To feed or to wrap? Female silk cues elicit male nuptial gift construction in a semiaquatic trechaleid spider

By wrapping prey and offering it as a nuptial gift, males can obtain mating and/or parental benefits despite some costs. Males of the Neotropical semiaquatic spider Paratrechalea ornata (Trechaleidae) offer females a nuptial gift consisting of a prey item wrapped in silk. What stimulus inhibits males from feeding and elicits gift construction? We hypothesized that signals associated with female silk threads could affect decision-making by males. We investigated three groups of males carrying a captured prey under different experimental treatments. In the treatment S, males were exposed to an arena with female silk; in SF, males were exposed to both silk and a female confined in a cell, and in the control group, males were exposed to a clean arena. Gift construction was observed only in the S and SF groups, with a similar occurrence rate. After touching females (SF group), males did not change their pattern of gift construction. Gift construction occurrence increased with male and female age. The results lead us to assume that the existence of chemical cues associated with female silk elicits male searching behaviour and gift construction, allowing males to decide between eating or wrapping prey according to the possibility of a sexual encounter. Anticipating gift construction, males are ready to mate, diminishing the risks of predation, female desertion or male–male scramble competition. The effect of age on behavioural variation and the rate of construction is discussed.     

Why Do Males of the Spider Pisaura mirabilis Wrap Their Nuptial Gifts in Silk: Female Preference or Male Control?

Males of the spider Pisaura mirabilis present a nuptial prey gift to the female during courtship as a mating effort. The gift is usually round and wrapped in white silk. It was suggested that the wrapped gift functions as a sensory trap by mimicking the female's eggsac implying that males exploit the female maternal care instinct and not her foraging motivation in a sexual context. The shape of the gift (round) and appearance (white) should then increase female acceptance of males. We tested these predictions experimentally and found that neither gift shape (round or oblong) nor silk wrapping (wrapped or unwrapped) facilitated female acceptance, in contrast unwrapped gifts were accepted faster than wrapped ones. Instead, we found that silk wrapping benefited the males because it significantly decreased the risk of females stealing the gift without copulation and consequently directly increased male mating success. Large oblong gifts were difficult for males to handle during copulation, resulting in shorter copulations for oblong vs. round gifts. Thus, round gifts were not preferred by the females but were beneficial to the males. Our results indicate two adaptive benefits to males of wrapping the nuptial gift: to reduce the risk of losing the gift to females without copulation, and make it possible to reshape an oblong prey into a round gift that facilitates the male's access to the female's genitalia. Our results suggest that the male gift wrapping trait may be selected though sexual conflict over remating rate.     

Nuptial gifts of male spiders function as sensory traps

While nuptial food gifts come in various forms in arthropods, their evolutionary origins are unclear. A previous study on insects has shown that such gifts may arise as a sensory trap that exploits a female's underlying motivation to feed. Here I present independent evidence of a sensory trap in spiders. In certain visually oriented spiders, I suggest that males initially exploit the maternal care instinct by producing a nuptial gift that closely resembles the female egg sac. Males of the spider Pisaura mirabilis cover their prey gift with a silk layer, transforming it into a white round object. In a laboratory experiment I tested whether the colour of the gift affected the rate that females accepted males displaying their gifts. I found that the brighter and the more alike the nuptial gift to a female's egg sac, the faster the female responded by grabbing the gift. My results support the hypothesis that the nuptial gift in P. mirabilis works as a sensory trap.     

Sexual selection in the gift-giving dance fly, Rhamphomyia sulcata, favors small males carrying small gifts

In some species of insects males transfer a gift to females during courtship or copulation. In the dance flies these nuptial gifts vary from nutritious prey items to inedible tokens such as a leaf, stone, or silk balloon. Nuptial gifts in dance flies are presumed to increase male mating success. We examined the strength and form of sexual selection on male Rhamphomyia sulcata, an empidid in which males provide females with a nutritious prey item as a nuptial gift. We found that whereas large males carried large gifts, neither large males nor gifts were targets of sexual selection. Indeed, correlational selection analysis and nonparametric examination of the fitness surfaces revealed that small males carrying small gifts were the most successful. Males may be more maneuverable or flight efficient with small gifts, or small males with large gifts may be unable to carry both a large gift and a female in the paired descent flight. These results suggest carrying constraints may be an important factor in determining selection on nuptial gift size. The largest target of sexual selection was old males. Old males were also paired with the largest and most fecund females, highlighting the role mate quality can further contribute to selection on males. Correlational selection analysis also revealed selection for an increase in covariance between male wing length and body size, and for an increase in slope between these traits. Males who deviate away from the optimal phenotypic relationship for two tightly related morphological traits, such as tibia and wing length, may have overall reduced performance. These findings highlight the role correlational sexual selection can play in optimizing nonsexual male morphology and scaling relationships. This study questions the role of the nuptial gift in dance flies as a resource for females.     

Male nutritional history affects female fecundity in a male-dimorphic mite: Evidence for a nuptial gift?

In male-dimorphic species, males are often either armoured ‘majors’ that can monopolise access to females, or unarmoured and defenceless ‘minors’ that cannot. However, majors, unlike minors, have to spend energy to maintain their weaponry. Like-for-like, this could mean that minors have relatively more energy available to increase their reproductive output through e.g. sperm competition, or the transference of nutrients by means of a nuptial gift. Such a fitness advantage to minors could therefore contribute to explaining the coexistence of both morphs in single populations. We tested if food-deprived females of the male-dimorphic bulb mite Rhizoglyphus robini produced more eggs when mated to a minor or to a major male, and whether egg production depended on whether their mates were starved or fed prior to mating. We found no effect of male morph on female fecundity, but females did produce more eggs when mated to previously fed males. We also found that females increased in mass, but males decreased in mass over the course of the experiment. From these observations we infer that fed males are able to transfer nutrients, a nuptial gift, to their mate. This is the first observation to suggest nuptial gift transfer in mites. Though males of both morphs appeared able to produce nuptial gifts; other factors, like habitat complexity, should be considered to identify fitness benefits of minor over major males to understand why the two morphs coexist.     

Is male puddling behaviour of tropical butterflies targeted at sodium for nuptial gifts or activity?

An apparent sexual difference in adult feeding behaviour in many species of Lepidoptera relates to puddling on mud, dung and carrion. In most butterfly species, puddling is exclusively a male behaviour. A possible explanation for this division in feeding behaviour is that nutrients derived from puddling are transferred to the female in the spermatophore during mating as a nuptial gift. Sodium derived from puddling has been shown to act as a nuptial gift in a few Lepidoptera species. It can also be used for neuromuscular activity in both males and females and may therefore correlate with flight morphology. In this study, we examine the generality of these two hypotheses in comparative work on a community of African fruit-feeding butterflies. We investigated puddling behaviour of males and females on carrion and dung together with sodium preferences, polyandry, relative wing-size, sexual size dimorphism and sodium concentrations in the bodies and spermatophores of several species. The results show that sodium as a nuptial gift can explain the sexual division in puddling in some species, but not in all. Species in which both sexes puddle transfer little sodium in the nuptial gift, which is consistent with the nuptial gift theory. Wing loading and puddling are not significantly correlated, but the trend followed the direction predicted by the activity hypothesis. However, the sodium concentration in the species with the smallest wing area to thoracic volume (WA/TV) ratio (the largest Charaxes spp.), was relatively low. Moreover, in all investigated species, the sodium concentration was higher in the abdomen than in the thorax. The results are discussed in the light of differences between the sexes in foraging behaviour in both larvae and adults, and with respect to alternative explanations for puddling.  © 2005 The Linnean Society of London, Biological Journal of the Linnean Society , 2005, 86 , 345–361.     

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 Conflict Over Spermatophore Attachment in a Nuptially Feeding Cricket

Sexual conflict is implicated in the evolution of nuptial feeding. One function of nuptial gifts lies in mating effort, where the female’s eating of the gift reduces her likelihood of prematurely terminating sperm transfer. We test several ideas regarding sexual conflict in the nuptially feeding wood cricket Nemobius sylvestris. In this cricket, males pass two kinds of spermatophores to females: spermless microspermatophores and larger sperm‐filled macrospermatophores. Females may palpate the males’ forewing secretions as a possible additional form of nuptial feeding. We manipulated male mobility and female feeding regime to examine the effects on spermatophore transfer, macrospermatophore attachment duration, and palpations of the males’ forewings. Neither male confinement nor female feeding regime affected the occurrence of macrospermatophore transfer. Males transferred the macrospermatophore sooner to low‐food females than to high‐food females. Males that were freely mobile (unconfined and sham treatments) had longer macrospermatophore attachment durations than confined males, while female feeding regime did not affect attachment duration. The overall occurrence of female palpation was not significantly affected by female feeding regime. However, high‐food females were more likely to perform short palpations before microspermatophore transfer, while low‐food females were more likely to palpate after macrospermatophore transfer. Sexual conflict is evident in that males appear to guard against premature removal of the sperm‐filled macrospermatophore. Low‐food females appear to facilitate the early transfer of the macrospermatophore, while being more likely to perform relatively long post‐insemination palpations than better‐fed females.     

Optimal numbers of matings: the conditional balance between benefits and costs of mating for females of a nuptial gift‐giving spider

In species where females gain a nutritious nuptial gift during mating, the balance between benefits and costs of mating may depend on access to food. This means that there is not one optimal number of matings for the female but a range of optimal mating numbers. With increasing food availability, the optimal number of matings for a female should vary from the number necessary only for fertilization of her eggs to the number needed also for producing these eggs. In three experimental series, the average number of matings for females of the nuptial gift‐giving spider Pisaura mirabilis before egg sac construction varied from 2 to 16 with food‐limited females generally accepting more matings than well‐fed females. Minimal level of optimal mating number for females at satiation feeding conditions was predicted to be 2–3; in an experimental test, the median number was 2 (range 0–4). Multiple mating gave benefits in terms of increased fecundity and increased egg hatching success up to the third mating, and it had costs in terms of reduced fecundity, reduced egg hatching success after the third mating, and lower offspring size. The level of polyandry seems to vary with the female optimum, regulated by a satiation‐dependent resistance to mating, potentially leaving satiated females in lifelong virginity.     

The influence of nuptial feeding and sperm transfer on the immunological cost of reproduction in the ground cricket Allonemobius socius

Mating is often accompanied by decreased female immune function across numerous animals systems, suggesting that immune suppression is a widespread reproductive cost. However, the trade‐off between immunity and reproduction can be minimized when females have access to abundant nutrient resources. This observation suggests that the nuptial gifts provided by males in many insect systems may help to offset the common immunological cost to reproduction. In the present study, this hypothesis is tested in the ground cricket Allonemobius socius (Scudder), whose females receive a sizeable haemolymph‐based gift. Accordingly, male gift donation is controlled by covering the tibial spur (the source of the gift) of randomly chosen males with clear nail polish. The influence of sperm transfer on female immunity is disentangled from that of the nuptial gift by also examining females who fail to receive sperm during mating (spermatophore transfer has a 40% failure rate in virgin males). It is predicted that females who receive a nuptial gift will exhibit superior immune function compared with those who receive no gift. The results show that sperm transfer reduces female immune function, which is an expected immunological cost of reproduction. By contrast to the prediction, nuptial gifts do not minimize the immunological cost of reproduction in this system. Unexpectedly, the receipt of a gift appears to decrease female immune function independent of sperm transfer. The findings suggest that the nuptial gift, similar to sperm, signals the female to begin her reproductive investment, causing limited resources to be reallocated from immune function.     

All that Glisters is not Gold: Sensory Bias, Sexual Conflict and Nuptial Feeding in Insects and Spiders

It is becoming increasingly clear that the evolutionary interests of the sexes are often in conflict when it comes to mating. Sexual encounters involving nuptial gifts, however, have often been viewed as prime examples of sexual co‐operation, rather than conflict. In this review, I explore the proposition that nuptial gifts act as sensory traps: by exploiting the female's gustatory responses, the male may be able to entice females to accept superfluous matings and/or transfer greater volumes of ejaculate than are in the female's reproductive interests. Evidence suggests that the females’ sensory biases may have played an important role in shaping gift characteristics in at least four different systems, although relatively few forms of nuptial feeding have so far been examined from this perspective. I argue that gift composition is more likely to be tailored to increasing the attractiveness of the gift to the female and/or maximizing gift handling time than to suit the female's nutritional needs and that the fecundity‐enhancing benefits of nuptial gifts are often questionable and have been over‐stated in the literature. Fertilization biases associated with the female's attraction to the nuptial gift, however, could lead to in‐direct benefits for the female. On the other hand, nuptial feeding may also lead to significant costs to the female. Evidence suggests that some types of gift entice the female to mate, but it is not clear whether the resultant degree of polyandry is higher than optimal for the female. In other cases, evidence suggests that the gift enables the male to overcome the resistance of the female to accepting an extra large ejaculate and that large ejaculates are associated with longer post‐mating sexual refractory periods in the female. This could represent a cost to the female by delaying or preventing her from receiving the genetic benefits of polyandry. At present, it is not clear, however, whether such costs outweigh the potential benefits of nuptial feeding for the female.     

Male mate choice in a sexually cannibalistic species: male escapes from hungry females in the praying mantid <Emphasis Type="Italic">Tenodera angustipennis</Emphasis>

While competing males and choosy females may be common in animal mating systems, male choice can evolve under certain conditions. Sexual cannibalism is such a condition because of the high mortality risk for males. In mantids, female body condition is associated with male mate preference, with fat females preferred, due to at least two reasons: females in poor nutritional condition are likely to attack and predate males, and fat females can potentially increase the number of offspring. Thus, the risk of cannibalism and female fecundity can influence male mating behavior. In this study, we attempted to separate these factors by using the praying mantid Tenodera angustipennis to examine whether male preference for fat female mantids was based on avoiding sexual cannibalism (cannibalism avoidance hypothesis) or preference for female fecundity (fecundity preference hypothesis). The feeding regimes were experimentally manipulated to discriminate between the effects of female fecundity and female hunger status on male and female mating behaviors. We found that recently starved females more frequently locomoted toward the male, and that male abdominal bending was less intensive and escape was sooner from recently starved females. These female and male behavioral responses to female hunger condition may reveal male avoidance of dangerous females in this mantid.     

Responses of Acilius sulcatus (Coleoptera: Dytiscidae) to chemical cues from perch (Perca fluviatilis)

In this study we tested the hypothesis that the presence of chemical stimuli from a hungry predator would initiate anti-predator responses, while stimuli from a satiated predator would not. We used chemical stimuli released from starved perch (Perca fluviatilis) and from satiated perch (predator). As prey we used adult Acilius sulcatus (Coleoptera: Dytiscidae). The reaction of the beetles to different predator conditions was tested during daytime. We also tested the reaction to starved perch during the night. A. sulcatus activity decreased when it was exposed to stimuli released from starved perch during daytime when visibility was poor, due to the presence of artificial vegetation. There was, however, no reaction to satiated perch under the same experimental conditions. These results indicate that A. sulcatus can discriminate between chemical cues from hungry and satiated fish predators. When visibility was good and the concentration of chemical cues was constant, the beetles did not react to starved perch in the daytime, but their activity decreased at night in response to stimuli released from starved perch. Visual as well as chemical cues seem to be important for detecting a potential predator. When visibility is good, beetles seem to rely on visual stimuli, while in darkness they seem to use chemical stimuli to detect the presence of predators. Received: 4 October 1996 / Accepted: 7 February 1997     

Nuptial feeding by male bushcrickets: an indicator of male quality?

Male bushcrickets transfer a spermatophore at mating that consistsof a sperm-containing ampulla and a product of the accessoryglands, the spermatophylax, that is consumed by the female duringinsemination. Male Requena verticalis produce functionally differentspermatophores depending on the availability of sexually receptivefemales. They will maintain high mating frequency by providinga gift sufficient to ensure sperm transfer, or will invest parentallyin females when their mating frequency is low. We examined therelationship between male quality and nuptial feeding underconditions where males invest in ejaculate protection or inparental investment. When investing in ejaculate protection,males reduced the quality of the spermatophylax meal by reducingboth the concentration of protein and the absolute amount ofprotein it contained. There was no relationship between malephenotype and gift size or quality. Moreover, we could findno evidence for the recently advanced hypothesis that femalescan exercise mate choice by interfering with insemination. However,when males were investing parentally, we found a positive associationbetween spermatophylax size and male size, but no relationshipbetween protein content and male size. Males with high levels offluctuating asymmetry invested more heavily in the nutritionalcontent of their spermatophylaxes than did symmetrical males.Thus, male quality does influence nuptial feeding, but in amanner predicted by a model of indirect fitness benefits frommate choice.     

Nuptial gift consumption influences female remating in a scorpionfly: male or female control of mating rate?

In the scorpionfly Panorpa cognata, males provide females with saliva secretions as nuptial food gifts. Consequently, females derive material benefits and possibly also genetic benefits from multiple matings. Females therefore generally should have a high motivation to remate. Males, on the other hand, do not share this interest, which will generate a sexual conflict over remating interval, possibly leading to male adaptations that prevent females from remating with other males. In this study, I found that mated females were less prone to copulate than virgin females, despite female benefits of multiple matings. Further, I found that the remating interval was significantly longer if the first copulation was long compared to shorter matings. This effect does not entirely depend on copulation duration per se, but on the amount of saliva, that a female is consuming during copulation. These results suggest a mating-induced refractory period and can be interpreted as male manipulation of female remating behaviour mediated through substances in the nuptial gift. Alternatively, receiving large nuptial gifts may decrease the prospective direct fitness benefits from further copulations, and thus change optimal female remating rate. Furthermore, gift size has been shown to correlate with male nutritional condition, which may be an indicator of male genetic quality. Females may therefore benefit indirectly by not remating following copulations involving large saliva gifts. In this scenario, female remating interval would be an effect of cryptic female choice.     

Does part reproductive history predict competitive interactions and male mating success in pupfish?

Two experiments were performed to determine the effect of past territoriality and mating success on subsequent dominance and ability to attract females. First, in 14 staged, pair-wise encounters, the development of nuptial coloration and agonistic behaviour was examined in two types of males: previously territorial (PT) and previously non-territorial (PNT) males. Previously territorial males developed a more intense nuptial coloration and won all contests. Second, to test the males' ability to attract females, other factors were controlled that could have affected female mate choice, such as male size, quality of breeding substrate and male-male interactions. In 40 trials, PT males were more active, developed a more intense nuptial coloration, courted females more vigorously, spawned sooner and had a higher mating success than PNT males. Thus, in pupfish, Cyprinodon pecosensis, previous reproductive history is a good indicator of both dominance and mating success. Only males in good physical condition achieve high mating success, and both intra- and inter-sexual selection are important in maintaining the close correlation between expression of nuptial coloration, a second sexual trait, and other male attributes, such as physical condition and vigour, that allow a male to secure and defend a territory against rivals and to attract and spawn with females.     

Prenuptial agreements: mating frequency predicts gift-giving in Heliconius species

Theory predicts that when males provision females with nuptial gifts that include nutrients, the degree of polyandry should be positively correlated with the size or quality of the gift. This is because larger and more nutritious gifts tend to increase female refractory period, reducing the chances the female will remate soon. This decreases the likelihood of sperm competiton and consequently increases the donor male fitness. Butterflies in the genus Heliconius Kluk (Lepidoptera: Nymphalidae: Heliconini) exhibit variable mating systems that include monandry and polyandry. In addition to protein in the spermatophore, males increase gift quality by providing females with cyanide, which may contribute to protection of the female or her eggs. We tested whether degree of polyandry and gift quality (spermatophore weight and cyanide content) were correlated in nine Heliconius species from greenhouse populations. As predicted, both spermatophore weight and cyanide content were correlated with mating frequency. This is the first report to show that degree of polyandry correlates with allocation of defensive chemical as part of a nuptial gift.     

Sperm storage mediated by cryptic female choice for nuptial gifts

Polyandrous females are expected to discriminate among males through postcopulatory cryptic mate choice. Yet, there is surprisingly little unequivocal evidence for female-mediated cryptic sperm choice. In species in which nuptial gifts facilitate mating, females may gain indirect benefits through preferential storage of sperm from gift-giving males if the gift signals male quality. We tested this hypothesis in the spider Pisaura mirabilis by quantifying the number of sperm stored in response to copulation with males with or without a nuptial gift, while experimentally controlling copulation duration. We further assessed the effect of gift presence and copulation duration on egg-hatching success in matings with uninterrupted copulations with gift-giving males. We show that females mated to gift-giving males stored more sperm and experienced 17% higher egg-hatching success, compared with those mated to no-gift males, despite matched copulation durations. Uninterrupted copulations resulted in both increased sperm storage and egg-hatching success. Our study confirms the prediction that the nuptial gift as a male signal is under positive sexual selection by females through cryptic sperm storage. In addition, the gift facilitates longer copulations and increased sperm transfer providing two different types of advantage to gift-giving in males.     

Diet‐dependent female evolution influences male lifespan in a nuptial feeding insect

Theory predicts that lifespan will depend on the dietary intake of an individual, the allocation of resources towards reproduction and the costs imposed by the opposite sex. Although females typically bear the majority of the cost of offspring production, nuptial feeding invertebrates provide an ideal opportunity to examine the extent to which reproductive interactions through gift provisioning impose a cost on males. Here we use experimental evolution in an Australian ground cricket to assess how diet influences male lifespan and how the costs of mating evolve for males. Our findings show that males had significantly shorter lifespans in populations that adapted to a low‐quality diet and that this divergence is driven by evolutionary change in how females interact with males over reproduction. This suggests that the extent of sexual conflict over nuptial feeding may be under‐realized by focusing solely on the consequences of reproductive interactions from the female’s perspective.