A secondary sex trait under construction: age- and nutrition-related salivary gland development in a scorpionfly (Insecta: Mecoptera)

Males of Panorpa vulgaris Imhoff and Labram, 1836 (Insecta: Mecoptera) can apply three alternative mating tactics to gain access to female mating partners: (1) without nuptial feeding, (2) providing females with a dead arthropod or (3) producing salivary masses. Providing females with salivary masses during copulation leads to the highest reproductive success, as it results in longer mating durations relative to the other tactics. While the number of sperm transferred correlates with the duration of copulation, the sperm of different males are used according to the fair raffle model. Therefore, salivary mass production is an important fitness determining factor for males. In order to provide females with salivary masses, males must first produce and store saliva secretion inside their salivary glands. The present study was concerned with the development of male salivary glands (= production of saliva) in the course of time after adult emergence. We can show that saliva production did not start before adult emergence, that the state of development of salivary glands was affected by larval nutrition as well as by adult nutrition and, moreover, by age. Older individuals had developed glands of greater mass than had younger animals. After receiving a one‐time feeding immediately after eclosion salivary gland mass increased, while body mass decreased with age. Therefore, male P. vulgaris were able to enlarge the amount of their mating resources (= saliva) independently from external nutritional supply (after the initial feeding) and at the expense of losing weight. Possible reasons and functional explanations are discussed.     

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.     

Building a Beetle: How Larval Environment Leads to Adult Performance in a Horned Beetle

The link between the expression of the signals used by male animals in contests with the traits which determine success in those contests is poorly understood. This is particularly true in holometabolous insects such as horned beetles where signal expression is determined during metamorphosis and is fixed during adulthood, whereas performance is influenced by post-eclosion feeding. We used path analysis to investigate the relationships between larval and adult nutrition, horn and body size and fitness-related traits such as strength and testes mass in the horned beetle Euoniticellus intermedius. In males weight gain post-eclosion had a central role in determining both testes mass and strength. Weight gain was unaffected by adult nutrition but was strongly correlated with by horn length, itself determined by larval resource availability, indicating strong indirect effects of larval nutrition on the adult beetle’s ability to assimilate food and grow tissues. Female strength was predicted by a simple path diagram where strength was determined by eclosion weight, itself determined by larval nutrition: weight gain post-eclosion was not a predictor of strength in this sex. Based on earlier findings we discuss the insulin-like signalling pathway as a possible mechanism by which larval nutrition could affect adult weight gain and thence traits such as strength.     

Condition‐dependent ejaculate production affects male mating behavior in the common bedbug Cimex lectularius

Food availability in the environment is often low and variable, constraining organisms in their resource allocation to different life‐history traits. For example, variation in food availability is likely to induce condition‐dependent investment in reproduction. Further, diet has been shown to affect ejaculate size, composition and quality. How these effects translate into male reproductive success or change male mating behavior is still largely unknown. Here, we concentrated on the effect of meal size on ejaculate production, male reproductive success and mating behavior in the common bedbug Cimex lectularius. We analyzed the production of sperm and seminal fluid within three different feeding regimes in six different populations. Males receiving large meals produced significantly more sperm and seminal fluid than males receiving small meals or no meals at all. While such condition‐dependent ejaculate production did not affect the number of offspring produced after a single mating, food‐restricted males could perform significantly fewer matings than fully fed males. Therefore, in a multiple mating context food‐restricted males paid a fitness cost and might have to adjust their mating strategy according to the ejaculate available to them. Our results indicate that meal size has no direct effect on ejaculate quality, but food availability forces a condition‐dependent mating rate on males. Environmental variation translating into variation in male reproductive traits reveals that natural selection can interact with sexual selection and shape reproductive traits. As males can modulate their ejaculate size depending on the mating situation, future studies are needed to elucidate whether environmental variation affecting the amount of ejaculate available might induce different mating strategies.     

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.     

Selection of male traits during and after copulation in the seedbug Lygaeus simulans (Heteroptera, Lygaeidae)

In order to evaluate selection of male morphological traits during copulation, a laboratory experiment was performed with the promiscuous seedbug Lygaeus simulans. Three male traits suspected as putative targets of selection were measured: weight, fluctuating asymmetry of a measure on the forewings, and length of a conspicuous genital structure, the processus gonopori. As fitness measures we considered total fecundity (number of fertilized eggs), insemination and fertilization success (established if a female laid fertilized eggs after copulation), and the interval between copulation and oviposition. Eighty-four males were allowed a single copulation with one virgin female each. Out of 67 copulations, 27 (40.2%) resulted in fertilized eggs and the oviposition latency ranged from 6 to 26 days. Regressions of male traits on the fitness measures showed significant phenotypical selection of two male traits: (1) males of average weight are more likely to achieve fertilization and (2) the oviposition latency was shorter for males with lower asymmetry. The copulation-oviposition interval may be especially important for male fertilization success because Lygaeus males perform copulatory mate guarding and the last male copulating with a female fertilizes most of the eggs. No selection of the genitalic trait was detected.     

Genetic variation but weak genetic covariation between pre‐ and post‐copulatory episodes of sexual selection in Drosophila melanogaster

When females mate polyandrously, male reproductive success depends both on the male's ability to attain matings and on his ability to outcompete rival males in the fertilization of ova post‐copulation. Increased investment in  ejaculate components may trade off with investment in precopulatory traits due to resource allocation. Alternatively, pre‐ and post‐copulatory traits could be positively related if individuals can afford to invest heavily in traits advantageous at both episodes of selection. There is empirical evidence for both positive and negative associations between pre‐ and post‐copulatory episodes, but little is known about the genetic basis of these correlations. In this study, we measured morphological, chemical and behavioural precopulatory male traits and investigated their relationship with measures of male fitness (male mating success, remating inhibition and offensive sperm competitiveness) across 40 isofemale lines of Drosophila melanogaster. We found significant variation among isofemale lines, indicating a genetic basis for most of the traits investigated. However, we found weak evidence for genetic correlations between precopulatory traits and our indices of male fitness. Moreover, pre‐ and post‐copulatory episodes of selection were uncorrelated, suggesting selection may act independently at the different episodes to maximize male reproductive success.     

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

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

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.     

Nuptial feeding in the scorpionfly <Emphasis Type="Italic">Panorpa vulgaris</Emphasis>: maintenance of genetic variance in sexual advertisement through dependence on condition influencing traits

In Panorpa vulgaris scorpionflies, females choose males on the basis of their saliva secretion ability depending on salivary gland weight. Condition dependent salivary gland weight indicates male quality in terms of food acquisition ability (FAA). In the present study we compare standardised estimates of additive genetic variance (V _a) in conditional status and salivary gland weight under conditions including and excluding food competition. Estimates of V _a were high when individuals compete for food and significantly lower when food competition was excluded, indicating that a large proportion of V _a in conditional status as well as salivary gland weight attributes to V _a in FAA. As FAA is likely to be determined by various underlying traits, maintenance of V _a in FAA, and therewith in salivary gland weight, is easily conceivable. Furthermore, we found a strong genetic correlation between condition and salivary gland weight under conditions including food competition that decreased when food competition was excluded and thereby diminished the strength of sexual selection on condition influencing traits. In sum, our results demonstrate that estimates of V _a in sexual signals (especially if estimated using standardised breeding conditions) will be strongly influenced by the presence/absence of environmental factors related to male performance in natural selection context.     

The notal organ of the scorpionfly (Panorpa vulgaris): an adaptation to coerce mating duration

The notal organ in P. vulgaris (Insecta: Mecoptera) is a clamplikestructure on the dorsum of the middle of the male’s abdomenthat holds one of the female’s forewings throughout mating.Males often provide salivary masses as food to their mates duringmating, and a male’s ability to produce saliva dependsupon whether he has fed adequately before mating. To test thehypothesis that the evolutionary function of the notal organis to coerce longer matings than are in the interests of females,the notal organ and the amount of food males and females receivebefore mating were experimentally manipulated. In support ofthe hypothesis, copulation was reduced when the notal organwas made inoperative under the following four conditions: (1)female fed and male starved before mating, no saliva duringmating; (2) same as in condition 1 but with one salivary massduring mating; (3) both sexes starved before mating, no salivarymass during mating; and (4) both sexes fed before mating. However,when females were starved before mating and males were fed,resulting in multiple masses being provided during mating, thenotal organ had no effect on length of copulation, and thusthere was no sexual conflict over mating duration. In addition,the larger the female relative to her mate, the briefer thecopulation when the notal organ was operative, which suggeststhat a physical struggle between the male and female may occurduring sexual conflict about mating duration. This is one ofonly a few studies that provide evidence of adaptation to thedomain of sexual coercion. [Behav Ecol 1991;2:156–164]     

Genetic and nutritional effects on male traits and reproductive performance in Tribolium flour beetles

In Tribolium flour beetles and other organisms, individuals migrate between heterogeneous environments where they often encounter markedly different nutritional conditions. Under these circumstances, theory suggests that genotype-by-environment interactions (GEI) may be important in facilitating adaptation to new environments and maintaining genetic variation for male traits subject to directional selection. Here, we used a nested half-sib breeding design with Tribolium castaneum to partition the separate and joint effects of male genotype and nutritional environment on phenotypic variation in a comprehensive suite of life-history traits, reproductive performance measures across three sequential sexual selection episodes, and fitness. When male genotypes were tested across three nutritional environments, considerable phenotypic plasticity was found for male mating and insemination success, longevity and traits related to larval development. Our results also revealed significant additive genetic variation for male mating rate, sperm offence ability (P(2)), longevity and total fitness and for several traits reflecting both larval and adult resource use. In addition, we found evidence supporting GEI for sperm defence ability (P(1)), adult longevity and larval development; thus, no single male genotype outperforms others in every nutritional environment. These results provide insight into the potential roles of phenotypic plasticity and GEI in facilitating Tribolium adaptation to new environments in ecological and evolutionary time.     

The function of nuptial feeding in insects: a review of empirical studies

Nuptial feeding encompasses any form of nutrient transfer from the male to the female during or directly after courtship and/or copulation. In insects, nuptial gifts may take the form of food captured or collected by the male, parts, or even the whole of the male's body, or glandular products of the male such as salivary secretions, external glandular secretions, the spermatophore and substances in the ejaculate. Over the past decade, there has been considerable debate over the current function of nuptial feeding in insects. This debate has centred on the issue of whether nuptial gifts function as paternal investment (i.e. function to increase the fitness and/or number of the gift-giving male's own offspring) or as mating effort (i.e. function to attract females, facilitate coupling, and/or to maximize ejaculate transfer), although the two hypotheses are not mutually exclusive. In the present article, evidence for the potential of nuptial gifts to function as either paternal investment, mating effort, or both is reviewed for each form of nuptial feeding in each insect taxon for which sufficient data are available. Empirical evidence suggests that many diverse forms of nuptial feeding in different insect taxa function, at least in part, as mating effort. For example, nuptial prey and salivary masses in the Mecoptera, regurgitated food in Drosophila (Diptera), hind-wing feeding in Cyphoderris (Orthoptera) and the secretion of the male's cephalic gland in Neopyrochroa (Coleoptera) and Zorotypus (Zoraptera) appear to function to entice females to copulate and/or to facilitate coupling. Nuptial prey and salivary masses in the Mecoptera also appear to function to maximize ejaculate transfer (which is also a form of mating effort), as do nuptial prey in Empis (Diptera), external glandular secretions in Oecanthus and Allonemobius (Orthoptera) and the spermatophylax in gryllids and tettigoniids (Orthoptera). Large spermatophores in, for example, the Lepidoptera and Coleoptera, also appear to be maintained by selection on the male to maximize ejaculate transfer and thereby counter the effects of sperm competition. In contrast to the large amount of evidence in support of the mating effort hypothesis, there is a relative lack of good evidence to support the paternal investment hypothesis. Certain studies have demonstrated an increase in the weight and/or number of eggs laid as a result of the receipt of larger gifts, or a greater number of gifts, in tettigoniids, gryllids, acridids, mantids, bruchid beetles, drosophilids and lepidopterans. However, virtually all of these studies (with the possible exception of studies of the spermatophylax in tettigoniids) have failed to control adequately for hormonal substances in the ejaculate that are known to affect female reproductive output. Furthermore, in at least four tettigoniids (but not in the case of two species), three lepidopterans, a drosophilid and probably also bruchid beetles and bittacids, evidence suggests that the male has a low probability of fertilising the eggs that stand to benefit from his nuptial gift nutrients. Therefore, the hypothesis that paternal investment might account for the function of nuptial gifts in general is not supported.     

Unpredictable offspring survivorship in the damselfly, Megaloprepus coerulatus, shapes parental behavior, constrains sexual selection, and challenges traditional fitness estimates

Evolutionary biologists typically assume that the number of eggs fertilized or developing embryos produced is correlated with an individual's fitness. Using microsatellite markers, we document for the first time estimates of realized fitness quantified as the number of offspring surviving to adulthood in an insect under field conditions. In a territorial damselfly whose males defend tree hole oviposition sites, patterns of offspring survivorship could not be anticipated by adults. Fewer than half of the parents contributing eggs to a larval habitat realized any reproductive success from their investment. The best fitness correlate was the span over which eggs in a clutch hatched. Among parents, female fecundity and male fertilization success were poor predictors of realized fitness. Although body size was correlated with female clutch size and male mating success, larger parents did not realize greater fitness than smaller ones. The uncoupling of traditional fitness surrogates from realized fitness provides strong empirical evidence that selection at the larval stage constrains selection on mated adults.     

Male‐induced costs of mating for females compensated by offspring viability benefits in an insect

Sexual conflict facilitates the evolution of traits that increase the reproductive success of males at the expense of components of female fitness. Theory suggests that indirect benefits are unlikely to offset the direct costs to females from antagonistic male adaptations, but empirical studies examining the net fitness pay‐offs of the interaction between the sexes are scarce. Here, we investigate whether matings with males that invest intrinsically more into accessory gland tissue undermine female lifetime reproductive success (LRS) in the cricket Teleogryllus oceanicus. We found that females incur a longevity cost of mating that is proportional to the partner’s absolute investment into the production of accessory gland products. However, male accessory gland weight positively influences embryo survival, and harmful ejaculate‐induced effects are cancelled out when these are put in the context of female LRS. The direct costs of mating with males that sire offspring with higher viability are thus compensated by direct and possibly indirect genetic benefits in this species.     

Contribution of maternal effects to dietary selection in Mediterranean fruit flies

Individual responses to dietary variation represent a fundamental component of fitness, and nutritional adaptation can occur over just a few generations. Maternal effects can show marked proximate responses to nutrition, but whether they contribute to longer term dietary adaptation is unclear. Here, we tested the hypotheses that maternal effects: (i) contribute to dietary adaptation, (ii) diminish when dietary conditions are constant between generations, (iii) are trait‐specific and (iv) interact with high‐ and low‐quality food. We used experimental evolution regimes in the medfly (Ceratitis capitata) to test these predictions by subjecting an outbred laboratory‐adapted population to replicated experimental evolution on either constant high calorie sugar (‘A’) or low‐calorie starch (‘S’) larval diets, with a standard adult diet across both regimes. We measured the contribution of maternal effects by comparing developmental and adult phenotypes of individuals reared on their own diet with those swapped onto the opposite diet for either one or two generations (high and low maternal effect conditions, respectively), both at the start and after 30 generations of selection. Initially, there were strong maternal effects on female body mass and male mating success but not larval survival. Interestingly, the initial maternal effects observed in female body mass and male mating success showed sex‐specific interactions when individuals from high calorie regimes were tested on low calorie diets. However, as populations responded to selection, the effects of maternal provisioning on all traits diminished. The results broadly supported the predictions. They show how the contribution of maternal effects to dietary responses evolves in a context‐dependent manner, with significant variation across different fitness‐related traits. We conclude that maternal effects can evolve during nutritional adaptation and hence may be an important life history trait to measure, rather than to routinely minimize.     

Selection and reproductive success in males of the dragonfly,Orthetrum japonicum (Odonata: Libellulidae)

Reproductive success, copulation success, and mating success were measured for a population of male dragonflies,Orthetrum japonicum. Copulation success explained the greatest variation in reproductive success. The proportion of copulations followed by oviposition was positively correlated with the number of oviposited eggs per mating. Directional selection on four morphological characters was estimated. The effect of selection on correlated traits was comparable to that of direct selection. Directional selection varied between traits and between episodes in a single trait. The probability that the observed directional selection on the four morphological traits was expected under the condition of the selective neutrality of traits was not smaller than 5%.     

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.     

Eutrophication and predation risk interact to affect sexual trait expression and mating success

Sexual traits are especially sensitive to low food resources. Other environmental parameters (e.g., predation) should also affect sexual trait expression by favoring investment in viability traits rather than sexual traits. We know surprisingly little about how predators alter investment in sexual traits, or how predator and resource environments interact to affect sexual trait investment. We explored how increasing phosphorous (P) availability, at a level mimicking cultural eutrophication, affects the development of sexual, nonsexual, and viability traits of amphipods in the presence and absence of predators. Sexual traits and growth were hypersensitive to low P compared to nonsexual traits. However, a key sexual trait responded to low P only when predator cues were absent. Furthermore, investment trade-offs between sexual traits and growth only occurred when P was low. The phenotypic changes caused by predator cues and increased P availability resulted in higher male mating success. Thus, eutrophication not only affects sexual trait expression but also masks the trade-off between traits with similar P demand. Sensitivity of sexually selected traits to changes in P, combined with the important roles these traits play in determining fitness and driving speciation, suggests that human-induced environmental change can greatly alter the evolutionary trajectories of populations.     

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.