Is diversification in male reproductive traits driven by evolutionary trade-offs between weapons and nuptial gifts?

Many male animals have evolved exaggerated traits that they use in combat with rival males to gain access to females and secure their reproductive success. But some male animals invest in nuptial gifts that gains them access to females. Both these reproductive strategies are costly in that resources are needed to produce the weapon or nuptial gift. In closely related species where both weapons and nuptial gifts are present, little is known about the potential evolutionary trade-off faced by males that have these traits. In this study, we use dobsonflies (order Megaloptera, family Corydalidae, subfamily Corydalinae) to examine the presence and absence of enlarged male weapons versus nuptial gifts within and among species. Many dobsonfly species are sexually dimorphic, and males possess extremely enlarged mandibles that they use in battles, whereas in other species, males produce large nuptial gifts that increase female fecundity. In our study, we show that male accessory gland size strongly correlates with nuptial gift size and that when male weapons are large, nuptial gifts are small and vice versa. We mapped weapons and nuptial gifts onto a phylogeny we constructed of 57 species of dobsonflies. Our among-species comparison shows that large nuptial gift production evolved in many species of dobsonfly but is absent from those with exaggerated weapons. This pattern supports the potential explanation that the trade-off in resource allocation between weapons and nuptial gifts is important in driving the diversity of male mating strategies seen in the dobsonflies, whereas reduced male–male competition in the species producing large spermatophores could be an alternative explanation on their loss of male weapons. Our results shed new light on the evolutionary interplay of multiple sexually selected traits in animals.     

Mating tactic dependent sperm transfer rates in Panorpa similis (Mecoptera; Panorpidae): a case of female control?

Abstract 1. Male Panorpa scorpionflies offer salivary masses as nuptial gifts during copulation. Previous studies have shown that there is usually a strong correlation between the number or size of salivary masses provided and copulation duration. As a result of constant sperm transfer rates, copulation duration is the most important determinant of male fitness in these species. 2. Differences in copulation durations for gift‐giving and non‐gift‐giving males of the Caucasian scorpionfly Panorpa similis have been shown to be much smaller on average than those observed in other Panorpa species. In this study, we therefore focus on the number of sperm transferred in copulations of P. similis both with and without salivary masses. 3. We find that although the average copulation duration in the presence of nuptial gifts is only twice as long as the average copulation duration without nuptial gifts, gift‐giving males transfer almost 11 times more sperm during copulations than non‐gift‐giving males. This is as a result of substantially higher sperm transfer rates (sperm/minute) in copulations in which nuptial gifts are present. 4. Implications of this finding for the interpretation of the mating system of P. similis and the question of which sex controls sperm transfer rates are discussed.     

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.     

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.     

FUNCTIONAL EQUIVALENCE OF GRASPING CERCI AND NUPTIAL FOOD GIFTS IN PROMOTING EJACULATE TRANSFER IN KATYDIDS

The function of nuptial gifts has generated longstanding debate. Nuptial gifts consumed during ejaculate transfer may allow males to transfer more ejaculate than is optimal for females. However, gifts may simultaneously represent male investment in offspring. Evolutionary loss of nuptial gifts can help elucidate pressures driving their evolution. In most katydids (Orthoptera: Tettigoniidae), males transfer a spermatophore comprising two parts: the ejaculate‐containing ampulla and the spermatophylax—a gelatinous gift that females eat during ejaculate transfer. Many species, however, have reduced or no spermatophylaces and many have prolonged copulation. Across 44 katydid species, we tested whether spermatophylaces and prolonged copulation following spermatophore transfer are alternative adaptations to protect the ejaculate. We also tested whether prolonged copulation was associated with (i) male cercal adaptations, helping prevent female disengagement, and (ii) female resistance behavior. As predicted, prolonged copulation following (but not before) spermatophore transfer was associated with reduced nuptial gifts, differences in the functional morphology of male cerci, and behavioral resistance by females during copulation. Furthermore, longer copulation following spermatophore transfer was associated with larger ejaculates, across species with reduced nuptial gifts. Our results demonstrate that nuptial gifts and the use of grasping cerci to prolong ejaculate transfer are functionally equivalent.     

Nuptial gifts and the evolution of male body size

In many insect systems, males donate nuptial gifts to insure an effective copulation or as a form of paternal investment. However, if gift magnitude is both body size-limited and positively related to fitness, then the opportunity exists for the gift to promote the evolution of large male size. In the striped ground cricket, Allonemobius socius, males transfer a body size-limited, somatic nuptial gift that is comprised primarily of hemolymph. To address the implications of this gift on male size evolution, we quantified the intensity and direction of natural (fecundity) and sexual (mating success) selection over multiple generations. We found that male size was under strong positive sexual selection throughout the breeding season. This pattern of selection was similar in successive generations spanning multiple years. Male size was also under strong natural selection, with the largest males siring the most offspring. However, multivariate selection gradients indicated that gift size, and not male size, was the best predictor of female fecundity. In other words, direct fecundity selection for larger gifts placed indirect positive selection on male body size, supporting the hypothesis that nuptial gifts can influence the evolution of male body size in this system. Although female size was also under strong selection due to a size related fecundity advantage, it did not exceed selection on male size. The implications of these results with regard to the maintenance of the female-biased size dimorphic system are 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.     

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.     

Nuptial food gifts influence female egg production in the scorpionfly Panorpa cognata

Abstract.  1. Before copulation, male Panorpa cognata scorpionflies offer females a salivary secretion, which is consumed by the female during copulation. It has previously been demonstrated that this nuptial food gift functions as mating effort by increasing male attractiveness and by increasing ejaculate transfer during copulation.
2. In this study, the effect of saliva consumption on female reproductive output was investigated, and thus the possibility that nuptial food gifts also serve as paternal investment. The experimental design enabled the effect of nuptial gift consumption to be disentangled from other possible effects of multiple mating or increased copula duration.
3. The results showed that saliva consumption increases female egg production by on average 8% (4.5 eggs) per consumed salivary mass, whereas mean egg weight was not influenced.4. These results have important implications for the evolution and maintenance of both male nuptial gifts and female polyandry in this and other species.     

Nuptial gift chemistry reveals convergent evolution correlated with antagonism in mating systems of harvestmen (Arachnida,Opiliones)

Nuptial gifts are material donations given from male to female before or during copulation and are subject to sexual selection in a wide variety of taxa. The harvestman genus Leiobunum has emerged as a model system for understanding the evolution of reproductive morphology and behavior, as transitions between solicitous and antagonistic modes of courtship have occurred multiple times within the lineage and are correlated with convergence in genital morphology. We analyzed the free amino acid content of nuptial gift secretions from five species of Leiobunum using gas chromatography–mass spectrometry. Multivariate analysis of the free amino acid profiles revealed that, rather than clustering based on phylogenetic relationships, nuptial gift chemical composition was better predicted by genital morphology and behavior, suggesting that convergent evolution has acted on the chemical composition of the nuptial gift. In addition, we found that, species with solicitous courtship produce gifts consisting of a 19% larger proportion of essential amino acids as compared to those with more antagonistic courtship interactions. This work represents the first comparative study of nuptial gift chemistry within a phylogenetic framework in any animal group and as such contributes to our understanding of the evolution of reproductive diversity and the participant role of nuptial gift chemistry in mating system transitions.     

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.     

Sex-specific response to nutrient limitation and its effects on female mating success in a gift-giving butterfly

Animals with complex life cycles respond to early food limitation by altering the way resources are allocated in the adult stage. Response to food limitation should differ between males and females, especially in organisms whose mating systems include nutritional nuptial gifts. In these organisms, males are predicted to keep their allocation to reproduction (sperm and nuptial gift production) constant, while females are predicted to sacrifice allocation to reproduction (egg production) since they can compensate by acquiring nuptial gifts when mating. In this study, we investigated how dietary nitrogen limitation during the larval stage affects sex-specific resource allocation in Pieris rapae butterflies. Also, we tested whether nutrient-limited females increased nuptial gift acquisition as a way to compensate for low allocation to reproduction. We found that as predicted females, but not males, sacrifice allocation to reproduction when larval dietary nitrogen is limited. However, females were unable to compensate for this low reproductive allocation by increasing their mating rate to acquire additional gifts. Females reared on low nitrogen diets also reduced wing coloration, a potential signal of female fecundity status. We suggest that female mating frequency is constrained by male mate choice based on females’ wing coloration. This study provides new insights into how larval dietary nitrogen, a key nutritional resource for all herbivores, alters male and female allocation to reproduction as well as to ornamentation.     

Worthless and Nutritive Nuptial Gifts: Mating Duration,Sperm Stored and Potential Female Decisions in Spiders

In nuptial gift-giving species females sometimes select their potential mates based on the presence and size of the gift. But in some species, such as the Neotropical polyandrous spider Paratrechalea ornate male gifts vary in quality, from nutritive to worthless, and this male strategy can be in conflict with female nutritional benefits. In this species, males without gifts experience a reduction in mating success and duration, while males that offer worthless or genuine nutritive gifts mate with similar frequencies and durations. The female apparently controls the duration of copulation. Thus, there is scope for females to favour males offering gifts and further if these are nutritious, via post-copulatory processes. We first tested whether females differentially store sperm from males that offer the highest nutritional benefits by experimentally presenting females with males that offer either nutritive or worthless gifts (uninterrupted matings). Second, we carried out another set of experiments to examine whether females can select sperm based only on gift presence. This time we interrupted matings after the first pedipalp insertion, thus matching number of insertions and mating duration for males that: offered and did not offer gift. Our results showed that the amount of sperm stored is positive related to mating duration in all groups, except in matings with worthless gifts. Gift presence itself did not affect the sperm stored by females, while they store similar number of sperm in matings with males offering either nutritive or worthless gifts. We discuss whether females prefer males with gifts regardless, if content, because it represents an attractive and/or reliable signal. Or alternatively, they prefer nutritive nuptial gifts, as they are an important source of food supply and/or signal of male donor ability.     

The evolution of sex differences in mate searching when females benefit: new theory and a comparative test

Sexual selection is thought to have led to searching as a profitable, but risky way of males obtaining mates. While there is great variation in which sex searches, previous theory has not considered search evolution when both males and females benefit from multiple mating. We present new theory and link it with data to bridge this gap. Two different search protocols exist between species in the bush-cricket genus Poecilimon (Orthoptera): females search for calling males, or males search for calling females. Poecilimon males also transfer a costly nuptial food gift to their mates during mating. We relate variations in searching protocols to variation in nuptial gift size among 32 Poecilimon taxa. As predicted, taxa where females search produce significantly larger nuptial gifts than those where males search. Our model and results show that search roles can reverse when multiple mating brings about sufficiently strong material benefits to females.     

Condition dependence of male nuptial gift construction in the spider <Emphasis Type="Italic">Pisaura mirabilis</Emphasis> (Pisauridae)

Pisaura mirabilis males offer a prey wrapped in silk as a nuptial gift that functions as a male mating effort. If nuptial gift construction is costly, males in poor feeding condition would invest less in this behaviour than males in good condition. We investigated frequencies and characteristics of gift construction in males under different sexual stimuli and different feeding conditions. We analysed gift construction behaviours of 17 males exposed sequentially to three treatments: female silk (S), female silk plus female (SF) and no female cues (control; C). The same individuals were first tested when in good feeding condition (young/satiated) and subsequently in poor feeding condition (old/starved). A separate group in good feeding condition controlling for effects of male age was also tested (old/satiated). Presence of female cues (S and SF) elicited much stronger gift construction response in males compared with the control group. Both groups of satiated males constructed nuptial gifts more frequently than starved males, spending more time on gift construction and using more silk. Our findings show that poor feeding condition affects pre-copulatory gift construction behaviour. Nuptial gift construction may be an honest indicator of male condition and therefore a target of female choice.     

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.     

Function of the Hemolymph Nuptial Gift in the Ground Cricket,Allonemobius socius

Nuptial feeding, although common in the insect world, varies greatly in its form and function. Here, we test the function of the hemolymph nuptial gift in the southern ground cricket, Allonemobius socius, and attempt to determine if it functions as parental investment or mating effort. We manipulated the number of gifts a female received during courtship (one vs. none). We also recorded other aspect of courtship, such as feeding duration and spermatophore attachment duration. Female fecundity was measured for 7 d post‐mating. Our results indicate that female egg laying is significantly higher when a gift is provided, but the increase in egg laying is not related to gift size. In addition, the lack of a gift does not affect the male's ability to transfer a spermatophore. Together, these data suggest that the nuptial gift acts as parental investment and not as mating effort.     

Ejaculate size in bushcrickets: the importance of being large

Sexual size dimorphism is common in animals. Females, which often experience increased fecundity with size, are generally the larger sex. In males, the pre-copulatory advantages of large size have been extensively investigated. However, in polyandrous species, large male size may also be advantageous after copulation due to sperm competition. Male size co-varies with ejaculate size and increased fertilization success in many insects. Large male size can also be important for production of nuptial gifts enhancing female fecundity. In this study, the relative importance of male size for ejaculate and nuptial gift production is assessed in 20 bushcricket species (Orthoptera: Tettigoniidae). Relative male size is found to correlate with increased ejaculate size across taxa. In contrast, no association is found between relative male size and the size or quality of the nuptial gift. These findings indicate that selection for increased ejaculate volumes as a response to sperm competition may act to promote large male size in insects.     

SPERMATOPHORE SIZE IN BUSHCRICKETS: COMPARATIVE EVIDENCE FOR NUPTIAL GIFTS AS A SPERM PROTECTION DEVICE

During courtship and copulation, males of many insect species provide the female with a nuptial gift of a prey item or synthesized material. These gifts may be explained as a form of paternal investment by increasing female reproductive output, or in terms of mating effort by increasing male fertilization success. These explanations, while not mutually exclusive, are controversial. While experimental studies examine the maintenance of nuptial gifts in single species, comparative studies are required to indicate more general evolutionary trends. Male bushcrickets provide females with a nuptial gift, a spermatophylax, which is transferred to females at mating along with the sperm-containing ampulla. Analysis of comparative data of 28 species of bushcrickets (Orthoptera: Tettigoniidae), reveals that male spermatophore size (spermatophylax and ampulla weight) is positively correlated with female refractory period, which, in turn, correlates with male fertilization success. Moreover, gift size (the spermatophylax) covaries with ejaculate size (the ampulla), which is consistent with the hypothesis that it serves as a sperm protection device. In contrast, there is no significant correlation between any measure of female fecundity and male spermatophylax size. This indicates that the variation in spermatophore size among bushcrickets is better explained by a mating-effort function than a paternal investment function.     

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.