Amorous scorpionflies: causes and consequences of the long pairing prelude of Panorpa cognata

The scorpionfly Panorpa cognata has a prolonged premating period. After the male attracts a female, there is usually a long delay, from a few minutes to almost 7 h, before the male initiates copulation by secreting a salivary mass. In our experiments, we manipulated the amount of food, and hence the condition, of males and then measured their premating duration. The premating duration was strongly influenced by male nutrient availability and, consequently, male mating resource limitation. Males with ample resource availability, that is with large salivary glands, initiated copulations faster than males with limited resources. In addition, premating duration decreased with increasing male age. The secretion of a salivary mass was more likely to result in a successful copulation if males delayed copulation. When males initiated copulation soon after attracting a mate, nuptial gift offering often failed because of interruption by other scorpionflies or female rejection. Since the value of each invested salivary mass is high for males with limited resources, we suggest that these males invest prudently: to enhance the probability of a return on their investment, they delay secreting the salivary mass until they are confident that females are motivated to mate. Furthermore, with this strategy, males enhance the likelihood of copulating in a sheltered location, where they are unlikely to be interrupted by intruders. Alternative hypotheses are that males in poor condition have more difficulty in persuading females or that males with small salivary glands need longer to produce the salivary mass. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.     

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 consumption influences female remating in a scorpionfly: male or female control of mating rate?

In the scorpionfly Panorpa cognata, males provide females with saliva secretions as nuptial food gifts. Consequently, females derive material benefits and possibly also genetic benefits from multiple matings. Females therefore generally should have a high motivation to remate. Males, on the other hand, do not share this interest, which will generate a sexual conflict over remating interval, possibly leading to male adaptations that prevent females from remating with other males. In this study, I found that mated females were less prone to copulate than virgin females, despite female benefits of multiple matings. Further, I found that the remating interval was significantly longer if the first copulation was long compared to shorter matings. This effect does not entirely depend on copulation duration per se, but on the amount of saliva, that a female is consuming during copulation. These results suggest a mating-induced refractory period and can be interpreted as male manipulation of female remating behaviour mediated through substances in the nuptial gift. Alternatively, receiving large nuptial gifts may decrease the prospective direct fitness benefits from further copulations, and thus change optimal female remating rate. Furthermore, gift size has been shown to correlate with male nutritional condition, which may be an indicator of male genetic quality. Females may therefore benefit indirectly by not remating following copulations involving large saliva gifts. In this scenario, female remating interval would be an effect of cryptic female choice.     

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.     

Structural evidence why males of Panorpa liui offer prey rather than salivary mass as their nuptial gift

Ma, N. and Hua, B. 2010. Structural evidence why males of Panorpa liui offer prey rather than salivary mass as their nuptial gift. —Acta Zoologica (Stockholm) 92 : 398–403. The scorpionflies are considered as ideal model animals for the study of mating systems in insects. The males generally offer both prey and salivary mass as nuptial gifts to the females during copulation. Our field observations show that Panorpa liui is peculiar because the males offer only prey rather than salivary secretions as nuptial gift. Through anatomical and histological examinations, the salivary glands of P. liui were found to be devoid of sexual dimorphism in Panorpa for the first time. Both the male and female P. liui bear simple salivary glands, which are only composed of a common duct and two short sac‐like glands. This is the first attempt to explore the relationship between the salivary glands and the mating tactics from the structural aspect in Panorpa, speculating that the simple structure of the male salivary glands in P. liui might be responsible for its failing to produce salivary mass as a nuptial gift during copulation. Compared with Boreidae, Meropidae, Bittacidae and Panorpidae, we presume that the absence of sexual dimorphism of the salivary glands might represent a plesiomorphy in P. liui. The origin and evolutionary process of the nuptial gift behaviour are tentatively speculated in Panorpa.     

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.     

Strategic male mating effort and cryptic male choice in a scorpionfly

In animal species with high male mating effort, males often find themselves in a dilemma: by increasing their mating effort, the gain from each copulation increases but simultaneously reduces available resources and, thus, the opportunity for future copulations. Therefore, we expect males to spend less reproductive resources on matings that provide low reproductive potential, thereby saving resources for future copulations, possibly with high-quality females, a sort of cryptic male choice. However, the strength of the trade-off between investment in a current mating and resources available for future matings must not be the same for all males. Males with relatively high mating costs should allocate their limited resources more cautiously than males with more plentiful resources. Here, we examine this prediction in the scorpionfly Panorpa cognata. Prior to copulation, males produce a large salivary mass on which females feed during copulation. We show that the production of larger salivary masses leads to longer copulations. Moreover, the size of the salivary gland and salivary mass increases with increasing male condition. However, males in poor condition make a relatively higher mating investment than males in good condition. We therefore expect male condition to influence cryptic male choice. In accordance with our hypothesis, only males in poor condition choose cryptically, producing larger salivary masses in copulations with females of high fecundity.     

Limits to Nuptial Gift Production by Male Fireflies, Photinus ignitus

Males of diverse insect species provide females with nuptial gifts, and limits on males' ability to produce these gifts may influence courtship behavior and mating systems. In the firefly Photinus ignitus, males transfer a complex spermatophore to females during mating. We provided firefly males unlimited access to responsive females to examine whether spermatophore production limits male mating success. Male spermatophore mass decreased significantly across sequential matings, and the percentage of successful matings declined during the second half of each male's life span. Male body mass explained a significant proportion of variation in size of the first spermatophore produced by P. ignitus males, but this relationship disappeared with second spermatophores. This study indicates that males' ability to produce spermatophores declines over their lifetime and that limits on nuptial giftproduction can constrain male mating success in Photinus fireflies.     

Virgin male mating advantage in a primitive acoustic insect (Orthoptera: Haglidae)

Male reproductive behavior in the relict flightless haglid, Cyphoderris strepitans,entails the generation of sound signals and the provision of nuptial gifts to mates. These food gifts take two forms: (1) a gelatinous mass (spermatophylax) augmenting the spermatophore and (2) fleshy metathoracic wings adapted to be eaten. The female consumes a portion of the male's underwings during courtship and copulation and the spermatophylax afterward. The incidence of wing-feeding wounds can be used to monitor the mating success of field-caught males. If, when a male mates, he compromises his ability to provide subsequent nutritive gifts, females would benefit by mating with virgin rather than nonvirgin males. To test this, mating success of virgin and nonvirgin males was compared in a field population. Virgins were found to obtain more matings than explained by their numbers relative to nonvirgins in the population. We conclude that, having mated, a male is at a disadvantage, relative to his virgin competitors, in securing further matings.     

A life-history perspective on strategic mating effort in male scorpionflies

In species with high male mating effort, there is a trade-offbetween mating effort spent in a current mating and resourcesleft for future matings. Consequently, to maximize their reproductivesuccess, males have to invest strategically, saving resourcesin matings with low reproductive gain for future, more valuablematings. However, as males age, the expected future reproductivesuccess constantly declines. Thus, the importance of resource rationing may drastically change during a lifetime. Males ofthe scorpionfly Panorpa cognata offer females a costly nuptialgift before copulation, which functions as male mating effort.Resources for the production of these salivary masses are severelylimited for males in poor condition. We found that males investedmore in copulations with high-quality females than in copulationswith low-quality females. However, males ceased to discriminateas they became older. Old males, with a relative small numberof expected future matings, did not invest differentially incopulations with high- versus low-quality females. In copulationswith low-quality females, males invested more in late thanin initial matings, whereas in matings with high-quality females,time of mating had no influence on mating effort. These resultsimply that males adaptively change their resource allocationstrategy during the course of the season. Initial matings seemto be characterized by male prudence; in later matings, malesseem to adopt a more opportunistic mating strategy.     

Determinants of sperm transfer in the scorpionfly Panorpa cognate: male variation, female condition and copulation duration

Recent studies suggest that sperm production and transfer may have significant costs to males. Male sperm investment into a current copulation may therefore influence resources available for future matings, which selects for male strategic mating investment. In addition, females may also benefit from actively or passively altering the number of sperm transferred by males. In the scorpionfly Panorpa cognata, the number of sperm transferred during copulation depended on copulation duration and males in good condition (residual weight) copulated longer and also transferred more sperm. Moreover, sperm transferred and stored per unit time was higher in copulations with females in good condition than in copulations with females in poor condition. Males varied greatly and consistently in their sperm transfer rate, indicative of costs associated with this trait. The duration of the pairing prelude also varied between males and correlated negatively with the male's sperm transfer rate, but no other male character correlated significantly with male sperm transfer rate. The results are consistent with strategic mating effort but sperm transfer could also be facilitated by the physical size of females and/or females in good condition may be more cooperative during sperm transfer.     

Insemination efficiency of two alternative male mating tactics in the guppy Poecilia reticulata

In this study we compared the insemination efficiency of two alternative mating tactics (courtship and sneak mating) in the guppy Poecilia reticulata by quantifying the number of sperm delivered during a copulation. During a single copulation, guppies delivered between zero and 92% of the sperm available, as determined by mechanically stripping the males'' sperm reserve at rest. The absolute number of sperm delivered after courtship was three times larger than that delivered through sneak mating; nonetheless, the variance was large with both tactics and the two distributions largely overlapped. The number of sperm available at rest increased with male size. With both tactics, the number of sperm delivered was positively correlated with the sperm available. Contrary to courtship copulations, in sneak copulations there was no correlation between the number of sperm delivered and male size. However, once the data were standardized for sperm reserve, small males delivered a larger proportion of their available sperm during sneak copulation. The rate of sexual acts (sigmoid and thrust rate) before copulation was not correlated with the number of sperm available. After the occurrence of a copulation in both the courtship and sneak copulation groups, the sexual activity of the male decreased in proportion to the amount of sperm he previously inseminated.     

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.     

Courtship Behavior in the Hawaiian Cricket Laupala cerasina: Males Provide Spermless Spermatophores as Nuptial Gifts

The role of sexual selection in the crickets (family Gryllidae) is well known but new forms of courtship behavior continue to be discovered. Here we describe the elaborate mating behavior of the Hawaiian endemic Laupala cerasina (subfamily Trigonidiinae) on the basis of both laboratory and field observations. We found that courtship and mating involve multiple copulations during which repeated spermatophores are transferred. Initial copulations involved the transfer of relatively small ‘microspermatophores’. The final copulation results in the transfer of a considerably larger ‘macrospermatophore’. We tested and rejected the hypothesis that the number of spermatophore transfers results in greater offspring sired by a given male. Matings involving only microspermatophores resulted in no offspring, whereas most matings involving micros and a macrospermatophore, or a macrospermatophore only, produced offspring. A direct examination of the contents of the microspermatophore revealed an absence of sperm, whereas examination of the macrospermatophore revealed the presence of sperm. Given that females consume the spermless microspermatophores, we conclude that the microspermatophores are a form of nuptial feeding of females by males. We discuss possible hypotheses to explain this unusual courtship system.     

Male Performance and Body Size Affect Female Re-Mating Occurrence in the Orb-Web Spider Leucauge mariana (Araneae, Tetragnathidae)

Females can affect male probabilities of paternity success through behavioural, morphological and/or physiological processes occurring during or after copulation. These processes under female-control include the acceptance or rejection of mating attempts by subsequent males. Leucauge mariana is an orb weaving spider that shows male mate guarding of penultimate females, male–male competition on female webs and copulatory plugs, suggesting a polyandric mating system. The aim of the present study was to ascertain whether male behaviour during courtship and copulation in L. mariana relate with female re-mating decisions. Forty-three virgin females were exposed to up to three males until they mated. In 24 cases, the copulatory plug was absent after mating and females were exposed the next day to up to three other males. Eighteen females accepted a second mating. Relatively larger females were more receptive to second matings and were more likely to copulate if the second male was smaller. Longer duration of female tapping and abdominal bobbing during courtship, and first copulations with less short insertions and more flubs, were associated with increased female acceptance to second matings. The results indicate cryptic female choice on male courtship and copulatory performance and suggest female-control over the determination of male mating success in this spider species.     

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.     

Resource-dependent nuptial feeding in Panorpa vulgaris: an honest signal for male quality

In mating systems that are characterized by resource-dependentmale behavior like nuptial feeding, food limitation obviouslyplays a major role in male performance. In Panorpa vulgaris(Mecoptera: Panorpidae), the ability to produce nuptial giftshas major fitness consequences as the number of gifts determinescopulation duration, which then determines the number of eggsfertilized by a given male. In the present study, we are ableto show that males of P. vulgaris were limited in their productionof salivary secretions. The number of saliva secretions maleswere able to produce declined in successive matings. Moreover,males of nutritionally high status produced more gifts thanthose of nutritionally low status. The proximate factor determiningmale saliva secretion was the development of the salivary gland,which in turn depended on the amount of food a male could access.The degree of male mating effort corresponded to the size ofthe salivary gland, yet while absolute investment increasedwith gland size, the relative investment decreased. Mating costsfor males thus depend on nutritional status.     

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.     

Courtship and copulation in Tarsius bancanus

The reproductive behavior of 6 paired, captive Bornean tarsiers was studied over an 8-month period. Seven copulations were observed. Females signalled males by visual displays and olfactory cues from vulval rubbing. Males signalled females with courtship calls heard before matings. After a courtship lasting from 1 to 2 h, copulation occurred with the male thrusting 61-190 times for 60-90 s, ending in ejaculation. The female regulated timing of mating by rejection or avoidance of the male. Multiple matings were not observed, and mating occurred once or twice a night during each night of estrus. This copulatory pattern of infrequent matings of short duration and active female solicitation and regulation of copulating timing suggests a harem or monogamous system.     

Non-random Mating in the Dance Fly Empis borealis: The Importance of Male Choice

In the dance-fly Empis borealis (Diptera, Empididae), females form swarms to which males, carrying a nuptial gift, come for mating. We examined whether males or females were choosy and/or competed for mates. First, measurements of the size relationships between copulating males and females, nuptial gifts and the swarming females from different swarms were assessed. Second, male visiting time in differently sized female swarms was recorded. Larger (wing-length) females participated disproportionately in copulations in each swarm, but not for the population at large. Female mating status (virgin/non-virgin) or proximity to oviposition (egg size) did not influence the likelihood of copulation. No assortative mating pattern was found: male size and size of nuptial gift did not correlate with size of the mating female. The time spent by males in swarms increased with the number of females present and it took longer when males left a swarm without copulation than when doing so. Male visiting time per female was negatively correlated with number of females in swarms. Males more often left smaller than larger swarms without mating. We conclude that E. borealis males discriminate among females but find no evidence for male competition or for female choice. It is still a question to what degree females compete for males.