Mate with the young, kill the old: reversed sexual cannibalism and male mate choice in the spider Micaria sociabilis (Araneae: Gnaphosidae)

Female mate choice is regarded as a strong selective force that significantly affects male mating success. In extreme cases, mate rejection can result in sexual cannibalism. However, males may choose between their partners as well. The killing of potential female mates, i.e. reversed form of sexual cannibalism, may be related to male mate choice. We examined male mate choice in the spider Micaria sociabilis, focusing on the roles of female mating status (virgin/mated), size and age. Reversed cannibalism reached its highest frequency in the period of generation overlap, i.e. when young males from the summer generation met old(er) females from the spring generation. These results suggest discrimination against old(er) females. The frequency of cannibalism was not affected by female mating status or female size. However, larger males from the summer generation were more cannibalistic than smaller males from the spring generation. We conclude that reversed sexual cannibalism might be an adaptive mate choice mechanism and can be explained in the context of the aggressive spillover hypothesis.     

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.     

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.     

Mate attraction by females in a sexually cannibalistic praying mantis

We studied mate attraction by females of the praying mantid, Tenodera aridifolia sinensis, testing honest signaling of mate availability versus deceptive signaling to attract males for sexual cannibalism. We experimentally varied female diet and mating history and measured the rate of attraction of a wild population of males to caged females. Honest signaling theory predicts that virgin females will attract males at the greatest rate whereas deceptive signaling predicts that hungry females (which are more likely to cannibalize males) will attract more males, particularly among non-virgin females. Our results show that hungry females did not attract more males than well-fed females. Indeed, the opposite was true: hungry females attracted significantly fewer males. Moreover, hungry females were no more likely than well-fed females to attract males subsequent to mating, and mated females attracted males at a lower rate than did virgin females. We also observed female T. aridifolia sinensis and male Mantis religiosa arriving at the caged females and we discuss the significance of these observations. The results refute the hypothesis of deceptive signaling and show that mate attraction signals of female T. aridifolia sinensis are honest indicators of female mate availability and a lower risk of sexual cannibalism.     

Mate quality,not aggressive spillover,explains sexual cannibalism in a size-dimorphic spider

Sexual cannibalism particularly before mating is costly for the male victim but also for the female aggressor if she risks remaining unmated. The aggressive spillover hypothesis explains the persistence of this behavior as a maladaptive side effect of positive selection on aggressiveness in a foraging context. The hypothesis predicts that the occurrence of sexual cannibalism is explained by female aggressiveness but is not related to male phenotype or behavioral type. An alternative hypothesis invokes sexual selection and makes the opposite prediction namely that sexual cannibalism is an expression of female choice and should hence mainly target males of low quality. We tested the above hypotheses on a sexually dimorphic nephilid spider Nephilengys livida, known for male monopolization of females via genital damage, female genital plugging, and mate guarding, by staging mating trials during which we recorded mating behaviors and occurrences of pre- and postcopulatory cannibalism. We did not restrict assessment of aggressiveness to the mating and foraging context but also included aggression against same sex conspecifics. To assess female personalities, i.e., consistent individual differences in behavior including aggressiveness, we repeatedly tested them for intra-sex aggression, voracity towards prey, locomotory activity, and boldness. Females exhibited consistent differences in intra-sex aggressiveness, latency to attack prey, and boldness. Aggressive females had shorter latencies to attack prey and were more active than non-aggressive ones. In contrast to the predictions of the aggressive spillover hypothesis, females that were aggressive towards prey and towards other females were not more likely to attack a male than non-aggressive females. In support of the mate choice hypothesis, less aggressive males were more likely attacked and cannibalized than more aggressive ones. This hints at sexual selection for aggressiveness in males and raises the question of mechanisms that maintain variation in male aggressiveness.     

Sexual cannibalism facilitates genital damage in <Emphasis Type="Italic">Argiope lobata</Emphasis> (Araneae: Araneidae)

Sperm competition is a potent driving force in evolution leading to a remarkable variety of male adaptations that prevent or reduce fertilization by rivals. An extraordinary defensive strategy against sperm competition has evolved in a number of web spiders where males break off parts of their paired genitalia in order to obstruct the copulatory openings of females (mating plug). A recent comparative analysis on the family level reports that genital damage is most frequent in species with sexual cannibalism although, as yet, a functional association between sexual cannibalism and genital damage has not been found. Using the moderately sexually cannibalistic orb-web spider Argiope lobata, we show for the first time that males cannibalized during their first copulation damaged their pedipalps with significantly higher probability (74%) than males that escaped (15%). Of all males that damaged their genitalia, 44% were able to place a genital fragment inside the copulatory opening of the female, resulting in a relatively low total plugging rate of 14%. Successful obstruction of the female copulatory opening reduced the share of paternity of subsequent males (P ₂ = 0.06%), thus, indicating that genital damage may have evolved as a response to sperm competition in this species as well. However, the low incidence of successful plugging and the strong relationship between sexual cannibalism and genital damage suggest that apart from paternity protection, the nature of genital damage in A. lobata is further shaped by sexual conflict or cryptic female choice.     

Mate choice,fecundity and sexual dimorphism in two pipefish species (Syngnathidae)

Summary In order to understand the causes of sexual dimorphism, mate choice and size-related fecundity were studied in two pipefish species, Syngnathus typhle and Nerophis ophidion. Sexual dimorphism is more pronounced in N. ophidion; females are larger, have sexual colourings, and are more active during courtship. In S. typhle the sexes are alike in all these respects. Males brood their offspring in both species. In N. ophidion fecundity was positively correlated with both body size and the amount of sexual colouring in females. In males no correlation between body size and fecundity, or between body size and embryo size existed. Predictably, in mate choice experiments with equal-sized females, males chose females with more extensive sexual colourings. We explain sexual dimorphism in this species as a consequence of both natural selection (fecundity increases with size in females but not in males) and sexual selection (males prefer larger females). We argue that sexual size dimorphism did not evolve by selection minimizing overlap in food niches between the sexes, because food production is high in the Zostera beds where the fishes live, and no size dimorphism was found in the sympatrically occurring S. typhle. Furthermore, in N. ophidion dimorphism is not greater in a particular mouth character than in overall body size. In S. typhle egg size and the average number of eggs transferred per spawning were positively correlated with female body size. Apparently more energy per offspring was provided by larger males than by smaller males, and larger males also carried more offspring. As predicted, large mates were preferred by both sexes in mate choice experiments. This is explicable in terms of both natural selection (fecundity increases with size in both sexes) and sexual selection (both sexes prefer large mates). As a consequence of selection acting in the same direction in both sexes, sexual dimorphism is absent in S. typhle.     

Fitness consequences of sexual cannibalism in female<Emphasis Type="Italic"> Argiope bruennichi</Emphasis>

The evolution of sexual cannibalism as the most extreme form of nuptial feeding is still poorly understood. Although increasing evidence suggests that female aggressiveness is related to other aspects of foraging behaviour, it is not clear whether the nutritional value of a male is sufficient to provide an adaptive significance for sexual cannibalism. A widely cited though rarely tested explanation is based on a paternal investment model, and predicts that consumption of a male results in increased female fecundity. The available evidence is either correlational or restricted to species with relatively large and potentially nutritious males, and different studies have come to different conclusions. Here we present a test of the paternal investment hypothesis using the very cannibalistic and highly size-dimorphic spider Argiope bruennichi. After a preset schedule, we had females consume none, one or two males independent of the female's cannibalistic behaviour. Consumption of male bodies did not result in any detectable fitness benefit for the female: neither the number of clutches, nor clutch size or hatching success were affected by consumption of males. The frequency of cannibalism was around 80%, independent of the female mating status. We did not observe male complicity, but cannibalism was associated with prolonged copulation. This suggests a sexually selected benefit of cannibalism for males. We conclude that the paternal investment hypothesis does not explain the existence of sexual cannibalism in A. bruennichi and probably not in other spider species with a pronounced sexual size dimorphism.Communicated by L. Simmons     

Sex ratios,mating behavior and sexual size dimorphism of the northern water snake,Nerodia sipedon

Competition among males to mate is generally associated with male-biased size dimorphism. In this study we examine mating behavior in the northern water snake (Nerodia sipedon), a species in which males are much smaller than females despite substantial competition among males to mate. Competition among males was a consequence of a male-biased operational sex ratio due to slightly higher female mortality from a birth sex ratio of 1 : 1, and, in 1 year, more synchronous and longer mating activity by males. Approximately one-third of both males and females appeared not to mate in a given year. Larger males were generally more likely to attempt mating, but size did not explain the variance in the number of aggregations in which individual males participated. Within aggregations, males that were successful at achieving intromission were larger than unsuccessful males in 1 of 2 years. Variation in condition (mass relative to length) and relative tail length were not generally useful predictors of either mating effort or success in males. Because large size was often advantageous to males, sexual size dimorphism appeared not to be a consequence of sexual selection favoring smaller males. Because sexual dimorphism was evident at birth, and both males and females matured sexually at about 4 years, sexual dimorphism was not simply a consequence of one sex growing at the maximum rate for longer. Female fecundity increased with size, and sex differences in size-fecundity relations may underly the pattern of sexual size dimorphism. However, because multiple mating by females is common, sperm competition is likely to be important in determining male reproductive success. Therefore, allocation of energy to sperm rather than growth may also prove to be an important influence on male growth rates and sexual size dimorphism.     

Body size and sexual selection in the koala

Sexual selection is often characterized by polygynous breeding systems, size dimorphism, and skewed operational sex ratios. Koalas are sexually dimorphic in multiple domains, yet are absent from the literature on sexual selection and the structure of their mating system is unclear. We provide the first documentation of the strength of sexual selection in koalas by using microsatellite markers to identify sires. We combine the genetic data with morphological data in order to assess the role of body size in regulating reproductive output. During our 4-year study, 37% of males were identified as possible sires. Males were significantly larger than females, with sires heavier than non-sires. Male body mass correlated with annual reproductive output, with Crow’s Index of Opportunity for Selection revealing that variation in male reproductive success was threefold higher than that of females. Since it appears that male koalas rarely engage in physical confrontations over access to females, size dimorphism could be based upon non-agonistic competition and/or female mate choice. We propose that size dimorphism in koalas evolved as a consequence of endurance rivalry promoting vocal sexual advertisements that attract females. We suggest that female choice is a key mediator of male reproductive output.     

Pre-copulatory sexual selection in the cigarette beetle Lasioderma serricorne

Traditional concepts of sexual selection and sexual conflict make different predictions about the costs and benefits to females of exposure to males with higher mating success. The traditional concepts of sexual selection assume that females benefit from their mate choices, whereas sexual conflict assumes that the females suffer greater costs by mating with males who have greater mating success and thus reduce their fitness. In order to understand how mate choice evolves, it is necessary to estimate the overall effect of mate choice on female fitness. However, relatively few studies have conducted that investigation. In this study, we investigated the direct and indirect effects of mating with attractive males on the fitness of females in the cigarette beetle Lasioderma serricorne. Mating with attractive males increased the number of female offspring but did not affect female longevity. Additionally, we found evidence that attractive males sire highly attractive sons. Thus, mating with an attractive male provides direct and indirect benefits but no fitness cost to female L. serricorne.     

Mate availability accelerates male filial cannibalism in a nest brooding fish: effects of number and fecundity of females

Theoretical models predict that increased mate availability accelerates filial cannibalism by the parental male, but we do not yet fully understand how the various aspects of mate availability contribute to this effect. We examined the effects of two elements of mate availability—female fecundity and sex ratio—on filial cannibalism by the lizard goby, Rhinogobius flumineus, which is a paternal nest brooding fish. We used three types of females (stimulus-females): a single female with slim belly (not ready to spawn), a single gravid female (ready to spawn), and two gravid females. Stimulus-females were housed in a transparent cage and shown to subject males just before and after spawning with a separate female, after which males cared for the brood. A single gravid stimulus-female accelerated filial cannibalism, compared with a control-stimulus consisting of an empty cage, but only during the early care period. In contrast, a single slim-bellied stimulus-female did not accelerate cannibalism. A stimulus of two gravid females accelerated cannibalism to the same degree as a single gravid female stimulus. Our results suggest that in lizard gobies, filial cannibalism by parental males is accelerated by female quality (fecundity) in the early care period, but not by a higher number of available females (sex ratio).     

Intersexual dominance relationships and the influence of leverage on the outcome of conflicts in wild bonobos (Pan paniscus)

Dominance relationships between females and males are characteristic traits of species and are usually associated with sexual dimorphism. Exploring the social and contextual circumstances in which females win conflicts against males allows one to study the conditions triggering shifting power asymmetries between the sexes. This study investigates dominance relationships in bonobos (Pan paniscus), a species in which females are thought to display social dominance despite male-biased sexual dimorphism. To identify dominance relationships among females and males, we first explored how intrasexual dominance status affects the outcome of intersexual conflicts. Second, by incorporating social and behavioral information about the context of intersexual conflicts, we tested to which extent different components of power are relevant to the observed asymmetries in the relationships. Post-hoc analyses indicate a sex-independent dominance hierarchy with several females occupying the top ranks. Our results also reveal that two factors—female leverage and motivation to help offspring—had a significant influence on the outcome of intersexual conflicts. The results of our study do not indicate an overall reduction in male aggression against females but do show lower levels of male aggression in the mating context, and an absence of male aggression toward those females displaying visual signs of elevated fecundity. This indicates that both female sexuality and male mating strategies are involved in the shifting dominance relationships between the sexes.     

Is sexual monomorphism a predictor of polygynandry? Evidence from a social mammal, the collared peccary

Sexual dimorphism is common in polygynous species, and there is clear evidence that both intra-sexual competition and female preferences can drive the evolution of large body size in males. In contrast, sexual monomorphism is often argued to reflect a relaxation of male mate competition or an intensification of resource competition among females. Alternatively, it might imply opportunities for females to circumvent or counteract male mate competition in a polygynandrous mating system. We test the prediction that sexual monorphism is associated with polygynandry in the collared peccary (Pecari tajacu, Tayassuidae), a social ungulate closely related to the old-world suids. The genetic mating system in the Tayassuidae is unknown, but its sexual monomorphism presents a striking contrast to the strong size dimorphism found in most Suidae, so that a departure from the polygynous system common in Suidae would be noteworthy. We characterized genetic relationships among adults within herds in three geographically distinct populations, assigned parents to 75 offspring, and tested for skew in individual reproductive success. Parentage assignment data indicated that multiple males sire offspring within a herd, and in the population for which genetic data were most complete, 19% of parentage assignments were potentially sired by extra-herd males. Some litters have multiple sires, and neither males nor females monopolized reproduction, even in small herds. This result supports our prediction and suggests that sexual monomorphism may either select for or be an evolutionary consequence of a promiscuous mating system.     

Age-related female mating decisions are condition dependent in wolf spiders

Female mating behaviors are known to be sensitive to a variety of individual factors both external and internal to a female; however, mating decisions are likely due to a suite of interacting factors. By independently manipulating female and male diet in the wolf spider Rabidosa rabida and testing females across age groups, we demonstrate that, in addition to its independent effect, female nutritional condition interacts with female age to influence female mating behavior. Overall, high-quantity diet (HD) females were more likely to mate than low-quantity diet (LD) females. Within the LD females, older individuals were more likely to mate than younger individuals, while within HD females, mating probabilities were equal across females of different age classes. With respect to mate choice, only female age influenced the likelihood of mating based on male diet. Young females were choosier as they were more likely to mate with HD males than LD males; in contrast, older females were equally likely to copulate with males of each diet treatment. In addition, the likelihood of pre-sexual cannibalism was dependent on both female and male diet. High-quantity diet females were more likely to cannibalize than LD females, and attacks were directed towards LD males most often. We discuss our results in terms of costs versus benefits of female mate choice.     

Experience with chemotactile cues indicating female feeding history impacts male courtship investment in the wolf spider <Emphasis Type="BoldItalic">Schizocosa ocreata</Emphasis>

Male fitness is often determined by the ability of the male to gain access to multiple mates, although in species that exhibit sexual cannibalism, males might increase their likelihood of being cannibalized with each encounter. This risk should create selection for males who are able to perceive potential risks associated with mating encounters. We studied male Schizocosa ocreata wolf spiders to determine whether they use female chemotactile cues (silk, excreta) as indicators of potential risks and how these cues affected subsequent male courtship behaviors. Female treatments included satiated females vs. starved females, as well as a treatment where females had recently cannibalized a male S. ocreata. We performed experiments to assess (1) if males use female chemotactile cues to determine potential risks associated with differing female feeding treatments and alter courtship investment, and 2) how male experience with female chemotactile cues affected courtship investment in subsequent female encounters. At first encounter, males do not vary courtship investment (number of bouts, duration, and vigor) with different female feeding treatments. However, male behaviors during subsequent encounters with female chemotactile cues varied in complex ways, depending on female feeding treatment and male first encounter experience. These data suggest that male experience impacts perception of female chemical cues and offers the male opportunity to avoid sexual cannibalism in high-risk situations.     

Influence of alternate reproductive tactics and pre- and postcopulatory sexual selection on paternity and offspring performance in a lizard

Sexual selection theory predicts different optima for multiple mating in males and females. We used mating experiments and genetic paternity testing to disentangle pre- and postcopulatory mechanisms of sexual selection and alternate reproductive tactics in the highly promiscuous lizard Eulamprus heatwolei. Both sexes mated multiply: 30–60 % of clutches were sired by two to four fathers, depending on the experiment. Larger males sired more offspring when we allowed male contest competition: 52 % of large males but only 14 % of small males sired at least one offspring. In the absence of male contest competition, females mated promiscuously and there was no large male advantage: 80 % of large males and 90 % of small males sired at least one offspring, and there was no evidence for last-male precedence. Multiple mating did not yield obvious direct or indirect benefits to females. E. heatwolei represents a complex system in which males attempt to improve their fertility success by limiting rivals from access to females and through adopting alternate reproductive tactics. Conversely, females exhibit no obvious precopulatory mate choice but may influence fitness through postcopulatory means by either promoting sperm competition or through cryptic female choice. Our results support the hypothesis that female multiple mating in nonavian reptiles is best explained by the combined effect of mate encounter frequency and high benefits to males but low costs to females.     

A female preference for experienced males in the almond moth, Cadra cautella

Male mating status can affect female reproductive output if male ejaculate investment declines over consecutive matings. Accordingly, females are predicted to mate preferentially with virgin males. In mildly polyandrous lepidopterans, female fitness is less affected by reduced male investment than in more polyandrous species, and so the predictions for female mating preferences are less clear. We examined female mating preferences in the mildly polyandrous almond moth, Cadra cautella, in which ejaculate size does not affect female reproductive output. First, we allowed females to mate with virgin or once-mated males, in which the males were presented individually or simultaneously. We recorded the latency to mating and, in the case of the simultaneously presented trials, the identity of the successful, copulating male. We found that females mated more frequently with mated males (when simultaneously presented with both males), yet females did not differ in the time taken to initiate copulation with any male. We further examined if this mated male advantage was due to differential mate detection or locomotory behaviour of the male treatments. We tested the ability of virgin and mated males to locate a receptive female within a wind tunnel using long-distance pheromone cues and recorded their activity budget. We found no difference in the ability of mated or virgin males to locate or approach a receptive female, or in their activity levels. These data suggest a female preference for mated males in this species, a preference that may minimise other potential costs of mating.     

The effects of mating system on male mate choice in a coral reef fish

Summary We show how mate limitation appears to be critical in determining whether or not males exercise mate choice among available females. Thalassoma bifasciatum is a Caribbean reef fish with two distinct mating patterns: group-spawning and pair-spawning. In both mating systems, female fecundity is variable and size dependent, and female availability is high. However, sperm competition among group-spawning males apparently limits the number of effective matings in which a male may engage, whereas territorial pair-spawning males have little or no such limitation. Group-spawning males should be discriminating in their choice of mates and our data confirm this: there is strong evidence for assortative mating in group-spawns, with more large males joining in mating groups around large females. In contrast, pair-spawning males show no indication of mate preferences, and spawn with all females who arrive at their territories.     

Polyandrous female butterflies forage for matings

Butterfly mating systems exhibit great variation and range from strict monandry to strong polyandry. During mating males transfer ejaculates containing both sperm and accessory substances to females. In the polyandrous green-veined white butterfly, Pieris napi (Lepidoptera, Pieridae) these ejaculates average 15% of male body mass, but can represent up to 23% of body mass for individual males. Hence, mating is costly to males, and recently mated males increase copula duration but decrease ejaculate mass transferred to females. Substances transferred to females during mating are later incorporated into female soma and reproductive tissues, and multiply mated female butterflies have higher lifetime fecundity, lay proportionately larger eggs, and live longer compared to once mated females. Here we report that females of P. napi allowed to mate at liberty with recently mated males only (i.e. males that delivered a small ejaculate) increased their lifetime number of matings compared to females allowed to mate with virgin males only (i.e. males that delivered large ejaculates), the former group mating on average 5.1 times (range 2–10) and the latter group mating on average 2.8 times (range 1–4). The lifetime fecundity of the two groups of females did not differ significantly. Because nutrient donation from males is essential for females to realize their potential fecundity, we conclude that females of the polyandrous green-veined white actively forage for matings.