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.     

Mating stimulates female feeding: testing the implications for the evolution of nuptial gifts

Nutritional benefits from nuptial gifts have been difficult to detect in some species, raising the question: what maintains nuptial feeding when gifts do not benefit females? The sensory trap hypothesis proposes that nuptial feeding may be explained by pre‐existing sensory responses that predispose females to ingest gifts. Recent studies have shown that male seminal proteins can induce a nonspecific increase in female feeding after mating, which may represent a sensory trap for nuptial feeding if it results in increased intake of post‐mating gifts. I tested these ideas using female beetles that ingest a spermatophore after mating. I show that males stimulate strongly increased female feeding post‐mating. However, there was little evidence for dose dependence in the feeding response that could allow males to stimulate feeding beyond the female optimum. Moreover, the post‐mating feeding response could not explain nuptial feeding: despite feeding more in general, newly mated females were less likely than nonmated females to ingest spermatophore gifts.     

The contribution of multiple mating and spermatophore consumption to the lifetime reproductive success of female field crickets (Gryllus bimaculatus)

ABSTRACT.

• 1 The adaptive significance of multiple mating by female Gryllus bimaculatus (De Geer) was investigated.
• 2 Multiple mating prevented the depletion of sperm stores and, therefore, maintained high hatching success. This may not, however, explain the high frequency of remating in this species.
• 3 Male-derived egg stimulants known to be passed with sperm at mating increased the number of eggs produced only when females mated throughout their lifespans.
• 4 Spermatophore consumption appeared to provide nutrients which, while they did not increase the quantity of eggs, increased egg quality as indicated by weight. Females who consumed spermatophores had a greater hatching success.
• 5 While females may derive non-genetic benefits from mating, these are apparently long-term benefits; females must mate throughout their lives in order to accrue them.
• 6 Since the benefits of mating may not be derived from individual males, the spermatophores and their contents in this species are best considered as mating effort.

     

Diet affects female mating behaviour in a seed‐feeding beetle

In species where males provide nuptial gifts, females can improve their nutritional status and thus increase their fecundity by mating when in need of resources. However, mating can be costly, so females should only mate to acquire resources when the need for resources is large, such as when females are nutritionally‐deprived. Two populations of the seed‐feeding beetle Callosobruchus maculatus, a species that produces relatively large nuptial gifts, are used to test whether female nutritional status affects mating behaviour. Female access to water, sugar and yeast are manipulated and the fitness consequences of these manipulations are examined together with the effects of diet on the propensity of nonvirgin females to mate. Access to water has a small but significant effect on mass loss over time, lifespan and fecundity of females, relative to unfed controls. Access to sugar (dissolved in water) improves female fecundity and lifespan above that of hydrated females but access to yeast has no positive effects on female survival or reproduction. Diet has a large effect on both receptivity of nonvirgin females to a male and how quickly they accept that male. Unfed females are both more likely to mate, and accept a mate more quickly, than females provided access to water, which are more likely to mate and accept a mate more quickly than females provided with sugar. This rank order of behaviours matches the order predicted if females increase their mating rate when nutritionally deprived (i.e. it matches the effect of diet on female fitness). The results obtained also suggest that mate choice may be condition‐dependent: females from one population (Burkina Faso) show a preference for large males when well‐fed but not when unfed, although this result is not found in a second population (South India). It is concluded that nutritionally‐deprived females are more receptive to mates than are well‐fed females, consistent with the hypothesis that females ‘forage’ for nuptial gifts, or at least more willingly accept sperm in exchange for nuptial gifts, when they are nutritionally deprived.     

Hemolymph loss during nuptial feeding constrains male mating success in sagebrush crickets

Although costs of mating have been widely documented in females,intrinsic costs of copulation have been poorly documented inmales, and there is little evidence that such costs constrainmale mating success under natural conditions. Male sagebrushcrickets, Cyphoderris strepitans, offer females an unusual somaticfood gift at copulation that may constitute a significant costof copulation: females chew on the ends of the males' fleshyhind wings and ingest hemolymph seeping from the wounds theyinflict. Previous studies have shown that once a male has mated,his probability of obtaining an additional copulation is reducedrelative to that of a virgin male seeking to secure his firstmating. If the future mating prospects of nonvirgin males arediminished because of the costs of copulation, this could stemeither from the resources required to manufacture a new spermatophoreor through the energy needed to replenish hemolymph lost throughfemale wing-feeding. To distinguish between these two alternatives,we experimentally depleted virgin males of varying amounts hemolymphin a way that mimicked hemolymph loss of nonvirgin males, withoutthe attendant costs of spermatophore production. After theyhad been treated, males were released in the field and recapturedover the course of the breeding season to monitor their matingsuccess. Control males mated significantly sooner than did malesdepleted of hemolymph. We conclude, therefore, that the depletionof hemolymph that occurs through female wing feeding is sufficientby itself to diminish a nonvirgin male's ability to secure anothermating.     

Multiple mating and its effect on the reproductive success of female Epiphyas postvittana (Lepidoptera: Tortricidae)

Abstract.

• 1 Multiple mating and its effect on reproductive performance of female Epiphyas postvittana (Walker) moths were studied under controlled conditions.
• 2 The age at which the moths mated for the first time ranged from the first to the tenth day after emergence, but 71% of first matings were during the first 3 days.
• 3 The majority (63%) of females had one or two spermatophores in the bursa copulatrix. Some (24%) were found with three to five spermatophores, whereas no successful mating occurred among 13% of individuals. The number of matings was partly dependent on the number of mates available to the female. Between the range of sex ratios of one male to one female and four males to one female maximal mating success occurred at the ratio of three males to one female.
• 4 Virgin females were capable of egg-laying, but mating stimulated and accelerated oviposition. Mated individuals laid twice as many eggs as unmated ones.
• 5 The level of copulatory activity did not influence the longevity of females irrespective of the number of males available to them.
• 6 Sex ratios with greater than one male to a female improved the reproductive success by marginally increasing fecundity and fertility.
• 7 It is concluded that multiple mating would enhance population growth, and is of particular benefit to populations with a preponderance of females, as is known to occur naturally in this species.

     

Terminal investment in the gustatory appeal of nuptial food gifts in crickets

Investment in current versus future reproduction represents a prominent trade‐off in life‐history theory and is likely dependent on an individual's life expectancy. The terminal investment hypothesis posits that a reduction in residual reproductive value (i.e. potential for future offspring) will result in increased investment in current reproduction. We tested the hypothesis that male decorated crickets (Gryllodes sigillatus), when cued to their impending mortality, should increase their reproductive effort by altering the composition of their nuptial food gifts (i.e. spermatophylaxes) to increase their gustatory appeal to females. Using a repeated‐measures design, we analysed the amino acid composition of spermatophylaxes derived from males both before and after injection of either a saline control or a solution of heat‐killed bacteria. The latter, although nonpathogenic, represents an immune challenge that may signal an impending survival threat. One principal component explaining amino acid variation in spermatophylaxes, characterized by a high loading to histidine, was significantly lower in immune‐challenged versus control males. The relevance of this difference for the gustatory appeal of gifts to females was assessed by mapping spermatophylax composition onto a fitness surface derived in an earlier study identifying the amino acid composition of spermatophylaxes preferred by females. We found that immune‐challenged males maintained the level of attractiveness of their gifts post‐treatment, whereas control males produced significantly less attractive gifts post‐injection. These results are consistent with the hypothesis that cues of a survival‐threatening infection stimulate terminal investment in male decorated crickets with respect to the gustatory appeal of their nuptial food gifts.     

Promiscuous mating produces offspring with higher lifetime fitness

In many species, each female pairs with a single male for the purpose of rearing offspring, but may also engage in extra-pair copulations. Despite the prevalence of such promiscuity, whether and how multiple mating benefits females remains an open question. Multiple mating is typically thought to be favoured primarily through indirect benefits (i.e. heritable effects on the fitness of offspring). This prediction has been repeatedly tested in a variety of species, but the evidence has been equivocal, perhaps because such studies have focused on pre-reproductive survival rather than lifetime fitness of offspring. Here, we show that in a songbird, the dark-eyed junco (Junco hyemalis), both male and female offspring produced by extra-pair fertilizations have higher lifetime reproductive success than do offspring sired within the social pair. Furthermore, adult male offspring sired via extra-pair matings are more likely to sire extra-pair offspring (EPO) themselves, suggesting that fitness benefits to males accrue primarily through enhanced mating success. By contrast, female EPO benefited primarily through enhanced fecundity. Our results provide strong support for the hypothesis that the evolution of extra-pair mating by females is favoured by indirect benefits and shows that such benefits accrue much later in the offspring's life than previously documented.     

Male mating costs in a butterfly that produces small ejaculates

In many insects, ejaculate size is positively related to male fitness, although the production of large ejaculates entails physiological costs that can result in decreased male longevity. Ejaculate production costs have been studied in butterfly species because males generally produce large ejaculates that are rich in resources. However, lepidopterans show interspecific variation with respect to relative investment in ejaculates (i.e. percentage of male body weight invested in ejaculates) that could influence the magnitude of costs. The physiological costs of ejaculate production are expected to differ between males with different amounts of resources stored. The effect of male size (an estimate of the amount of resources stored) on ejaculate production and on survivorship costs of multiple mating is studied in males of Leptophobia aripa Boisduval (Pieridae), the butterfly with the smallest relative investment in spermatophores recorded to date (0.31%). ‘Small males’ produce smaller spermatophores, although male size has no effect on ejaculate size (spermatophore + accessory substances), indicating that ‘small males’ make a relatively larger investment in the production of accessory substances. The results indicate that L. aripa males are able to modify the relative amount of resources invested in ejaculate production. Multiple mating has a negative effect on male longevity and this effect depends on male size: in comparison with virgin males, the longevity of ‘small males’ decreases after just one copula, whereas the longevity of ‘large males’ decreases after two copulations. The possible reasons why ‘small males’ invest relatively more resources in ejaculate production, despite the fact that they pay larger costs, are discussed.     

Linking larval nutrition to adult reproductive traits in the European corn borer Ostrinia nubilalis

Throughout an organism's lifetime, resources are strategically allocated to many different functions, including reproduction. Reproduction can be costly for both sexes; females produce nutrient‐rich eggs, whereas males of many species produce large and complex ejaculates. In capital breeding insects, nutrients are mainly acquired during the larval period, yet allocation decisions impact the reproductive fitness of adults. The present study examines the effect of larval dietary nitrogen on both male and female reproductive traits in the European corn borer moth Ostrinia nubilalis Hübner, whose adults do not feed and whose males transfer a large, nitrogen‐rich spermatophore. One day post‐eclosion, O. nubilalis adults reared on one of three different diets (3.0%, 1.6%, or 1.1% nitrogen) are mated and two experiments are undertaken: one to measure nitrogen and carbon content of male ejaculates, and the other to determine female fecundity and fertility. Although male larval diet does not alter the percentage nitrogen content of adult somatic tissue, males reared on the higher nitrogen diet (3.0%) produce spermatophores with increased nitrogen relative to somatic nitrogen. Furthermore, females raised on the 3.0% nitrogen diet receive spermatophores with lower carbon : nitrogen ratios and thus more nitrogen. Overall, females lay more eggs as their larval dietary nitrogen increases, although they lay fewer eggs when their mates are raised on the higher (3.0%) nitrogen diet. This suggests that O. nubilalis females may use male‐derived nitrogen not to supplement egg production, but rather for somatic maintenance. Overall, the present study furthers our understanding of how larval diet can affect adult fitness in Lepidoptera.     

Early growth,dominance acquisition and lifetime reproductive success in male and female cooperative meerkats

In polygynous species, variance in reproductive success is higher in males than females. There is consequently stronger selection for competitive traits in males and early growth can have a greater influence on later fitness in males than in females. As yet, little is known about sex differences in the effect of early growth on subsequent breeding success in species where variance in reproductive success is higher in females than males, and competitive traits are under stronger selection in females. Greater variance in reproductive success has been documented in several singular cooperative breeders. Here, we investigated consequences of early growth for later reproductive success in wild meerkats. We found that, despite the absence of dimorphism, females who exhibited faster growth until nutritional independence were more likely to become dominant, whereas early growth did not affect dominance acquisition in males. Among those individuals who attained dominance, there was no further influence of early growth on dominance tenure or lifetime reproductive success in males or females. These findings suggest that early growth effects on competitive abilities and fitness may reflect the intensity of intrasexual competition even in sexually monomorphic species.     

Sex Differences in “Time Out” from Reproductive Activity and Sexual Selection in Male Bushcrickets (Orthoptera: Zaprochilinae: <Emphasis Type="Italic">Kawanaphila mirla</Emphasis>)

Animals of many species prefer some partners over others. Discriminating among potential mates causes strong sexual selection that shapes characters and behaviors. In bushcrickets the sexes shows different latencies to remate due to differences in investment in production of the nuptial gift by males and the induced refractory period in females. We conducted experiments with the Australian bushcricket Kawanaphila mirla to test the variation in male mating success by female choice. Male remating intervals under unlimited access to food and mates were around two days, whereas most females did not remate within 12 days. Males had therefore a much shorter “time-out” from mating than females. The adult sex ratio from field samples was near to 1:1. Consequently, the OSR was male-biased with more males than females ready to mate. This male-biased OSR led to mating competition in males and choosiness in females. In a field enclosure with unlimited supply of receptive females the number of matings varied widely between males, with twenty percent of males neglected by the females. The number of matings within this enclosure was neither related to male size nor to song characters, recorded previously in the lab. However, the number of matings by individual males was positively correlated to the size of their spermatophore producing accessory gland. Females appear to prefer males with a large nutritive donation, thereby receiving a direct fitness benefit.     

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.     

Resource availability,mating opportunity and sexual selection intensity influence the expression of male alternative reproductive tactics

The expression of alternative reproductive tactics can be plastic and occur simultaneously depending on cues that vary spatially or temporally. For example, variation in resources and sexual selection intensity is expected to influence the pay‐off of each tactic and shape the decision of which tactic to employ. Males of the nuptial gift‐giving spider Pisaura mirabilis can adopt three tactics: offering a genuine prey gift, a ‘worthless’ non‐nutritious gift or no gift. We hypothesized that resources and/or male body condition, and mating opportunity and sexual selection intensity, vary over the course of the mating season to shape the co‐existence of alternative traits. We measured these variables in the field over two seasons, to investigate the predictions that as the mating season progresses, (i) males become more likely to employ a gift‐giving tactic, and (ii) the likelihood of switching from worthless to genuine gifts increases. Prey availability increased over the season and co‐varied with the propensity of males to employ the gift‐giving tactic, but we found no support for condition‐dependent gift giving. Males responded to an increase in female availability by increasing their mating effort (gift production). Furthermore, the frequency of genuine gift use increased with sexual selection intensity, consistent with the assumption that sperm competition intensity increases with time. Our results suggest that the frequency of alternative tactics is shaped by seasonal changes in ecological factors and sexual selection. This leads to relaxed selection for the gift‐giving tactic early in the season when females are less choosy and resources more scarce, and increased selection for genuine gifts later in the season driven by mating opportunity and risk of sperm competition.     

Impact of male mating history on the postmating resumption of sexual receptivity and lifetime reproductive success in Choristoneura rosaceana females

Abstract.  The first objective of the present study is to test the hypothesis that the decrease in the number of eupyrene spermatozoa in the spermatheca is directly associated with the resumption of sexual receptivity in female moths, an aspect that has not been examined in previous studies. The obliquebanded leafroller, Choristoneura rosaceana , is used and females mated with previously mated males have a shorter refractory period than those mated with virgins. This difference is associated with a faster rate of movement of sperm from the spermatheca. Overall, the length of the female refractory period coincides with the mean time required for the number of eupyrene sperm in the spermatheca to drop to approximately 3000, regardless of male mating history. Although such a decline in sperm numbers may be a factor responsible for the resumption of sexual receptivity, this is clearly not the only one because more than 40% of females remate even though sperm numbers in the spermatheca are well above this threshold. Virgin males do not vary the mass or the content of their ejaculate as a function of the female's reproductive status and this may increase the risk of sperm competition if the female is previously mated. The second objective of this study is to examine the effect of previous male mating history on female reproductive potential. Females mated with previously mated males have a significantly lower fecundity than those mated with virgin males. However, in all treatments, remating increases both female longevity and lifetime fecundity. There is also a significant effect of female mass on the length of the refractory period and on lifetime fecundity, with large females resuming sexual receptivity sooner and laying more eggs than small ones, regardless of male mating history.     

Costs of mating competition limit male lifetime breeding success in polygynous mammals

Although differences in breeding lifespan are an important source of variation in male fitness, the factors affecting the breeding tenure of males have seldom been explored. Here, we use cross-species comparisons to investigate the correlates of breeding lifespan in male mammals. Our results show that male breeding lifespan depends on the extent of polygyny, which reflects the relative intensity of competition for access to females. Males have relatively short breeding tenure in species where individuals have the potential to monopolize mating with multiple females, and longer ones where individuals defend one female at a time. Male breeding tenure is also shorter in species in which females breed frequently than in those where females breed less frequently, suggesting that the costs of guarding females may contribute to limiting tenure length. As a consequence of these relationships, estimates of skew in male breeding success within seasons overestimate skew calculated across the lifetime and, in several polygynous species, variance in lifetime breeding success is not substantially higher in males than in females.