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

Precopulatory sexual cannibalism, or female predation of a potentialmate before mating, illustrates an extreme intersexual conflict.Unlike sexual cannibalism occurring after mating, precopulatorysexual cannibalism cannot be construed as a male strategy. Thus,research on the adaptive significance of this phenomenon hasfocused on female benefits. In the present study, I test theidea that precopulatory sexual cannibalism represents an adaptivefemale trade-off between the material costs and benefits ofmating with a male (forgoing food, securing sperm) and preyingon a male (forgoing sperm, securing food). I pay particularattention to the rarely tested prediction that precopulatorysexual cannibalism by virgin females should increase as eachfemale's expectation of future mating opportunities increases.I use the phenomenon of cohabitation between adult males andjuvenile females nearing sexual maturity as a means to manipulatefemale expectation of future mate availability. Results indicatethat feeding on a male has significant positive effects on severalmeasures of female fecundity. However, the likelihood of precopulatoryattacks was not explained by a female's recent feeding history.Finally, as predicted, juvenile female cohabitation with maturemales (expectation of future mating opportunities) heightensthe prevalence of precopulatory attacks by virgin females, suggestingthat juvenile experience can alter a female's propensity forsexual cannibalism. This is the first study to suggest thatjuvenile experience can alter a female's propensity for sexualcannibalism. This finding emphasizes the point that studiesof sexual selection and mating systems need to consider theeffects of juvenile experience on adult behavior.     

Sexual cannibalism and sperm competition in the golden orb-web spider Nephila plumipes (Araneoidea): female and male perspectives

Mating systems are frequently shaped by conflicts over reproductive interests between males and females. Sexual cannibalism canbe an especially dramatic manifestation of such conflicts.However, the resolutions of this conflict differ among sexuallycannibalistic spider species. Cannibalism may be in the interestof both sexes when females consume males as a foraging decisionto improve fecundity and/or males sacrifice their bodies toincrease fertilization success. In other species, females exertsequential choice of partner by selectively terminating copulationthrough cannibalism while males fail to obtain a paternityadvantage. Here, we investigate the adaptive value of cannibalismin the orb-web spider Nephila plumipes where 60% of males donot survive copulation. Virgin females in poor condition aremore frequently cannibalistic and more likely to kill largemales, but the frequency of cannibalism among mated femalesis not influenced by these factors. Instead, males that matewith mated females increase their fertilization success bybeing cannibalized. Cannibalized males generally mate for longer,but longer copulations correspond with increased paternity onlyin mated females. The amount of sperm from particular malesthat a female stored was not influenced by any of the measuredvariables. The number of sperm stored was not related to paternity,nor was there any detectable reduction in sperm number afterfemales had reproduced. Our data suggest that the conflict between the sexes differs between virgin and mated females.Females should always cannibalize a male, but males only gainfrom cannibalism when mating with mated females, not when matingwith virgin females. Interestingly, the frequencies of cannibalismare not different in matings with virgin or mated females.     

Sexual cannibalism by Octopus cyanea on a Pacific coral reef

Sexual cannibalism is rare in the animal kingdom. Although cannibalism is not uncommon in cephalopods, here we report the first documented case of sexual cannibalism. A large female Octopus cyanea was observed continuously for 2.5 days in Palau, Micronesia, when she was out of her den. On the second day, a small male followed and mated her 13 times during 3.5 h while she continued to forage over 70 m distance. After the 12th mating, she aggressively chased a different small octopus that barely escaped by jetting, inking and swimming upwards. Shortly thereafter, the original small male mated her a 13th time, but subsequently she attacked and suffocated him and spent 2 days cannibalizing him in her den. This sort of intraspecific aggression helps to explain several reports of octopuses mating out in the open, a behaviour that may serve to allow the smaller mate to escape cannibalism.     

Sexual cannibalism in Nephila plumipes as a consequence of female life history strategies

The evolution of sexual cannibalism has been modelled as both an adaptive and nonadaptive female strategy. Recent evidence from several species suggests a connection between female foraging and sexual cannibalism, but the precise benefits for females have remained obscure. Here, we investigate the difference between cannibalistic and noncannibalistic female Nephila plumipes by removing the potential nutritional benefit of cannibalism. Courting and mating males that were killed by a female were immediately removed so that the female could not consume them. Nevertheless, cannibalistic females gained more mass from maturation to oviposition and produced larger first clutches than noncannibalistic females, although cannibalistic females matured at a smaller size and mass than noncannibalistic females. In juvenile instars, mass gain was generally smaller in females that moulted in a good condition but intermoult intervals were shorter. However, the time from maturity to oviposition was not shorter in females that matured in a good condition. Male behaviour did not differ according to the risk of cannibalism. We suggest that sexual cannibalism in N. plumipes is a side‐effect of an increased foraging vigour of females that matured at a smaller size and body mass. Selection pressure on males to avoid cannibalism may be weak because of limited mating opportunities.     

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

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

Sexual dimorphism and the genetic potential for evolution of sex allocation in the gynodioecious plant, Schiedea salicaria

Sex allocation theory addresses how separate sexes can evolve from hermaphroditism but little is known about the genetic potential for shifts in sex allocation in flowering plants. We tested assumptions of this theory using the common currency of biomass and measurements of narrow-sense heritabilities and genetic correlations in Schiedea salicaria, a gynodioecious species under selection for greater differentiation of the sexes. Female (carpel) biomass showed heritable variation in both sexes. Male (stamen) biomass in hermaphrodites also had significant heritability, suggesting the potential for further evolution of dioecy. Significant positive genetic correlations between females and hermaphrodites in carpel mass may slow differentiation between the sexes. Within hermaphrodites, there were no negative genetic correlations between male and female biomass as assumed by models for the evolution of dioecy, suggesting that S. salicaria is capable of further changes in biomass allocation to male and female functions and evolution toward dioecy.     

Nuptial gift in the spider Pisaura mirabilis maintained by sexual selection

The nuptial prey gift in the spider Pisaura mirabilis has been suggested to function as a male protection against sexual cannibalismduring courtship and mating. This hypothesis together withtwo alternatives—male mating effort and paternal investment hypotheses—were tested in a laboratory experiment withsexually inexperienced males and females. One group of malesoffered no gift to the female while three groups of males offeredsmall, medium, or large sized gifts, respectively. No malewas cannibalized among 82 trials. Aggression was observed onlyin encounters where a gift was presented. Males without a gift courted females, and 40% of these males managed to copulate,compared to 90% of males offering a gift. The copulation durationwas positively correlated with gift size. In general, the femaleterminated the copulation and ran away with the gift. The proportionof eggs fertilized increased with copulation time. Presenceor size of the nuptial gift did not affect female fecundityor spiderling size significantly. The results refute the hypothesesof sexual cannibalism and paternal investment. The nuptialgift represents a male mating effort; it entices the femaleto copulate, facilitates coupling during copulation, and byprolonging copulation it may increase the amount of sperm transferred.I conclude that the nuptial prey gift in Pisaura mirabilisis maintained by sexual selection.     

Sexual selection research on spiders: progress and biases

The renaissance of interest in sexual selection during the last decades has fuelled an extraordinary increase of scientific papers on the subject in spiders. Research has focused both on the process of sexual selection itself, for example on the signals and various modalities involved, and on the patterns, that is the outcome of mate choice and competition depending on certain parameters. Sexual selection has most clearly been demonstrated in cases involving visual and acoustical signals but most spiders are myopic and mute, relying rather on vibrations, chemical and tactile stimuli. This review argues that research has been biased towards modalities that are relatively easily accessible to the human observer. Circumstantial and comparative evidence indicates that sexual selection working via substrate-borne vibrations and tactile as well as chemical stimuli may be common and widespread in spiders. Pattern-oriented research has focused on several phenomena for which spiders offer excellent model objects, like sexual size dimorphism, nuptial feeding, sexual cannibalism, and sperm competition. The accumulating evidence argues for a highly complex set of explanations for seemingly uniform patterns like size dimorphism and sexual cannibalism. Sexual selection appears involved as well as natural selection and mechanisms that are adaptive in other contexts only. Sperm competition has resulted in a plethora of morphological and behavioural adaptations, and simplistic models like those linking reproductive morphology with behaviour and sperm priority patterns in a straightforward way are being replaced by complex models involving an array of parameters. Male mating costs are increasingly being documented in spiders, and sexual selection by male mate choice is discussed as a potential result. Research on sexual selection in spiders has come a long way since Darwin, whose spider examples are reanalysed in the context of contemporary knowledge, but the same biases and methodological constraints have persisted almost unchanged through the current boom of research.     

Copulation duration in the spiderPhilodromus vulgaris (Hentz) (Araneae: Philodromidae) and its influence on the evolution of host transfer behavior during cannibalism byMantispa uhleri banks (Neuroptera: Mantispidae)

Matings and acts of cannibalism were observed in the crab spiderPhilodromus vulgaris, some of which were carrying a first-instar larva of the mantispidMantispa uhleri. Larval mantispids did not transfer during the copulation of their spider hosts but did switch from spider to spider during cannibalism. Twenty-three of 27 total cannibalisms in which the cannibalized spider carried a larva resulted in larval transfers, for a transfer rate of 85%. Copulation times inP. vulgaris were found to be extremely short in comparison to lycosids such asSchizocosa ocreata, whose long copulation time supports the larval transfer ofClimaciella brunnea. The time required for larval transfer during cannibalism inP. vulgaris was measured. Cannibalisms were much longer than copulations but larvae transferred to the cannibalizing spider in a comparatively short period of time.     

Spontaneous male death and monogyny in the dark fishing spider

Monogyny (male monogamy) is found in a diverse assemblage of taxa, and recent theoretical work reveals that a male-biased sex ratio can favour the evolution of this relatively rare mating system. We integrate this theoretical framework with field observations and laboratory experiments involving the sexually size dimorphic fishing spider, Dolomedes tenebrosus, to test the prediction that this species exhibits monogyny. Field surveys revealed a male-biased sex ratio, likely resulting from different life-history strategies (early male maturation). Results from mating trials supported our prediction of monogyny as we discovered that males mate with a single female. Unexpectedly, however, we observed that mating results in obligate male death and genital mutilation. Additional field observations of released individuals suggest that males are not limited by their ability to encounter additional females. Controlled laboratory assays demonstrated that males discriminate among virgin and non-virgin female silk cues, consistent with predictions of first-male sperm precedence. In summary, we report a novel case of male self-sacrifice in a species that exhibits female-biased sexual size dimorphism, male-biased sex ratio, genital mutilation and a suggestion of first-male sperm precedence; all of which are consistent with theoretical predictions of the evolution of monogyny.     

Sexual cannibalism, competition, and size dimorphism in the orb-weaving spider Nephila plumipes Latreille (Araneae: Araneoidea)

The degree and direction of sexual dimorphism varies widely,but in several taxa of orb-weaving spiders, including Nephila,males may be less than one-tenth the size of females. This differenceis commonly attributed to selection through precopulation sexualcannibalism: females may either fail to detect very small males,or ignore them as potential prey items. However, there is oftenthe potential for male-male competition in these species becauseseveral males can be found on the web of a single female. Weinvestigated experimentally the effects of sexual cannibalismand male-male competition on male body size and hence sexualdimorphism in the Australian golden orb-weaver (Nephila plumipes).Small males were less likely to be detected and cannibalizedthan larger males. However, larger males excluded small malesfrom the central hub of the web, where mating takes place. Theconflicting effects of sexual cannibalism and male-male competitionmay be responsible for the relatively large variation in malebody size in this species.     

Female remating propensity contingent on sexual cannibalism in sagebrush crickets, Cyphoderris strepitans: a mechanism of cryptic female choice

Male sagebrush crickets (Cyphoderris strepitans) permit femalesto engage in an unusual form of sexual cannibalism during copulation:females feed on males' fleshy hind wings and ingest hemolymphoozing from the wounds they inflict. These wounds are not fatal,and normally only a portion of the hind wings are eaten at anyone mating, so that mated males are not precluded from matingagain. As a result, nonvirgin males have fewer material resources tooffer females than do virgin males, such that females shouldbe selected to preferentially mate with high-investment virginmales. We tested the hypothesis that female mating preferencesfavor males capable of supplying females with the highest materialinvestment. Our results indicate that both female diet and opportunitiesfor sexual cannibalism influence female mating behavior. Femalesmaintained on a low-nutrient diet mounted males significantlysooner than females maintained on a high-nutrient diet, indicatingthat a female's overall nutrient intake may determine her propensityto mate. In addition, females were significantly more reluctantto mount and mate with males whose hind wings had been surgicallyremoved and thus were incapable of providing females with awing meal. Finally, females initially mated to dewinged malesremated with winged males significantly sooner than femalesallowed to feed freely during their initial mating, resultingin cryptic female choice of investing males.     

Life history responses depend on timing of cannibalism in a damselfly

1. Cannibalism has often been suggested as an important mechanism to reach the necessary developmental stage and size before a critical time horizon is reached, but this role has been largely unexplored. We studied effects of cannibalism on the life history of the damselfly Lestes viridis under combinations of a time constraint (by manipulating the perceived time available in the growth season) and a biotic constraint (density). 2. Larvae had a faster development and growth rate when reared at high time stress (late photoperiod). They also had a higher growth rate and mass at emergence when cannibalism occurred (density 2 and 4). Cannibalism occurred earlier at higher density. Accelerated life history responses (faster development and growth rate) and a higher mass at emergence were dependent upon the timing of cannibalism. Responses were more pronounced or only present if cannibalism occurred early in the larval period. 3. Our data suggest that cannibalism may not only act as a lifeboat mechanism by enabling cannibals to survive detrimental ecological conditions, but may also act as a compensatory mechanism to keep life history variables near‐optimal at life history transitions, even under sub‐optimal conditions.     

Beyond the phenotypic gambit: molecular behavioural ecology and the evolution of genetic architecture

Most studies of behaviour examine traits whose proximate causes include sensory input and neural decision-making, but conflict and collaboration in biological systems began long before brains or sensory systems evolved. Many behaviours result from non-neural mechanisms such as direct physical contact between recognition proteins or modifications of development that coincide with altered behaviour. These simple molecular mechanisms form the basis of important biological functions and can enact organismal interactions that are as subtle, strategic and interesting as any. The genetic changes that underlie divergent molecular behaviours are often targets of selection, indicating that their functional variation has important fitness consequences. These behaviours evolve by discrete units of quantifiable phenotypic effect (amino acid and regulatory mutations, often by successive mutations of the same gene), so the role of selection in shaping evolutionary change can be evaluated on the scale at which heritable phenotypic variation originates. We describe experimental strategies for finding genes that underlie biochemical and developmental alterations of behaviour, survey the existing literature highlighting cases where the simplicity of molecular behaviours has allowed insight to the evolutionary process and discuss the utility of a genetic knowledge of the sources and spectrum of phenotypic variation for a deeper understanding of how genetic and phenotypic architectures evolve.