivation to cannibalize males. Precopulatory cannibalism occurred after a shorter interval and required fewer chases and physical interactions for the female to successfully capture the male than was the case for postcopulatory cannibalism. Virgin females were more likely to engage in postcopulatory rather than precopulatory cannibalism and mated females vice versa. Those virgin females that did engage in precopulatory cannibalism had significantly lower body condition than virgin females engaging in postcopulatory cannibalism. While precopulatory cannibalism occurred more quickly and required fewer attacks by females, it comes at a potential cost of not mating with males. Hence, females are more likely to engage in precopulatory cannibalism if they have already mated or, if virgins, if they have low body condition. These results indicate that the decision of when to cannibalize males is dynamic and depends upon the relative value of a male as a mate versus a meal.

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.

Prior encounters with the opposite sex affect male and female mating behavior in a wolf spider (Araneae, Lycosidae)

Mate availability can vary widely in nature depending upon population density and sex ratio and can affect the ability of individuals to be selective in mate choice. We tested the effects of prior encounters with the opposite sex (i.e., exposure to the opposite sex either with or without mating) on subsequent mating behavior in two experiments that manipulated mate availability for both males and females in the wolf spider, Hogna helluo. The probability of mating in the experimental trial depended upon whether the prior encounter involved mating or not, and males and females responded in opposite directions. Exposure without mating resulted in a higher subsequent frequency of mating for females and a lower subsequent frequency of mating for males, while prior mating experience resulted in a lower frequency of female remating and a higher frequency of male remating. Prior exposure without mating did not affect female aggression. However, mated females engaged in precopulatory cannibalism more frequently than virgins. Mated males escaped postcopulatory cannibalism more frequently than virgins. Our results show that males respond to exposure without mating in the expected manner. However, prior mating (1 week earlier) had unexpected effects on males, which may be due to mated males being of higher quality. There were little or no effects of the size of the prior exposure individual or mate on subsequent mating behaviors. Further research is needed to determine why different species use different degrees of prior information in mate choice.

Seismic signals are crucial for male mating success in a visual specialist jumping spider (Araneae: Salticidae)

The diversity of courtship displays throughout the animal kingdom is immense and displays can range from seemingly simple, to incredibly complex. Signallers often possess elaborate morphological adaptations for signals directed at a specific sensory modality in receivers. In some cases, these signals are so compelling to human observers, the possibility that important signals exist in other sensory modalities is ignored, potentially resulting in an incomplete characterization of the communication system. Jumping spiders (Salticidae) have remarkable visual capabilities. Yet one species, Habronattus dossenus, has recently been shown to have a complex repertoire of multicomponent seismic courtship signals in addition to and produced in concert with its multiple visual ornaments and movement displays. Here, we demonstrate the importance of these seismic signals in the courtship display of H. dossenus by comparing mating frequencies across experimentally manipulated treatments. Virgin females were paired with males from one of two experimental groups: nonmuted males or muted males. We found that females were significantly more likely to copulate with nonmuted males than with muted males. Furthermore, in all pairs that copulated, the latency to copulation was significantly shorter in nonmuted pairings than in muted pairings and precopulatory cannibalism rates were significantly lower. These results demonstrate that seismic signals are a critical component of male H. dossenus courtship displays. Additionally, we demonstrate that many other Habronattus species include a diversity of seismic signals in their courtship displays and we discuss potential selection pressures that may drive the evolution of multimodal displays even in species that already possess elaborate morphological adaptations for signals directed at one sensory modality.

A test of sexual cannibalism models, using a sit-and-wait predator

Sexual cannibalism, the capture and consumption of one sex by the other resulting from sexual interactions, provides an intriguing set of conditional fitness payoffs. Usually these payoffs will only benefit the cannibal, but under certain circumstances advantages might accrue to the cannibalized individual as well. Here I test three models of sexual cannibalism with data from a sit-and-wait predator, the crab spider Misumena vatia, whose lifestyle differs from the species for which these models were generated. The models include both precopulatory mechanisms (no gametes exchanged) and postcopulatory ones (gametes exchanged) perceived to generate adult fitness payoffs and situations in which cannibalism is not adaptive in the adult stage (aggressive spillover). In M. vatia, females sometimes cannibalize males before mating can occur. Precopulatory cannibalism is unlikely to reward female M. vatia significantly because of the diminutive size of the males, but it could be part of a broader syndrome that provides the females with large food payoffs earlier in the life cycle. Although the frequency of cannibalism is low (3.8–7.6%), this level suffices to be an important selective factor, a point accentuated by the extremely cautious behaviour of the males toward the females. I then compare the traits associated with these models to the species for which they were designed and certain others for which adequate data also exist. None of the sets of responses to these traits closely resembles each other in the different species. These results suggest that sexual cannibalism has developed in response to a heterogeneous collection of lifestyles and phylogenetic constraints. © 2004 The Linnean Society of London, Biological Journal of the Linnean Society, 2004, 81, 427–437.

Costs of courtship and mating in a sexually cannibalistic orb-web spider: female mating strategies and their consequences for males

The costs of courtship and mating may include increased risks of predation, the transmission of pathogens, and a loss of foraging opportunities. Thus, a female's decision to tolerate a courting male will depend upon how these costs offset the benefits of mating, which will depend on her reproductive and nutritional status. While these costs may be similar for mated and unmated females, the benefits of mating will be less for mated than virgin females. However, the cost of lost foraging opportunities may be higher for females with fewer nutritional reserves necessary for forming eggs. We examined how these costs and benefits influence the courtship and mating behaviour of male and female orb-web spiders, Argiope keyserlingi. In the field, females on webs that also contained a courting male intercepted fewer prey items per hour than females on webs without a male. In the laboratory, the presence of a courting male at the hub also attracted mantid predators to the web, increasing the risk of predation for both male and female. Staged mating experiments in the laboratory revealed that the frequency of female attacks and pre-copulatory cannibalism was greater among mated than virgin females. Feeding history did not affect aggression in virgin females but, among mated females, food-deprived spiders attacked and cannibalized males more frequently than sated females and only the latter ever remated. These differences in female behaviour influenced male mating strategies. Choice experiments demonstrated that males preferred to venture onto the silk threads of virgin rather than those of mated females. Similar patterns of mate selectivity were observed in the field; females with narrow abdomens attracted more males to the webs than females with broad abdomens, and copulations were observed more frequently among females with narrow abdomens. These smaller females are likely to be virgins that have recently molted. Males that preferentially mate with virgin females will not only avoid potentially fatal attacks but also obtain, on average, a higher fertilization success.