Male Nuptial Gifts Research Articles

Sexually antagonistic coevolution of the male nuptial gift and female feeding behaviour in decorated crickets.

The evolution of nuptial gifts has traditionally been considered a harmonious affair, providing benefits to both mating partners. There is growing evidence, however, that receiving a nuptial gift can be actively detrimental to the female. In decorated crickets (Gryllodes sigillatus), males produce a gelatinous spermatophylax that enhances sperm transfer but provides little nutritional benefit and hinders female post-copulatory mate choice. Here, we examine the sexually antagonistic coevolution of the spermatophylax and the female feeding response to this gift in G. sigillatus maintained in experimental populations with either a male-biased or female-biased adult sex ratio. After 25 generations, males evolving in male-biased populations produced heavier spermatophylaxes with a more manipulative combination of free amino acids than those evolving in female-biased populations. Moreover, when the spermatophylax originated from the same selection regime, females evolving in male-biased populations always had shorter feeding durations than those evolving in female-biased populations, indicating the evolution of greater resistance. Across populations, female feeding duration increased with the mass and manipulative combination of free amino acids in the spermatophylax, suggesting sexually antagonistic coevolution. Collectively, our work demonstrates a key role for interlocus sexual conflict and sexually antagonistic coevolution in the mating system of G. sigillatus.

Female state and condition-dependent chemical signaling revealed by male choice of silk trails

Abstract Male mate choice is predicted in systems with high costs of mating, as for those with male nuptial gifts and/or sexual cannibalism. We ask whether males of the nuptial gift-giving spider Pisaura mirabilis exert preferences for mates varying in their reproductive potential based on chemical information during mate search. Males were presented with binary trails consisting of silk lines and substrate-borne chemicals deposited while females were walking, from females varying in 1) body condition (high vs. low), 2) developmental state (subadult vs. adult), and 3) mating state (unmated vs. mated). If female chemical signaling co-varies with individual state, we expect males to choose trails of females that are 1) in higher body condition, indicating higher fecundity, 2) adults, which can successfully reproduce, and 3) unmated, to avoid sperm competition. We show that female signaling is condition-dependent, with males being more likely to follow trails of higher body condition females, but not dependent on female mating state. Males also tended to prefer trails of adults over subadults. Choice did not depend on male individual body condition. Our findings suggest costs to chemical signaling in nutritionally deprived females, often considered negligible, and their potential as reliable indicators of individual quality. Selection may favor male preferences for more fecund partners given the energetic investment nuptial gifts entail. Nutritional and reproductive benefits of multiple mating to females and high share of paternity for males, may instead select against signaling of female mating state, and/or male discrimination and choice.

Paternity sharing in insects with female competition for nuptial gifts.

Male parental investment is expected to be associated with high confidence of paternity. Studies of species with exclusive male parental care have provided support for this hypothesis because mating typically co-occurs with each oviposition, allowing control over paternity and the allocation of care. However, in systems where males invest by feeding mates (typically arthropods), mating (and thus the investment) is separated from egg-laying, resulting in less control over insemination, as male ejaculates compete with rival sperm stored by females, and a greater risk of investing in unrelated offspring (cuckoldry). As strong selection on males to increase paternity would compromise the fitness of all a female's other mates that make costly nutrient contributions, paternity sharing (males not excluded from siring offspring) is an expected outcome of sperm competition. Using wild-caught females in an orthopteran and a dipteran species, in which sexually selected, ornamented females compete for male nuptial food gifts needed for successful reproduction, we examined paternity patterns and compared them with findings in other insects. We used microsatellite analysis of offspring (lifetime reproduction in the orthopteran) and stored sperm from wild-caught females in both study species. As predicted, there was evidence of shared paternity as few males failed to sire offspring. Further support for paternity sharing is the lack of last-male sperm precedence in our study species. Although paternity was not equal among sires, our estimates of paternity bias were similar to other insects with valuable nuptial gifts and contrasted with the finding that males are frequently excluded from siring offspring in species where males supply little more than sperm. This suggests paternity bias may be reduced in nuptial-gift systems and may help facilitate the evolution of these paternal investments.

Evolution of male nuptial gift and female remating: A quantitative genetic model

In some species of separate sexes, males present a nuptial gift containing nutrition to their mate. Producing a large nuptial gift is a considerable cost to the male, but it may improve his siring success if the female reduces the likelihood to accept another male after receiving a large gift. The female may receive a direct benefit by accepting another male who provides an additional nuptial gift. Additionally, the female may receive an indirect fitness benefit via laying offspring sired by a male who is able to produce a large nuptial gift. We formalized the multivariate quantitative genetics model describing the coevolution of the size of nuptial gift produced by the male (x) and the female’s propensity to engage in remating (y). We analyzed the model focusing two cases: [1] remating females receive no indirect fitness benefit, but enjoy direct benefit of nutrition; and [2] remating females receive no direct benefit, but enjoy an indirect fitness benefit due to a positive genetic correlation of x and y, which is possible if random mutations tend to make males produce small nuptial gifts. In both cases, the stable evolutionary equilibrium with neither nuptial gift nor remating (x-=y-=0) always exists. Another stable equilibrium may exist in which male produces nuptial gifts (x->0) and female engage in multiple mating (y->0). We discussed implications to the sexual conflict.

Correlated sexual selection on male genitalia, copulatory performance and nuptial gifts in a bushcricket (Orthoptera: Tettigoniidae) indicated by allometric scaling

Abstract We adopt an allometric framework of scaling relationships for comparison between mating-related traits in the middle European bushcricket Roeseliana roeselii (Hagenbach, 1822). Eight characters, covering ontogenetic fitness (size traits; fixed at final moult), male condition (mass traits) and mating motivation (reproductive behaviours), were analysed in unrestricted matings and in matings involving genital manipulation. Shortening the male titillators had no effect on mating-related traits in males. However, titillators, known to be under sexual selection, scale hyperallometrically, with larger males possessing proportionally longer titillators, performing more titillator movements and exhibiting a reduced duration of copulation. Scaling was also hyperallometric for spermatophore mass, with larger males being heavier and transferring heavier nuptial gifts. Both titillator length and spermatophore mass might be condition-dependent indicators, because their variances were nearly twice as large those of body size or body mass. Mass traits were also dynamic, increasing by 11% for male body mass and 17% for spermatophore mass between the first and second matings. Sexual selection by female choice seems to favour larger trait size in the bushcricket R. roeselii, acting in concert on titillator length, intensity of titillator movements and spermatophore mass.

Does silk mediate chemical communication between the sexes in a nuptial feeding spider?

Chemical signals play a crucial role in reproduction as a means for locating mates and/or gaining information about their quality, ultimately affecting mating system dynamics and mate choice. In spiders, one of the potential sources of chemical signalling is silk. However, while female silk is known to attract mates and/or elicit courtship, due to sex-specific roles in mate searching, male silk-related signals are often neglected. In the hunting spider Pisaura mirabilis (Pisauridae), both sexes leave silk draglines during movements while males additionally use silk to wrap nuptial gifts (food donations to females at mating). We explored the potential for both silk types (draglines and gift silk) to release signals and tested the hypothesis that chemical compounds bound to gifts’ silk serve to elicit female attraction. We conducted behavioural choice assays for dragline and gift silk, and their putative transmission mode (airborne or contact) by testing (i) male and female attraction towards draglines of the opposite sex and (ii) female attraction towards gift silk. Whereas males were attracted to female draglines (contact cues), females did not respond to male silk of any type. We suggest that females use draglines for advertisement to secure copulation and foraging of nuptial gifts. If these signals ease male mate searching, attractive male draglines are unnecessary. Overall, males may not invest in chemical stimulation but rather exploit female foraging interests through gift giving. Alternatively, they may release signals that prime other female sexual behaviours or towards which females may have evolved resistance. Animals commonly use chemical signals to communicate during reproduction, and spiders have the potential to release such signals from their silk. We investigated whether two silk types, draglines released during movements and silk covering male nuptial gifts (prey offered to females at mating) are attractive to the opposite sex in a hunting spider. While males were attracted to female draglines, females did not respond to male silk of any type. Females may be using silk to advertise themselves to secure matings and food through reception of nuptial gifts. If males can successfully locate females, attracting females through draglines may be unnecessary. The finding that males do not release attractant signals in the silk cover of their nuptial gifts further suggests that rather than attempting to increase their attractiveness by using chemical stimulation, males may be uniquely exploiting females’ interest in food through gift giving behaviour.

Prolonged copulations as an alternative to male nuptial gift investment in the bushcricket Letana inflata (Orthoptera: Tettigoniidae)

In most bushcricket species, the male transfers a nuptial gift to the female during mating, consisting of a gelatinous spermatophylax attached to the paired ampulla with the sperm. The spermatophylax acts as a sperm protection device; during its consumption, the sperm are transferred into the female’s spermatheca. Males of the bushcricket Letana inflata (Brunner von Wattenwyl, 1878) show strongly extended copulation duration. When the pair finally separates, only an ampulla is visible at the females’ genital opening, but no spermatophylax. To better understand copulation dynamics in the absence of a spermatophylax, we studied copula duration and sperm transfer pattern. Our results show that in Letana inflata the missing spermatophylax is replaced by extended copulation, securing the transfer of sperm into the spermatheca.

Determinants of reproductive success across sequential episodes of sexual selection in a firefly.

Because females often mate with multiple males, it is critical to expand our view of sexual selection to encompass pre-, peri- and post-copulatory episodes to understand how selection drives trait evolution. In Photinus fireflies, females preferentially respond to males based on their bioluminescent courtship signals, but previous work has shown that male paternity success is negatively correlated with flash attractiveness. Here, we experimentally manipulated both the attractiveness of the courtship signal visible to female Photinus greeni fireflies before mating and male nuptial gift size to determine how these traits might each influence mate acceptance and paternity share. We also measured pericopulatory behaviours to examine their influence on male reproductive success. Firefly males with larger spermatophores experienced dual benefits in terms of both higher mate acceptance and increased paternity share. We found no effect of courtship signal attractiveness or pericopulatory behaviour on male reproductive success. Taken together with previous results, this suggests a possible trade-off for males between producing an attractive courtship signal and investing in nuptial gifts. By integrating multiple episodes of sexual selection, this study extends our understanding of sexual selection in Photinus fireflies and provides insight into the evolution of male traits in other polyandrous species.

The monogamous reproductive strategy in Lepidoptera

On the basis of literary sources and experimental data, the advantages of a monogamous reproductive strategy are analyzed. Monogamous species of Lepidoptera have no postcopulative mechanisms of control over the success of reproductive sperm competition, cryptic female choice, and, probably, the male's nuptial gift. Selection of the sex partner and of the quality of the future generation is determined by the precopulative and copulative mechanisms of the reproductive behavior, which include chemocommunication and a "lock-and-key" mechanism. In an experiment with one male and one female, the quota of successful mating can depend on the morphological complication of the genital apparatus of males. Cases are considered of repeated mating for some, usually monogamous, species. In comparison with the variant of the experiment with one male x one female, the frequency of repeated mating increases with the addition of two males to one female but decreases in the presence of two females with one male. A possible reason for the appearance of repeated mating may be the weight of the insect's body exceeding the average.

Female bushcrickets fuel their metabolism with male nuptial gifts

In many arthropods, such as bushcrickets, males donate protein-rich nuptial gifts-so-called spermatophores-to females, which females ingest while the sperm enter the female's reproductive tract. Previously, it was shown that females route spermatophore nutrients over the course of hours and days to egg production or body synthesis. We investigated whether female bushcrickets fuel their metabolism with spermatophores immediately after consumption. We fed two male groups diets that were either enriched or depleted in 13C, and then tracked the isotopic changes in exhaled breath in female bushcrickets after spermatophore consumption. Within 3 hours, the stable carbon isotope ratio (delta13C) of female breath converged on the ratio of the male donor of the nuptial gift. This supports the idea that females quickly routed nutrients to metabolism, receiving immediate benefits from spermatophore feeding.

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.

MALE COURTSHIP ATTRACTIVENESS AND PATERNITY SUCCESS INPHOTINUS GREENIFIREFLIES

Although female mate choice and male sperm competition have separately attracted much attention, few studies have addressed how precopulatory and postcopulatory episodes of sexual selection might interact to drive the evolution of male traits. In Photinus fireflies, females preferentially respond to males based on their bioluminescent courtship signals, and females gain direct benefits through male nuptial gifts acquired during multiple matings over several nights. We experimentally manipulated matings of P. greeni fireflies to test the hypothesis that postcopulatory paternity success might be biased toward males that are more attractive during courtship interactions. We first measured male courtship attractiveness to individual females using field behavioral assays. Females were then assigned to two double-mating treatments: (1) least attractive second male-females were first mated with their most attractive male, followed by their least attractive male, or (2) most attractive second male-females mated with males in reverse order. Larval offspring produced by each female following these double matings were genotyped using random amplified polymorphic DNA (RAPD) markers, and male paternity was determined. Contrary to prediction, firefly males that were more attractive to females based on their bioluminescent courtship displays subsequently showed significantly lower paternity, reflecting possible male trade-offs or sexual conflict. Differences in male paternity were not related to male body condition, testes or accessory gland mass, or to variation in female spermathecal size. Additionally, this study suggests that changes in phenotypic selection gradients may occur during different reproductive stages. These results indicate that it is crucial for future studies on sexual selection in polyandrous species to integrate both precopulatory and postcopulatory episodes to fully understand the evolution of male traits.

Temperature and host species affect nuptial gift size in a seed‐feeding beetle

1 In many insects species, males contribute large nutritional gifts to females during mating, generally as seminal fluids (ejaculates) or spermatophores. These nuptial gifts can affect both male and female fitness, and can mediate selection on male body size. However, it is unclear how environmental variables, such as temperature and diet, affect gift size and the consequences of gift size for male and female fitness. 2 We examine how temperature and rearing host affect male nuptial gift size (both total ejaculate size and the proportion of a male's mass allocated to his seminal fluids), and the relationship between gift size and female reproduction, in two populations of the seed-feeding beetle Callosobruchus maculatus. 3 Males reared at lower temperature (20 °C) produced substantially larger ejaculates than males reared at higher temperatures (25, 30 and 35 °C). However, males allocated a smaller proportion of their body mass to their ejaculate at the lowest temperature compared with other temperatures. This effect of temperature on male allocation to their ejaculates mirrored the effect of temperature on female body size – male ejaculate size remained a relatively constant proportion of their mate's body mass across temperatures. 4 Rearing host also affected male ejaculate size but the magnitude and direction of the host effect differed between populations. 5 Rearing temperature affected the relationship between male body mass and ejaculate size. Temperature also affected the relationship between female body mass and fecundity. The relationship between male body mass and ejaculate size was significantly lower when beetles were reared on cowpea than when beetles were reared on azuki or mung. 6 We found no evidence that male body size or nuptial gift size affected female fecundity in either population of C. maculatus. We thus propose that the effect of nuptial gift size on male fitness is through a reduction in female mating frequency and thus increased paternity for males producing larger nuptial gifts.

The Energetics of Trading Nuptial Gifts for Copulations in Katydids

During copulation, male Isophya kraussi transfer a large nuptial gift to females. In this study, we hypothesized that the energy content of spermatophores should meet the energy requirements of both body maintenance and egg production of females. We measured the field metabolic rate of male and female I. kraussi using the doubly labeled water method and the energy content of spermatophores and male bodies with microbomb calorimetry. The energy content of male nuptial gifts averaged 0.66+/-0.09 kJ, approximately 20% of the total body energy content of male I. kraussi (3.24+/-0.26 kJ). Field metabolic rates averaged 0.41+/-0.17 kJ d(-1) (n = 8) for males and 0.30+/-0.15 kJ d(-1) (n = 5) for female I. kraussi. Thus, the energy content of spermatophores exceeded the daily energy requirements of existence in male I. kraussi. A single nuptial gift provides for all energy requirements of females for 1 or 2 d, depending on their activity, egg production, and ambient temperature. Because the shortest known remating interval of female katydids varies between 1 and 3 d, female I. kraussi could theoretically exist exclusively on spermatophores to meet their nutritional requirements.

The effect of male sodium diet and mating history on female reproduction in the puddling squinting bush brown Bicyclus anynana (Lepidoptera)

The males of butterflies transfer a spermatophore to the female during mating that can contain nutrients enhancing the reproductive potential of their partners. The nutrients transferred by males can be derived from both larval and adult feeding. These nutrients may be depleted by multiple matings. An apparent difference in adult feeding behaviour between the sexes is puddling on mud, dung and carrion, which in most butterfly species is exclusively a male behaviour. A possible explanation for this division in feeding behaviour is that nutrients derived from puddling by males are transferred to the female during mating. Here, we test this hypothesis in the African fruit-feeding butterfly Bicyclus anynana. We varied the male nuptial gift by (1) feeding males either a diet with or without sodium, and (2) varying the number of previous successful copulations by remating males up to five times on consecutive days. The results show both a strong effect of order of mating on the mating duration, and an individual effect with some males typically copulating for a shorter time than others. The effects on female reproduction were, however, minimal. The total number of eggs per female and the sodium content of the eggs did not differ significantly between diets, nor were they affected by the mating histories of the males. Eggs showed a non-significant lower hatching for females partnered by a male who had already mated several times. There was an indication of an interaction with male diet: the sodium treatment showing a decline in egg hatchability with order number of male mating, whilst the control treatment showed a constant hatchability. The results are discussed in relation to determinants of male gift-giving strategy and to other potential explanations for a restriction of puddling to males in butterflies.

Material and genetic benefits of female multiple mating and polyandry

The maintenance of female polyandry has traditionally been attributed to the material (direct) benefits derived from male mating resources (e.g. nuptial gifts) accrued by multiple mating. However, genetic (indirect) benefits offer a more robust explanation since only polyandrous, not monandrous, females may gain both material benefits from multiple mating and genetic benefits from multiple sires. Discriminating between material and genetic benefits is essential when addressing the mechanism by which polyandry is adaptively maintained, but are difficult to disentangle because they affect fitness in similar ways. To test the hypothesis that genetic benefits maintain polyandry, we compared four components of fitness (longevity, fecundity, hatching success and survivorship) between monandrous and polyandrous females in the ground cricket, Allonemobius socius. We discovered that females derived nongenetic benefits from mating multiply, in that the magnitude of the nuptial gift was positively associated with the number of eggs produced. However, polyandrous females had over a two-fold greater hatching success and a 43% greater offspring survivorship, leading to a significantly higher relative fitness than the monandrous strategy. These results were independent of the confounding effects of material benefits, implying that genetic contributions play a large role in the maintenance of polyandry and potentially in the antagonistic coevolutionary relationship between polyandry and male nuptial gifts. Copyright 2002 Published by Elsevier Science Ltd on behalf of The Association for the Study of Animal Behaviour

Nuptial Gifts, Resource Budgets, and Reproductive Output in a Polyandrous Butterfly

Many female insects receive material during mating, referred to as “nuptial gifts,” that may increase the female’s resource budget. This investigation examines how nuptial gifts influence female nitrogen and carbon budgets in a polyandrous butterfly, Pieris napi. During mating, a virgin male of this species transfers a large and nutritious ejaculate containing 14% nitrogen by dry mass. The amount of nitrogen transferred is equivalent to that in ∼70 eggs. Females use the male-transferred nutrients to increase their pool of nutrients used for egg production and show a positive relationship between amount of ejaculate material received and lifetime reproductive output. It is clear that for multiply mated females, nitrogen derived from male nuptial gifts is essential for a balanced nitrogen budget. As in earlier studies, female thorax mass decreased with age, indicating that old females of P. napi are able to use more of the resources from their thorax than young females. Since male-transferred material also increases female longevity, multiply mated females also use more of their resources from the thorax. Consequently, multiply mated females have a relatively higher reproductive investment than singly mated females, i.e., they transform a larger part of their body reserves to egg production. These results are important for studies that involve male-transferred nutrients in female life history patterns as well as for investigations of links between nuptial gifts and sexual selection theory. When the value of nuptial gifts is determined only on the nutritional value of the gift itself rather than the function within the female, there is an obvious risk for incorrect conclusions.

NUPTIAL GIFTS, RESOURCE BUDGETS, AND REPRODUCTIVE OUTPUT IN A POLYANDROUS BUTTERFLY

Many female insects receive material during mating, referred to as “nuptial gifts,” that may increase the female’s resource budget. This investigation examines how nuptial gifts influence female nitrogen and carbon budgets in a polyandrous butterfly, Pieris napi. During mating, a virgin male of this species transfers a large and nutritious ejaculate containing 14% nitrogen by dry mass. The amount of nitrogen transferred is equivalent to that in ∼70 eggs. Females use the male-transferred nutrients to increase their pool of nutrients used for egg production and show a positive relationship between amount of ejaculate material received and lifetime reproductive output. It is clear that for multiply mated females, nitrogen derived from male nuptial gifts is essential for a balanced nitrogen budget. As in earlier studies, female thorax mass decreased with age, indicating that old females of P. napi are able to use more of the resources from their thorax than young females. Since male-transferred material also increases female longevity, multiply mated females also use more of their resources from the thorax. Consequently, multiply mated females have a relatively higher reproductive investment than singly mated females, i.e., they transform a larger part of their body reserves to egg production. These results are important for studies that involve male-transferred nutrients in female life history patterns as well as for investigations of links between nuptial gifts and sexual selection theory. When the value of nuptial gifts is determined only on the nutritional value of the gift itself rather than the function within the female, there is an obvious risk for incorrect conclusions.

Decoupling of reproductive rates and parental expenditure in a polyandrous butterfly

Current theory postulates that the operational sex ratio (OSR) determines the relative degree of mating competition in the two sexes and is in turn influenced by a sexual difference in the potential reproductive rate (PRR) denned as I/time out, where time out is the time an individual must spend recovering from a bout of mating activity and/or caring for offspring. In bushcricket mating systems where males provide females with a nuptial gift, relative energy expenditure in of&pring influences the PRR of males and females and underlies a diet-mediated shift in the OSR. Here we investigated if there is a similar positive relationship between relative parental nutrient expenditure in of&pring and PRR in the polyandrous butterfly Pieris napi, where female fecundity is strongly dependent on male nuptial gifts at mating. By varying the amount of nutrients females receive at mating and relating this to number of of&pring produced, we show that male P. napi have, on average, a nutrient expenditure in of&pring equaling that of females. In spite of this, the male reproductive rate is 8-13 times higher than that of females. Hence the relative degree of parental expenditure in of&pring is largely decoupled from the degree of mating competition in P. napi. Two alternative explanations are advanced to account for the difference between the butterfly and the bushcricket mating systems.

Protein content of spermatophores in relation to monandry/polyandry in butterflies

The evolution of a mating system, and specifically mating frequency, is dependent on the costs and benefits to both sexes of mating once or several times. In butterflies, males transfer a spermatophore that contains both sperm and accessory gland products. Accessory gland substances contain nutrients which, in some species, females use to increase their reproductive output and longevity. Nutrients contained in these packaged ejaculates represent investment by males in reproduction. Consequently, the nutritional composition of spermatophores may vary depending on the mating system. There are two lines of arguments concerning the evolution of the nutrient content of ejaculates. One hypothesis argues that male nuptial gifts evolved in the context of certainty of paternity and ease of finding mates; thus spermatophores of polyandrous males (with lower certainty of paternity and greater ease of finding mates) should contain less protein than those of monandrous males, since more spermatophores are produced on average. The other hypothesis argues that polyandry evolved in the context of maximization of male transfer of nutrients to females, and hence spermatophores of polyandrous males should contain more protein than those of monandrous males. In an attempt to distinguish between these two hypotheses, we determined how protein content of ejaculates varied with the degree of polyandry in nine species of pierid and two species of satyrid butterflies. We found that both relative ejaculate mass and protein content increased with the degree of polyandry. Hence our results are consistent with the view that polyandry has evolved in the context of male transfer of nutrients to females, and provides another example of a male adaptation to multiple mating in butterflies.