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.     

An invasion of cheats; the evolution of worthless nuptial gifts

Nuptial gifts are food items or inedible tokens that are transferred to females during courtship or copulation . Tokens are of no direct value to females, and it is unknown why females require such worthless gifts as a precondition of mating. One hypothesis is that token giving arose in species that gave nutritious gifts and males exploited female preferences for nutritional gifts by substituting more easily obtainable but worthless items. An invasion of such behavior would require that females accept the substitute gift and copulate for a period of time similar to that with genuine gifts. We show that both these prerequisites are met in the dance fly Rhamphomyia sulcata, in which females normally accept a nutritious gift. We removed the gift from copulating pairs and replaced it with either a large or small prey item or inedible token. We found that although pairs copulated longest with a large genuine gift, the tokens resulted in copula durations equivalent to those with a small genuine gift. We also observed that males that returned to the lek with tokens re-paired successfully. These findings suggest that female behavior in genuine gift-giving species is susceptible to the invasion of male cheating on reproductive investment.     

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.     

Do Feeding Resources Induce the Adoption of Resource Defence Polygyny in a Lekking Butterfly?

Among polygynous species, males often compete for the possession of mating sites to increase their reproductive success. Weaker individuals frequently adopt alternative non‐territorial mate‐locating tactics, but the adoption of alternative territorial tactics may also occur. Although alternative tactics with territory defence are less common in arthropods, factors that drive its adoption may provide information to understand the organization of different territorial mating systems in the group. Here we investigate the adoption of resource‐based territoriality as an alternative to a non‐resource‐based one by males of the butterfly Paryphthimoides phronius. Male P. phronius commonly defend sunny clearings lacking feeding resources in the forest edge (non‐resource‐based territoriality). However, after experimentally offering fermenting fruit in previously undefended sites, we showed that males also adopt a resource defence tactic. Males in territories with fermenting fruits apparently feed on this resource when they are not defending the territory. However, males in sites without resources did not migrate to territories with resources when given the opportunity. To our knowledge, this is the first experimental investigation to show a non‐resource‐ and an alternative resource‐based mate‐locating tactic in a butterfly. We suggest that this behavioural flexibility may represent an important step to understand the ecological factors responsible for the organization and evolution of different territorial mating systems in insects.     

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.     

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.     

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.     

Operational sex ratio and resource defence as predictors of the mating system in European bitterling

Operational sex ratio (OSR), the ratio of sexually active males to fertilizable females in a population, plays a central role in the theory of mating systems by predicting that the intensity of male–male competition and the degree of sexual selection increases as the OSR becomes increasingly male biased. At high values of OSR, however, resource defence theory predicts the breakdown of territoriality and a shift towards scramble competition with a decrease in sexual selection. The direction that correlations between OSR and resource competition and variance in mating success will take depends on the biology of the species of interest. We investigated the effects of male population density and male‐biased operational sex ratio on male mating tactics shown by a freshwater fish, the European bitterling, Rhodeus sericeus . This species spawns inside living unioneid mussels. Large males defended territories, were aggressive towards conspecifics under equal sex ratios and monopolized pair spawnings with females. The mating tactic, however, changed at high male density where large males ceased to be territorial and instead competed with groups of smaller males to release sperm when females spawned. This change in male behaviour from pair to group spawning has two ramifications for sexual selection. The intensity of sexual selection and variance in male mating success decrease, and the form of sexual competition changes from resource‐ to sperm competition. Thus, the use of alternative mating tactics renders the OSR unable to predict the direction of resource competition and variance in male mating success at high densities.     

Female mating status affects male mating tactic expression in the wolf spider Rabidosa punctulata

Males and females have conflicting interests on the frequency and outcomes of mating interactions. Males maximize their fitness by mating with as many females as possible, whereas choosy females often reduce receptivity following copulation. Alternative male mating tactics can be adaptive in their expression to a variety of mating contexts, including interactions with a relatively unreceptive mated female. Male Rabidosa punctulata wolf spiders can adopt distinctive mating tactics when interacting with a female, a complex courtship display, and/or a more coercive direct mount tactic that often involves grappling with females for copulation. In this study, we set up female mating treatments with initial trials and then paired mated and unmated females with males to observe both female remating frequencies and the male mating tactics used during the interactions. Males adopted different mating tactics depending on the mating status of the female they were paired with. Males were more likely to adopt a direct mount tactic with already-mated females and courtship with unmated females. Already-mated females were considerably less receptive to males during experimental trials, although they did remate 34% of the time, the majority of which were with males using a direct mount tactic. Whereas males adjusting to these contextual cues were able to gain more copulations, the observation of multiple mating in female R. punctulata introduces the potential for sperm competition. We discuss this sexual conflict in terms of the fitness consequences of these mating outcomes for both males and females.     

Directional selection on body size but no apparent survival cost to being large in wild New Zealand giraffe weevils

When an individual's reproductive success relies on winning fights to secure mating opportunities, bearing larger weapons is advantageous. However, sexual selection can be extremely complex, and over an animal's life the opportunity to mate is influenced by numerous factors. We studied a wild population of giraffe weevils (Lasiorhynchus barbicornis) that exhibit enormous intra and intersexual size variation. Males bear an elongated rostrum used as a weapon in fights for mating opportunities. However, small males also employ sneaking behavior as an alternative reproductive tactic. We investigated sexual selection on size by tracking individual males and females daily over two 30‐day periods to measure long‐term mating success. We also assessed how survival and recapture probabilities vary with sex and size to determine whether there might be a survival cost associated with size. We found evidence for directional selection on size through higher mating success, but no apparent survival trade‐off. Instead, larger individuals mate more often and have a higher survival probability, suggesting an accumulation of benefits to bigger individuals. Furthermore, we found evidence of size assortative mating where males appear to selectively mate with bigger females. Larger and more competitive males secure matings with larger females more frequently than smaller males, which may further increase their fitness.     

Influence of Nutrition on Courtship and Mating in the Scorpionfly Panorpa cognata (Mecoptera, Insecta)

Scorpionflies have been used as model organisms for the study of alternative male mating tactics as well as sexual conflict and coercive mating. Here we describe the courtship and mating behaviour of the scorpionfly Panorpa cognata at different levels of nutrition. Alternative mating tactics in scorpionflies involve nuptial food gifts, and we expected an effect of nutrient availability and male individual condition on the relative frequency of these mating tactics. Subsequent to female attraction by means of male pheromonal emission (calling) and a conspicuous pairing prelude, the majority of matings were initiated by male secretion of one relatively large salivary mass on which females feed during copulation. Usually, males produced only a single salivary mass per mating, and the copulation was terminated after the female had consumed the salivary mass. Alternatively, in 40% of the copulations, males offered females a dead arthropod as nuptial gift. However, these matings were neither preceded by male calling nor by the pairing prelude. Copulations with no gifts were extremely rare, and forced copulations were absent. The manipulation of the clamp‐like notal organ used by male scorpionflies in coercive matings had no effect on the duration of copulation, suggesting that P. cognata males are not able to enforce longer matings. Copulations involving salivary mass gifts were significantly longer than copulations with prey provided as gifts. Although contrary to our expectations, nutrition had no effect on the relative frequency of the different male mating tactics, it had several effects on courtship and mating. First, well‐fed individuals copulated significantly more often, both with prey and salivary secretions, than individuals with limited nutrient resources available. This was true for both sexes, although the effect was stronger for males. Higher availability of nutrients decreased the time until male and female sexual maturity and increased male calling duration per day. Furthermore, high nutrient availability decreased the duration of the pairing prelude, and consequently pairs started copulating earlier at night in the high nutrient treatment.     

Alternative mate-finding tactics in a non-territorial damselfly (Odonata: Coenagrionidae)

Males of the non-territorial damselfly Enallagma hageni have two alternative tactics for finding mates: (1) they search the banks of the pond for unmated females (searching tactic), or (2) wait at oviposition sites for females that resurface prematurely from underwater oviposition (waiting tactic). Although the searching tactic yielded more fertilizations than the waiting tactic, for time invested, the waiting tactic became increasingly successful later in the reproductive season due to changes in female oviposition behaviour. The two tactics can be maintained in the population because males can mate by the waiting tactic during the afternoon when few females are available to searchers. Among males visiting the breeding site an equal number of times, males mating by a mixture of tactics were as successful as males mating only by the main tactic. Because marked males were found to use both tactics, these behaviours are interpreted as evidence of behavioural plasticity within individuals, representing one conditional evolutionary strategy.     

The Consequences of Predation Risk on the Male Territorial Behavior in a Solitary Bee

Territorial males may adopt a mating tactic that yields greater reproductive success but that at the same time increases the risk of predation. Plasticity in reproductive behavior can reflect a balance between sexual selection and natural selection. In this study, we sought to verify the effect of predation risk on territorial behavior of males of the solitary bee Ptilothrix fructifera (Apidae). Males of the species employ alternative mating tactics and can be territorial in defense of larval food sources. By manipulating predator models in the field, we tested whether (1) males avoid perch flowers containing predator models; (2) males alternate between mating tactics when their territory is associated with a predation risk; and (3) female foraging on flowers in a territory is altered in the presence of a predator model. We measured the responses of males and females in flowers containing and not containing a model of a spider or a stuffed bird. The results show that territorial males of P. fructifera alter their territorial behavior when faced with a high risk of predation. They do not abandon their territory or change to a non‐territorial mating tactic, but instead change the use of their territory, avoiding flowers containing predator models or perching on other flowers when the previous flower presented a potential predation risk. Female P. fructifera decreases the frequency of their visits to flowers and the length of time spent there in the presence of a spider model. In short, in the face of predation risk, females and males alter their behaviors at the cost of less efficient foraging and searching for partners, respectively.     

Biting off more than you can chew: sexual selection on the free amino acid composition of the spermatophylax in decorated crickets

Nuptial food gifts function to enhance male fertilization success, but their consumption is not always beneficial to females. In decorated crickets, the spermatophore transferred at mating includes a gelatinous mass, the spermatophylax, which is consumed by females after mating. However, females often discard spermatophylaxes shortly after mating, whereupon they terminate sperm transfer. We hypothesized that females discard gifts based on their assessment of the gift itself, and specifically the composition of free amino acids. We tested this hypothesis by comparing spermatophylaxes discarded by females after mating with those that were destined to be fully consumed, and employed multivariate selection analysis to quantify the strength and form of multivariate sexual selection operating on the free amino acid composition of gifts. The analysis yielded a saddle-shaped fitness surface with two local peaks. Different amino acid profiles appear to elicit continued feeding on the spermatophylax either because they offer the same level of gustatory appeal, or because they differentially affect both the gustatory appeal and texture of the spermatophylax. We conclude that the gustatory response of females to males' nuptial food gifts represents an important avenue of post-copulatory mate choice, imposing significant sexual selection on the free amino acid composition of the spermatophylax.     

The Resource-Based Mating System of the Mediterranean Pollen Wasp Ceramius fonscolombei Latreille 1810 (Hymenoptera, Vespidae, Masarinae)

Males of C. fonscolombei patrol and perch at water collection sites or at plants of Reseda, both of which are important resources for female brood care. The mating system can be classified as resource defense polygyny modified by the existence of alternative male mating tactics. Occupying temporary territories at watercollection sites constitutes the primary tactic which is more profitable for larger males. The secondary tactic of patrolling at flowers provides a nonaggressive alternative through which smaller males gain at least some mating success. Males at water collection sites occupy considerably smaller ranges but spend a higher proportion of time patrolling than males at flowers. They frequently grapple with other males, an activity that is absent at flowers. Males at water collection sites copulate about 2.5 times more frequently than males at flowers. The copulation frequency of the males at water collection sites is positively correlated with their body size, while copulation frequency is negatively correlated with body size at flowers. Males patrolling at water collection sites and males patrolling at flowers do not differ in body size, indicating that the decision between alternative mating tactics is not made relative to body size but is influenced by other factors.     

Secondary sexual characters and sperm traits in coho salmon Oncorhynchus kisutch

A study was undertaken to examine secondary sexual characters (spawning colouration and overall body size) in relation to sperm metrics in one alternative reproductive tactic of coho salmon Oncorhynchus kisutch : large hooknose males that spawn in dominance-based hierarchies. Males with less intense red spawning colouration had higher sperm velocities than males with darker red spawning colouration. There was no relationship between male body size and sperm metrics. These results suggest that within an alternative reproductive tactic, variation in sperm competition intensity may select for a trade-off between investment in sexual colouration and sperm quality.     

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.     

Mating tactics of male feral goats (Capra hircus): risks and benefits

Intense competition between males for reproduction has led to the evolution of alternative mating tactics (AMTs). Feral goat males usually use a tactic called tending, in which they defend oestrous females from other males. Males may also use a second mating tactic called coursing, in which they gain access to oestrous females by disturbing a tending pair. Herein, we examine estimated mating success (EMS) and risks of using these tactics. Tending was only used by mature (≥4 years old), higher-ranking males and accounted for 75% of EMS. Coursing was used by males of all ages and dominance ranks, and accounted for 25% of EMS. Using coursing, male kids achieved 8% of EMS. Mature males achieved 92% of EMS. Both age and dominance rank were related to EMS, but age was not important after its relationship with dominance was controlled. Tending bouts were, on average, ca. 30 min long, while coursing bouts only averaged ca. 2 min. Males were more likely to suffer a butt while coursing than while tending, and formerly tending males were responsible for most butts. Kids that coursed had the highest risk of being butted. In most AMTs, there are reductions in the risks in relation to low fitness benefits. However, we found that the risks of butts during coursing were high, while our evidence suggests that the EMS was probably low. Nevertheless, the existence of an effective AMT in male feral goats may have an important influence on the intensity of sexual selection and the effective population size.     

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.     

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.