Effect of Adult Feeding on Male Mating Behaviour in the Butterfly, <Emphasis Type="Italic">Bicyclus anynana</Emphasis> (Lepidoptera: Nymphalidae)

Many species of lepidopterans supplement their nectar diet with foods rich in nitrogen and minerals, which are present only in trace amounts in nectar. We examined the effect of adult diet on mating behaviour and spermatophore characteristics in male Bicyclus anynana (Butler, 1879) butterflies, which feed on rotten fruits as adults. We found little effect of adult diet on male reproduction in terms of mating rate and sperm production, although males fed on fruit produced larger spermatophores on their first mating compared to males fed sugar only. We also examined how males allocate sperm across matings. Males ejaculate larger spermatophores during their first mating, and produce spermatophores containing decreasingly fewer non-fertile sperm with number of matings performed. Males that produced more non-fertile sperm on their first mating had reduced lifespan possibly indicating a trade-off between sperm production and adult longevity. It is suggested that adult diet has little affect on male ejaculate production and males feed on fruit to supplement their energetic carbon requirements.     

Spermatophore and Sperm Allocation in Males of the Monandrous Butterfly Pararge aegeria: the Female’s Perspective

In insects, spermatophore production represents a non‐trivial cost to a male. Non‐virgin males have been shown to produce small spermatophores at subsequent matings. Particularly in monandrous species, it may be an issue to receive a sufficiently large spermatophore at the first and typically only mating. Females of the monandrous Speckled wood butterfly Pararge aegeria (L.) produce fewer offspring after mating with a non‐virgin male. After mating, females spend all their active time selecting oviposition sites and typically ignore other males. Here, we show that females did not discriminate between a virgin male and a recently mated male in our laboratory experiments. We demonstrate that the number of eupyrene sperm bundles relative to spermatophore mass differed with subsequent male matings. Males transferred a significantly smaller spermatophore after the first copulation, but the spermatophore mass did not decrease further with subsequent matings. However, the number of eupyrene sperm bundles decreased linearly. Therefore, there was proportionally more eupyrene sperm in the male’s second spermatophore compared with the first and the later spermatophores. Such a pattern has been shown in polyandrous species. Hence, it suggests that differences in sperm allocation strategy between polyandrous and monandrous butterflies may be quantitative rather than qualitative. There was also a tendency for females that had mated with a recently mated male to have higher propensity to remate than did females that had mated with a virgin male. We discuss the results relative to the mating system in P. aegeria, including female remating opportunities in the field and male mate‐locating behaviour.     

Impact of male condition on his spermatophore and consequences for female reproductive performance in the Glanville fritillary butterfly

In butterflies, male reproductive success is highly related to the quality and the size of the spermatophore transferred to the female. The spermatophore is a capsule produced by the male during copulation, which in many species contains sperm in addition to a nuptial gift, and which is digested by the female after copulation. The nuptial gift may contribute to egg production and offspring quality, and in some cases also to female body maintenance. The production of the spermatophore, however, represents a cost for the male and, in polyandrous species, ejaculates are sometimes allocated adaptively across matings. Nonetheless, although the ecological factors affecting the reproductive success of female butterflies have been the topic of numerous studies, little information exists on the factors affecting males’ contribution to reproduction, and the indirect impacts on female fecundity and fitness. We used the Glanville fritillary butterfly, Melitaea cinxia (Linnaeus, 1758) (Nymphalidae), in order to assess variation in male allocation to matings. In this species, smaller males produce smaller spermatophores, but variation in spermatophore size is not correlated with female reproductive success. We show that spermatophore size increases with male age at first mating, decreases with mating frequency and adult food‐deprivation, and is not influenced by developmental food‐limitation. The length of copulation period does not influence the spermatophore size nor influences the polyandrous mating behavior in this species. Male contribution to his spermatophore size is clearly influenced by his condition and adult‐resource at the time of mating. Despite this variation, spermatophore size does not seem to have a direct impact on female reproductive output or mating behavior.     

Nuptial gifts and the use of body resources for reproduction in the green-veined white butterfly Pieris napi

Reproduction in butterflies, as in many holometabolous insects, is usually constrained by the amount of nutrients the animals can collect as juveniles. In polyandric species the females can also supplement their larval-derived reserves with protein-rich donations, so-called nuptial gifts, delivered by the males at mating. Recent findings also indicate that females have access to nitrogen from the histolysis of flight muscles in the thorax. This field study examined how butterflies of the polyandric gift-giving species Pieris napi (Lepidoptera: Pieridae) use body resources in their reproduction and how the male donations affect the females use of stored reserves. The results support earlier studies, indicating that females use resources from the breakdown of thorax muscles to increase their reproductive potential and the results also indicate that males also use thorax material in their reproduction. The study also supports recent findings that the male donation increases the breakdown of body resources and thereby boosts the reproductive output of the female.     

Effects of male mating interval on spermatophore formation,transfer, and subsequent female receptivity and fecundity in the sorghum plant bug,Stenotus rubrovittatus

Males of the sorghum plant bug, Stenotus rubrovittatus (Matsumura) (Heteroptera: Miridae), transfer a spermatophore to females during copulation. After a 1‐day interval between the first and second copulation, males transferred both sperm and a spermatophore to females during the second copulation. However, when male mating interval was <1 h, they transferred sperm but no spermatophores to females during the second copulation. Therefore, the male mating interval probably produces two types of mated females, those with and those without a spermatophore. Mated females of S. rubrovittatus do not remate for at least 3 days after mating, even when courted, and lay more eggs than virgin females at the beginning of the oviposition period. The effects of spermatophores on female sexual receptivity and fecundity were examined using mated females with or without a spermatophore. Only one of the 40 (2.5%) mated females with a spermatophore remated, whereas 10 of the 26 (38.5%) without a spermatophore remated. Furthermore, mated females with a spermatophore laid more eggs than those without a spermatophore. These results suggest that spermatophores participate in reducing female sexual receptivity and enhancing female fecundity in S. rubrovittatus.     

Extreme Costs of Mating for Male Two-Spot Ladybird Beetles

Male costs of mating are now thought to be widespread. The two-spot ladybird beetle (Adalia bipunctata) has been the focus of many studies of mating and sexual selection, yet the costs of mating for males are unknown. The mating system of A. bipunctata involves a spermatophore nuptial gift ingested by females after copulation. In this study, we investigate the cost to males of mating and of transferring spermatophores in terms of lifespan, ejaculate production and depletion of nutritional reserves. We found that males faced a strong trade-off between mating and survival, with males that were randomly assigned to mate a single time experiencing a 53% reduction in post-mating lifespan compared to non-mating males. This is among the most severe survival costs of a single mating yet reported. However, spermatophore transfer did not impact male survival. Instead, the costs associated with spermatophores appeared as a reduced ability to transfer spermatophores in successive matings. Furthermore, males ingested more food following spermatophore transfer than after matings without spermatophores, suggesting that spermatophore transfer depletes male nutritional reserves. This is to our knowledge the first report of an effect of variation in copulatory behaviour on male foraging behaviour. Overall, our study highlights the advantages of assessing mating costs using multiple currencies, and suggests that male A. bipunctata should exhibit mate choice.     

Multiple mating of male and female codling moth (Lepidoptera: Tortricidae) in apple orchards treated with sex pheromone

Studies were conducted with codling moth, Cydia pomonella L., to evaluate the mating status of male and female moths in apple, Malus domestica (Borkhausen), orchards treated with and without sex pheromone dispensers. Laboratory studies first examined the effect of multiple mating of male and female moths on female fecundity and egg fertility. Females that had mated three times had a significantly higher fecundity than singly mated moths. Sequential mating by male moths had no effect on the fecundity of female moths or egg fertility. However, male moth age did impact female fecundity, with significantly fewer eggs laid after mating with virgin 1- versus 3-d-old males. The mean size of the first spermatophore transferred by males was significantly larger than all subsequent spermatophores. Classifying spermatophores based on size was used in field sampling to categorize the mating status of the female's partner. The proportion of mated females with small spermatophores (partner had previously mated) was significantly higher in treated versus untreated orchards. The proportion of female moths caught in traps baited with pear ester that were virgin was low (相似文献   

Male age, mating status and nuptial gift quality in a bushcricket

Female mate choice occurs in many animals, and in some species females prefer older males. Because older males have demonstrated their survival ability, they may be of higher genetic quality, providing genetic benefits to the offspring of their mates. However, in species where females receive direct benefits of matings, younger males may be more likely to provide more fertile or more nutritious ejaculates, so females may discriminate against older males. Males of the bushcricket Ephippiger ephippiger (Orthoptera: Tettigoniidae) produce large spermatophores at mating (>30% of body weight, circa 10% protein content). Female E. ephippiger discriminate against the song of older males. We examined the effects of male age and mating history on male reproductive investment (spermatophore size, sperm number, nitrogen content). Males produced spermatophores with significantly fewer sperm and of lower nitrogen content on their fourth mating, despite free access to food and a 1-week interval between matings, indicating that there is a cost of mating to males. There was no indication that older virgin males produced lower-quality spermatophores. Rather, older males produced bigger spermatophores of higher nutritional value and containing more sperm. Male age and mating history seem likely to be strongly correlated in the field. We conclude that female E. ephippiger probably prefer the songs of younger males, because in the field, this preference correlates with male mating history and therefore resources provided at mating. Thus, female preference for younger males could reflect discrimination against low-quality nuptial gifts.     

Age‐Related Male Reproductive Investment in Courtship Display and Nuptial Gifts in a Moth,Ostrinia scapulalis

Due to a trade‐off between current and future reproduction, costly reproductive investments should be increased towards the end of a lifespan when the probability of reproduction becomes low (terminal investment hypothesis). We investigated age‐related changes in male reproductive investment towards courtship display and the spermatophore in three age classes (young, middle‐aged and old) of a monandrous moth, Ostrinia scapulalis. As predicted, old males had higher mating success than young and middle‐aged males in no‐choice tests. Moreover, two‐choice tests revealed that middle‐aged males had a higher success rate than young males because of their higher courtship frequency rather than any female preference for them. It was found that old males produced a larger spermatophore than young and middle‐aged males, suggesting greater reproductive effort. The protein content of spermatophores also tended to increase with male age. Despite the age‐related variation in spermatophore size and protein content, age did not affect female fecundity or longevity. A decrease in the number of sperm in the older males might counteract the nutritional benefit of larger spermatophores. Alternatively, fitness components other than longevity and fecundity may be influenced by male age.     

Costs of Reproduction in Male Bicyclus anynana and Pieris napi Butterflies: Effects of Mating History and Food Limitation

Life history theory predicts trade‐offs arising from the costs of reproduction: individuals investing more into reproduction should have less energy available for their own somatic demands. Despite a wealth of research on such costs for females, very few studies have looked at the male side. We investigated the costs of reproduction in males of two butterfly species, Bicyclus anynana and Pieris napi. The males of these species differ tremendously in their allocation of nutrients to reproduction: virgin male spermatophores were 18.5 times larger in the latter compared with those in the former. Based on this striking difference, we expected to find a longevity cost of mating in P. napi, but not necessarily in B. anynana. In line with our predictions, we found no evidence for a survival cost of mating in B. anynana, while there was some evidence for such a cost in P. napi. Here, virgin males lived longer than once‐ or twice‐mated ones. However, this overall trend did not hold for all treatment groups, and there was no linear relationship between the number of copulations and longevity. Adult food limitation reduced longevity throughout, but had otherwise very little impact. Spermatophore dry mass decreased in later compared with first spermatophores, while water content increased, indicating that spermatophore production is indeed physiologically costly. Additionally, adult food limitation tended to reduce spermatophore fresh and dry mass, and tended to increase spermatophore water content. Based on our results we tentatively conclude that longevity and reproduction may not always be traded off against each other, as in our study organisms’ longevity seems to depend in first place on adult carbohydrate income, while male reproduction seems to be primarily (although not entirely) fuelled by larval storage reserves.     

Age-related changes in thoracic mass: possible reallocation of resources to reproduction in butterflies

In nectar-feeding butterflies, reproductive potential is usually thought to depend on the size of the reproductive reserves in the abdomen, the adult food quality and, for females, the amount of resources received in the spermatophores at mating. Recent findings show that thorax mass and nitrogen content decrease with age in some butterfly species, and that thorax resources may be used for reproduction in the butterfly Pieris napi , just as in some other insects. In order to determine whether this is a general pattern and ascertain how it relates to the investment of resources in reproduction we studied the dynamics of thorax and abdomen mass changes in 11 Swedish butterfly species. By regressing thorax and abdomen mass on age of field-collected specimens, we show that loss of mass from both the thorax and the abdomen is a common phenomenon among nectar-feeding temperate zone butterflies under natural conditions. We argue that our results indicate that resources from flight muscles can be reallocated to reproduction by these butterflies, thus increasing their reproductive potential. Within species, females use proportionately more resources from the thorax than do males, as expected from the difference in investment of resources in reproduction. Among males we expect species with a higher reproductive investment to have a larger decrease in thorax and abdomen mass, and our data indicate that this is the case. Looking at the change in relative thorax mass, our results suggest that the use of resources from the thorax does not affect flight performance negatively, something that could constrain the use of muscle resources.  © 2005 The Linnean Society of London, Biological Journal of the Linnean Society , 2005, 86 , 363–380.     

Determinants of paternity in a butterfly

Success in sperm competition is of fundamental importance to males, yet little is known about what factors determine paternity. Theory predicts that males producing high sperm numbers have an advantage in sperm competition. Large spermatophore size (the sperm containing package) also correlates with paternity in some species, but the relative importance of spermatophore size and sperm numbers has remained unexplored. Males of the small white butterfly, Pieris rapae (Lepidoptera: Pieridae), produce large nutritious spermatophores on their first mating. On their second mating, spermatophores are only about half the size of the first, but with almost twice the sperm number. We manipulated male mating history to examine the effect of spermatophore size and sperm numbers on male fertilization success. Overall, paternity shows either first male or, more frequently, second male sperm precedence. Previously mated males have significantly higher fertilization success in competition with males mating for the first time, strongly suggesting that high sperm number is advantageous in sperm competition. Male size also affects paternity with relatively larger males having higher fertilization success. This may indicate that spermatophore size influences paternity, because in virgin males spermatophore size correlates with male size. The paternity of an individual male is also inversely correlated with the mass of his spermatophore remains dissected out of the female. This suggests that females may influence paternity by affecting the rate of spermatophore drainage. Although the possibility of female postcopulatory choice remains to be explored, these results clearly show that males maximize their fertilization success by increasing the number of sperm in their second mating.     

Diet, sex, and death in field crickets

Senescence is shaped by age-dependent trade-offs between fitness components. Because males and females invest different resources in reproduction, the trade-offs behind age-dependent reproductive effort should be resolved differently in the sexes. In this study, we assess the effects of diet (high carbohydrate and low protein vs. equal carbohydrate and protein) and mating (once mated vs. virgin) on lifespan and age-dependent mortality in male and female field crickets (Teleogryllus commodus), and on male calling effort. Females always had higher actuarial ageing rates than males, and we found a clear lifespan cost of mating in females. Mated males, however, lived longer than virgin males, possibly because virgins call more than mated males. The fastest age-dependent increases in mortality were among mated males on the high-carbohydrate diet. Males on a high-carbohydrate diet showed a faster increase in calling effort earlier in life, and a more pronounced pattern of senescence once they reached this peak than did males on a diet with equal amounts of protein and carbohydrates. Our results provide evidence that the cost of mating in this cricket species is both diet and sex-dependent, and that the underlying causes of sex differences in life-history traits such as lifespan and senescence can be complex.     

Prolonged copulation and spermatophore size ejaculated in the sulfur butterfly,Colias erate (lepidoptera: pieridae) under selective harassments of mated pairs by conspecific lone males

Uninterrupted copula durations between virgin male and virgin female in the sulfur butterflyColias erate successfully lasted about 45 min in the greenhouse. Without harassment, the copula duration of virgin females with wild young males was similar to that in the greenhouse. The male structured a spermatophore about 40 min after copula initiation. Young males ejaculated bigger spermatophores than old males, while age did not influence copula duration. The mating behaviors of the wild males and the tethered females were observed and the copula duration was recorded. All copulating pairs were harassed by single males in the field, and the copula duration was increased, though there was no difference in spermatophore size. Single males harassed pairs with old males significantly longer duration than pairs with young males. Severe harassment elicited no particular response by the pairs. There was a successful mating takeover by a single male. Females tended to be more likely to re-mate when they had fewer spermatophores in the bursa copulatrix. The females that accepted re-mating retained smaller ejaculates in the bursa copulatrix than those that refused re-mating. Lone males seemed to be able to discriminate old and young males in copula. The harassment of pair with old males might be advantageous for single males to increase mating success.     

When do the Costs of Spermatogenesis Constrain Sperm Expenditure? Remarks on the Pattern of the Spermatogenic Cycle

The costs of spermatogenesis constrain sperm expenditure when sperm production per day is limited. Thus, males are challenged to allocate available resources to sperm production and other life history functions. However, this prevailing assumption is not applicable to species in which spermatogenesis becomes quiescent during the breeding season. Males of these species prepare large quantities of sperm before the breeding season. Among these species, constraints on ejaculates have been intensively investigated in salamanders that deposit spermatophores. Although it is predicted that sperm expenditure should not be limited because of abundantly prepared sperm, spermatophore deposition is often limited during the breeding season when vas deferens are full of sperm. We tested a hypothesis regarding limited spermatophore deposition by measuring sperm quantity and volume of spermatophores sequentially deposited by male eastern newts Notophthalmus viridescens. A male newt rarely deposits more than three spermatophores per mating. If depletion of non‐sperm components of spermatophores limits spermatophore deposition, we predicted that spermatophore volume decreases while sperm quantity remains constant as a male deposits more spermatophores. Alternatively, some regulative mechanisms allow a limited portion of available sperm to be expended per mating, in which sperm quantity is predicted to decrease while the spermatophore volume remains constant. Finally, depletion of non‐sperm components may regulate sperm expenditure, which predicted that both spermatophore volume and sperm quantity decrease. We found that both sperm quantity and the spermatophore volume decreased as a male deposited more spermatophores during a single mating. Sperm expenditure was constrained without the costs involved in active spermatogenesis, and depletion of non‐sperm components likely regulate sperm quantity loaded in spermatophores. In dissociated spermatogenesis, constrained sperm expenditure do not mean that costly spermatogenesis is directly limiting male mating capacity but rather suggest that the evolution of physiological mechanisms regulating sperm expenditure per mating maximizes male reproductive success.     

Potential Reproductive Advantage of Short-over Long-Winged Adult Males of the Cricket <Emphasis Type="Italic">Velarifictorus ornatus</Emphasis>

A trade-off between flight capability and reproduction is well known in adult females of the wing-dimorphic cricket Velarifictorus ornatus, but it is not clear whether such a trade-off exists in adult males of the species. In the present study, we investigated sexual maturation time, mating frequency, and the fertilization success of spermatophores after sequential mating in long-winged (LW) and short-winged (SW) adult males of V. ornatus to evaluate the potential reproductive advantage of the SW over the LW male morph. We found that the SW males of V. ornatus attained sexual maturity earlier and produced heavier spermatophores during the early stage after adult emergence than their LW counterparts. Additionally, within a 24-h mating period, the SW males showed a higher mating frequency, greater spermatophore weight, and shorter intermating time interval compared with their LW counterparts. Although females copulated with the two male morphs produced eggs of similar size, fertilization success by SW males was significantly higher than by the LW males. These results provide support for a trade-off between dispersal capability and reproduction success in wing-dimorphic males of V. ornatus.     

Pattern of sperm storage and migration in the reproductive tract of the swallowtail butterfly Papilio xuthus: cryptic female choice after second mating

Females of the swallowtail butterfly Papilio xuthus L. (Lepidoptera: Papilionidae) mate multiply during their life span and use the spermatophores transferred to increase their longevity as well as fecundity. Sperm from different males may be stored in the sperm storage organs (bursa copulatrix and spermatheca). To clarify the pattern of sperm storage and migration in the reproductive tract, mated females are dissected after various intervals subsequent to the first mating, and the type and activity of sperm in the spermatheca are observed. When virgin females are mated with virgin males, the females store sperm in the spermatheca for more than 10 days. Sperm displacement is found in females that are remated 7 days after the first mating. Immediately after remating, these females flush out the sperm of the first male from the spermatheca before sperm migration of the second male has started. However, females receiving a small spermatophore at the second mating show little sperm displacement, and the sperm derived from the small spermatophore might not be able to enter the spermatheca. Females appear to use spermatophore size to monitor male quality.     

Condition-dependent spermatophore size is correlated with male's age in a bushcricket (Orthoptera: Phaneropteridae)

During mating, male bushcrickets transfer a spermatophore that consists of a sperm-containing ampulla and a product of the accessory glands, the spermatophylax, which females directly ingest. In the present study, we demonstrate male spermatophore allocation in the bushcricket Poecilimon zimmeri . Males of this species show condition-dependent spermatophore investment. This investment depended upon the age at first mating of males, with older individuals transferring larger spermatophores than younger ones of the same body mass. Independently of age, heavier males transfer larger spermatophores, but the size of males (as measured by femur length) was not a good predictor. Heavier males allocate a lower proportion of their mass to spermatophores and reach their maximal investment point earlier than less heavy males. Spermatophylax production levelled off to a species specific maximum earlier than that of sperm investment (measured as ampulla mass), suggesting that males face high levels of sperm competition.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 96 , 354–360.     

Fitness advantage from nuptial gifts in female fireflies

Abstract 1. In many insects, males provide nuptial gifts to females in the form of spermatophores, sperm-containing structures produced by male accessory glands.
2. The work reported here examined the influence of both spermatophore number and spermatophore size on female reproductive output in two related firefly beetles, Photinus ignitus and Ellychnia corrusca (Coleoptera: Lampyridae). Based on differences in adult diet, male spermatophores were predicted to increase female reproductive output to a greater extent in P. ignitus than in E. corrusca .
3. Female fecundity was significantly higher in triply mated females than in singly mated females in both species, with no difference between mating treatments in female lifespan or egg hatching success. No effects of second male spermatophore size on fecundity, lifespan, or egg hatching success were detected in either species.
4. These results suggest a direct fitness advantage from multiple mating for females in both species, although enhanced fecundity may be due either to allocation of spermatophore nutrients to eggs or to other substances transferred within the spermatophore acting as oviposition stimulants.     

Rearing Temperature Influences Adult Response to Changes in Mating Status

Rearing environment can have an impact on adult behavior, but it is less clear how rearing environment influences adult behavior plasticity. Here we explore the effect of rearing temperature on adult mating behavior plasticity in the butterfly Bicyclus anynana, a species that has evolved two seasonal forms in response to seasonal changes in temperature. These seasonal forms differ in both morphology and behavior. Females are the choosy sex in cohorts reared at warm temperatures (WS butterflies), and males are the choosy sex in cohorts reared at cooler temperatures (DS butterflies). Rearing temperature also influences mating benefits and costs. In DS butterflies, mated females live longer than virgin females, and mated males live shorter than virgin males. No such benefits or costs to mating are present in WS butterflies. Given that choosiness and mating costs are rearing temperature dependent in B. anynana, we hypothesized that temperature may also impact male and female incentives to remate in the event that benefits and costs of second matings are similar to those of first matings. We first examined whether lifespan was affected by number of matings. We found that two matings did not significantly increase lifespan for either WS or DS butterflies relative to single matings. However, both sexes of WS but not DS butterflies experienced decreased longevity when mated to a non-virgin relative to a virgin. We next observed pairs of WS and DS butterflies and documented changes in mating behavior in response to changes in the mating status of their partner. WS but not DS butterflies changed their mating behavior in response to the mating status of their partner. These results suggest that rearing temperature influences adult mating behavior plasticity in B. anynana. This developmentally controlled behavioral plasticity may be adaptive, as lifespan depends on the partner’s mating status in one seasonal form, but not in the other.