The Evolution of Sexual Cannibalism
Kenwyn Blake Suttle
Sexual cannibalism is a special case of cannibalism in which a female organism kills and consumes a conspecific male before, during, or after copulation. Although other forms of cannibalism are widespread across animal classes (reviewed in Elgar and Crespi 1992), sexual cannibalism is a taxonomically rare phenomenon. It has been documented only in arachnids and insects (Polis 1981) and amphipods (Dick 1995), although anecdotal evidence suggests its existence in gastropods and copepods as well (Elgar 1992). Despite its overall rarity, sexual cannibalism is common in many families of spiders and scorpions, and can have important effects on population size (Zimmerman and Spence 1992), sex ratio (Hurd et al. 1994), and even persistence (Vandewalle 1997).
Most of the empirical research investigating sexual cannibalism has been done with spiders and scorpions, because of the relative prevalence of the interaction in these two orders. Within spiders and scorpions, sexual cannibalism takes many different forms with respect to the role and behavior of each sex, the potential benefit to each sex, and the timing in the courtship/copulatory sequence (Elgar 1991; Sasaki and Iwahashi 1995; Andrade 1996; Elgar and Babette 1996; Arnqvist and Henriksson 1997; Andrade 1998; Maxwell 1998). Due to these differences, researchers have proposed many pathways for its evolution, often invoking contradicting sets of selective forces acting on different sexes and different species. With several conflicting models and an increasing number of empirical studies attempting to explain its origin and maintenance in insects and arachnids, the evolution of sexual cannibalism remains a subject of debate.
Reproductive strategies of males and females often differ, resulting in asymmetric costs of reproduction on the two sexes and a consequent conflict between the sexes (Schneider and Lubin 1998). A major impediment to understanding the evolution of sexual cannibalism concerns the fitness effects of sexual cannibalism on each sex (Thornhill 1976; Buskirk et al. 1984; Gould 1984; Newman and Elgar 1991; Arnqvist and Henriksson 1997; Johns and Maxwell 1997). It is easy to imagine the evolution of sexual cannibalism as an adaptive female strategy. Females can gain nutritional benefits and resulting increases in fecundity by consuming their mates (Elgar and Nash 1988; Newman and Elgar 1991; Hurd et al. 1994; Andrade 1998). Male complicity (i.e. suicide) is a more difficult scenario to reconcile, because in sacrificing their soma to females, males forfeit any future mating opportunities and subsequent fitness benefits. Male complicity has long been the focus of debate among proponents of different models for the evolution of sexual cannibalism.
The first investigations into the evolution of sexual cannibalism sought to elucidate the conditions under which the phenomenon would provide fitness benefits to both sexes (Thornhill 1976; Parker 1979; Buskirk et al. 1984). For males, sexual cannibalism may have evolved as an extreme form of paternal investment. If a male's sacrifice significantly increases the quality or quantity of his offspring, sexual cannibalism could be an adaptive male strategy, rather than the result of a conflict of interest between the sexes (Thornhill 1976; Parker 1979). In a formal treatment of the theoretical aspects of sexual cannibalism, Buskirk et al. (1984) described the life history conditions under which it would be selectively advantageous for males. This model predicts sexual cannibalism will be favored by natural selection when cannibalism significantly increases the number or viability of eggs fertilized by the cannibalized male's sperm, and when the expected number of matings over a male's lifetime is low. An obvious drawback to this model is that it only applies to situations in which cannibalism occurs after sperm transfer.
Many researchers have rejected the paternal investment hypothesis as a general explanation for the evolution of sexual cannibalism. Most evidence for male complicity is anecdotal (Gould 1984) and has not been borne out by experimental and behavioral research (Polis and Farley 1979; Breene and Sweet 1985; Birkhead et al. 1988; Arnqvist and Henriksson 1997; Maxwell 1998; Maxwell 1999). Even in species in which cannibalism is known to increase the number and/or viability of offspring (including mantids, black widow spiders, jumping spiders, and scorpions) males approach females cautiously and retreat quickly after copulation. Breene and Sweet (1985) showed that in the sexually cannibalistic black widow spider Latrodectus mactans, when males survive copulation, they often fertilize multiple females. Males of sexually cannibalistic species use diverse strategies to decrease their chances of being cannibalized: male scorpions sometimes sting the female after deposition of the spermatophore (Polis and Farley 1979); male black widows (Gould 1984) and crab spiders (Bristowe 1958) often restrain females in silk prior to copulation; certain tetragnathid spiders have specialized jaws that hold open the jaws of females during copulation (Bristowe 1958); many orb-weavers preferentially mate with females in ecdydis, when cannibalism is physically impossible (Robinson 1982); other orb-weavers (Robinson 1982) and a jumping spider (Suttle, personal observation) delay their courtship approach until a female catches another prey item. Furthermore, in many taxa, sexual cannibalism occurs before the transfer of sperm to the female, thus precluding the cannibalized male from any fitness advantage (Elgar 1992; Elgar and Fahey 1996; Arnqvist and Henriksson 1997).
Research has demonstrated male complicity in sexual cannibalism in two species of spider (Forster 1992; Sasaki and Iwahashi 1995; Andrade 1996; Andrade 1998). Males of the orb-web spider Argiope aemula fiercely resist being caught by females after their first palpal insertion (in most spiders, males transfer sperm to females by inserting one or both palpi into the female), often losing legs in their defense. However, males that survive the first palpal insertion usually re-approach the same female and nearly ninety percent are cannibalized without resistance during or after the second palpal insertion (Sasaki and Iwahashi 1995). The adaptive significance of this interaction has not been studied explicitly, but it is probable that cannibalized males copulate for a longer duration than surviving males, decreasing the access of neighboring males to the female and decreasing the female's chance of remating. The clearest case of male complicity to sexual cannibalism and the resulting fitness advantage conferred to males, occurs in males of the Australian redback spider Latrodectus hasselti. Males of this species always perform a somersault during sperm transfer that positions their abdomen directly over the mouthparts of females (Forster 1992; Andrade 1996). Cannibalism is dependent on the females' hunger level, and occurs in approximately sixty five percent of matings (Andrade 1998). When cannibalism does occur, it is always initiated while the male is in the somersault posture. Complicity in cannibalism results in two paternity advantages for this species: females that cannibalize their mates are less likely to mate again, and cannibalized males copulate longer and fertilize roughly double the eggs fertilized by those not killed during copulation. Interestingly, the mass of males is less than two percent that of females, so consumption of a male provides no increase in egg number or mass. Nonetheless, copulatory suicide is an adaptive strategy for males because of the paternity advantage it confers. Furthermore, the cost of cannibalism is very low for males, as their intromittent organs break off inside the female during copulation, and leave the male mortally wounded (Andrade 1996).
Despite demonstrable male complicity in A. aemula and L. hasselti, and the adaptive significance of sexual cannibalism in L. hasselti, it is unlikely that adaptive male complicity represents a general model for the evolution of sexual cannibalism, because of the prevalence of premating sexual cannibalism. Elgar and Nash (1988) proposed a model to explain the evolution of premating sexual cannibalism as a mechanism of mate rejection, or female choice. According to this hypothesis, females assess potential mates and then cannibalize or mate depending on phenotypic characteristics that vary among males of the species (body size in their study). Females should mate with larger males to produce larger offspring, assuming large body size indicates superior and heritable foraging abilities. Females should cannibalize smaller males to increase fecundity. Moreover, as the cost of sexual cannibalism is very high for females that remain unmated, females are predicted to alter their cannibalistic behavior according to encounter rates with males (Elgar and Nash 1988). This model was developed based on an empirical study of the garden spider Araneus diadematus, a species in which sexual cannibalism occurs before copulation. The model is inapplicable to species in which females cannibalize males during or after sperm transfer.
Another model attempting to explain cannibalism from the female perspective suggests cannibalism can evolve simply through foraging considerations (Newman and Elgar 1991). According to this "Economic" model, the two most important factors for the evolution of sexual cannibalism are ecological: the expected number of males encountered and the mass gained from other prey. Females are expected to cannibalize males when the male encounter rate is high and the mean food intake rate from other prey is low. When males are less abundant or less mobile, and alternative prey items are more abundant, cannibalism should decrease. Whether a courting male is accepted as a mate or cannibalized thus depends on his value to the female as a mate versus his value as a meal. A unique case of reversed sexual cannibalism, in which the male amphipod Gammarus pulex consumes female conspecifics, lends support to this theory (Dick 1995). In this species, males cannibalize newly moulted females, which simultaneously are ready for copulation and at their most vulnerable stage, at much lower rates than they cannibalize other conspecifics. However, as the abundance of other prey organisms decreases, the incidence of reversed sexual cannibalism increases, as is predicted by the Newman and Elgar "Economic" model of sexual cannibalism (1991).
All of the models thus far discussed consider sexual cannibalism in terms of its adaptive value to one or both sexes. An obvious assumption of each is that sexual cannibalism evolved and is maintained because of fitness benefits conferred to reproductive adults. It has recently been suggested, however, that as attempts to generalize the evolution of this phenomenon, these approaches may be barking up the wrong proverbial tree. Recent theory suggests that sexual cannibalism in adult organisms may result indirectly from behaviors that are adaptive in previous life history stages, but nonadaptive or even maladaptive in adults (Arnqvist and Henriksson 1997). Sexual cannibalism may carry over into the adult stage as a result of genetic constraints on life history aggression.
This model was developed to explain the evolution of sexual cannibalism in the fishing spider Dolomedes fimbriatus. In several members of this genus, males approach females very cautiously when courting, and flee rapidly after copulation. Consumption of males is a common behavior, yet it confers no fitness benefit to females and actually decreases fertilization rates (Spence et al. 1996; Arnqvist and Henriksson 1997). Sexual cannibalism in Dolomedes species thus does not conform to the assumptions or follow the predictions of any adaptive theory. Arnqvist and Henriksson (1997) suggest that sexual cannibalism need not be adaptive for either sex, and instead is a byproduct of strong selection for juvenile female rapacity.
In Dolomedes species, food consumption is positively related to aggression, juvenile growth and adult female size depend on juvenile food consumption, female adult size is the major determinant of female fitness, and aggressive behavior is genetically constrained during development. Aggressive juvenile females therefore consume more prey, obtain larger sizes, and produce more offspring than non-aggressive juveniles. The result is intense selection for high female aggression toward both conspecific and heterospecific prey during juvenile development. Because of genetic constraints on aggressive behavior, adult females will exhibit high aggression and low discrimination (i.e. be sexually cannibalistic), and may remain unmated as a result. Arnqvist and Henriksson (1996) posit that aggression has likely evolved as a balance between conflicting selective pressures on aggression in juveniles and adults. They suggest that the taxonomic distribution of sexual cannibalism should reflect differences in the relationships between aggression, food consumption, adult size, and fecundity. A comparative study of sexual cannibalism across insect and arachnid taxa may thus yield insight into the general applicability of this model in exploring the evolution of sexual cannibalism in different taxa.
In light of the diversity in form of sexual cannibalism and the conflicting implications of empirical studies exploring its evolution, it is likely that sexual cannibalism evolved independently multiple times (Elgar 1992) and is maintained in different species by different selective forces. Development of an all-encompassing model for the evolution of sexual cannibalism is thus an unrealistic endeavor. We should attempt instead to explain sexual cannibalism on a case-by-case basis. Instead of using certain models and empirical data to refute others, we should assess the applicability of each existing model to the diverse interactions we see in nature. When we are unable to reconcile a natural pattern with any of the existing models, we should explore mechanisms and possibilities that may have been overlooked in existing explanations.
To this end, I present a hypothesis for the evolution of sexual cannibalism in the jumping spider Phidippus rimator (Araneae: Salticidae). Similar to the Dolomedes species studied by Arnqvist and Henriksson (1997), in many species of Phidippus, food consumption is positively related to aggression, juvenile growth and adult female size depend on juvenile food consumption, and female fecundity is positively related to size (Edwards 1980; Jackson 1980). I carried out extensive behavioral observations on P. rimator as part of a study examining top-down effects in old-field food webs. Through this work I learned that juvenile and adult females exhibit high levels of aggression toward conspecific and heterospecific prey. Females commonly attack and consume males before, during, and after copulation. Males approach females cautiously, and with an elaborate courtship display, and retreat rapidly after sperm transfer, usually by curling into a ball and rolling to the litter below. Furthermore, males often locate a female, but do not approach to court her until the female has successfully captured a prey item. In 32 observed courting approaches, fours of six successful copulations occurred when the female was consuming another prey item (one of these males was killed during copulation when the female dropped her lepidopteran prey and attacked her mate; another was killed after copulation in a similar scenario).
I have rejected a paternal investment/male complicity explanation for the evolution of sexual cannibalism in Phidippus rimator because of the males' distinctly non-compliant behavior. I have rejected the Elgar and Nash model of female choice (1988) because males are cannibalized during all stages of the courtship/copulatory sequence. Similarly, I have rejected the Newman and Elgar "Economic" model (1991) for the evolution of this interaction because females attack males regardless of their feeding status. Another possible explanation for sexual cannibalism is that the female attacks the male because she mistakes his identity as a prey item rather than a conspecific (reviewed in Elgar 1992). This hypothesis was not discussed because there has been no empirical evidence to support it (Elgar 1992). A case of mistaken identity certainly does not explain sexual cannibalism in Phidippus spiders. Salticids have the highest visual acuity of all arachnids (Forster 1985), and are thus unlikely to attack or approach anything by accident. Furthermore, the occurrence of cannibalism during and after copulation further precludes the possibility of mistaken identity.
It is more likely that the ontogeny of aggression explanation invoked by Arnqvist and Henriksson (1997) accounts in part for the evolution of sexual cannibalism in Phidippus rimator. However, while Arnqvist and Henriksson developed their hypothesis as a fitness trade-off between aggressive behavior in juvenile and adult fishing spiders, I posit that this ontogenetic conflict of interest is absent, or at least less important, in P. rimator. It is likely that aggressive behavior is selectively advantageous in juvenile P. rimator, as in juvenile D. fimbriatus. However, while this behavior is thought to confer negative fitness to adult fishing spiders by decreasing fertilization rates of adult females (Arnqvist and Henriksson 1997), it may have a less deleterious effect on jumping spiders. Male P. rimator travel extensively in search of mates, and single males often fertilize multiple females (K.B. Suttle, personal observation). Thus a population of P. rimator could achieve a high reproductive rate despite a female-biased sex ratio. Furthermore, the increase in female survival conferred by high levels of adult aggression may offset fitness costs to females that remain unmated. Female P. rimator are central place foragers and are highly territorial (K.B. Suttle, personal observation). When a female is placed within the visual range of an established female, and there is mutual detection, one female is killed in over 50% of the resulting interactions. Because aggressive females will better defend their eggs and foraging space from competitors and potential predators, high levels of aggression may confer survival and fitness advantages to adult females. I hypothesize, therefore, that sexual cannibalism in Phidippus rimator may have evolved along a similar pathway to that in Dolomedes fimbriatus, but does not cause the same conflict of interest between the adults and juveniles that it does in D. fimbriatus. Furthermore, sexual cannibalism may be maintained in the species through a selective advantage of aggressive behavior to both juveniles and adults.
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