Starvation and the Mating Success of Wild Male Mediterranean Fruit Flies (Diptera: Tephritidae)

Recent evidence suggests that the nutritional state of male Mediterranean fruit flies, Ceratitis capitata (Wied.) (medfly), is an important influence on various components of their reproductive biology, including mating success. The objective of the present study was to examine experimentally the effect of temporary starvation on the mating success of wild male C. capitata. Males were maintained on protein–sugar or sugar-only diets, and for each diet we compared the mating success of continuously fed males versus males starved for 18 or 24 h immediately before testing. In trials conducted on field-caged, host trees, males starved for 24 h obtained only about half as many matings as fed males for both diets. However, when the starvation period was 18 h, starved males reared on the protein–sugar diet mated significantly less frequently than fed males, whereas starved males reared on sugar mated as often as fed males. Measurements of male pheromone calling and female attraction revealed that reduced mating success likely reflected the decreased signaling activity of starved males.     

Sperm competition generates evolution of increased paternal investment in a sex role‐reversed seed beetle

When males provide females with resources at mating, they can become the limiting sex in reproduction, in extreme cases leading to the reversal of typical courtship roles. The evolution of male provisioning is thought to be driven by male reproductive competition and selection for female fecundity enhancement. We used experimental evolution under male‐ or female‐biased sex ratios and limited or unlimited food regimes to investigate the relative roles of these routes to male provisioning in a sex role‐reversed beetle, Megabruchidius tonkineus, where males provide females with nutritious ejaculates. Males evolving under male‐biased sex ratios transferred larger ejaculates than did males from female‐biased populations, demonstrating a sizeable role for reproductive competition in the evolution of male provisioning. Although larger ejaculates elevated female lifetime offspring production, we found little evidence of selection for larger ejaculates via fecundity enhancement: males evolving under resource‐limited and unlimited conditions did not differ in mean ejaculate size. Resource limitation did, however, affect the evolution of conditional ejaculate allocation. Our results suggest that the resource provisioning that underpins sex role reversal in this system is the result of male–male reproductive competition rather than of direct selection for males to enhance female fecundity.     

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.     

Environmental conditions affect sex expression in monoecious, but not in male and female plants of Urtica dioica

Urtica dioica is a sub-dioecious plant species, i.e. males and females coexist with monoecious individuals. Under standard conditions, seed sex ratio (SSR, fraction of males) was found to vary significantly among seed samples collected from female plants originating from the same population (0.05–0.76). As a first step, we investigated the extent to which SSR and sex expression of male, female, and monoecious individuals is influenced by external factors. We performed experiments to analyse: (1) whether the environment of a parental plant affects the sex ratio (SR) of its offspring, (2) whether SSR can be affected by environmental conditions before flowering, and (3) whether sex expression of male, female and monoecious plants that have already flowered can be modified by environmental conditions or by application of phyto-hormones. Within the range of our experimental design, SSR was not influenced by external factors, and gender in male and female plants was stable. However, sex expression in monoecious plants was found to be labile: flower sex ratio (FSR, fraction of male flowers) differed considerably between clones from the same individual within treatments, and increased toward 100% maleness under benign conditions. These results provide strong evidence that monoecious individuals are inconstant males, which alter FSR according to environmental circumstances. In contrast, we consider sex expression in male and female individuals to be solely genetically based. The observed variation in SSR between maternal parents cannot be explained by sex-by-environment interactions.     

Reproductive energetics of the role reversing bushcricket,Kawanaphila nartee (Orthoptera: Tettigoniidae: Zaprochilinae)

Theory predicts that sexual differences in reproductive strategies arise because of differences in the magnitude of investment made by males and females in reproduction. In some bushcrickets, the typical sex role of competitive male and choosy female is reversed when populations are subject to nutrient stress. Here I present an energetic analysis of reproduction for the role reversing bushcricket, Kawanaphila nartee, that supports the contention that this sex role reversal is a consequence of reversal in the pattern of relative reproductive investment. When fed ad libitum, males spent 16% of their daily energy reserves on the spermatophore compared with 26% spent on calling to attract a mate. Females spent 29% of their daily energy reserves in producing and laying eggs. However, when allowed only limited access to food, female expenditure in eggs was reduced to 23% of daily reserves while male expenditure remained unchanged. After accounting for the incorporation of male nutrients into eggs, female energy expenditure in reproduction exceeded male expenditure when animals were fed ad libitum, but male expenditure exceeded female expenditure when diet was limited. This role reversal in relative energy expenditure that is associated with courtship role reversal supports classical and contemporary theories on the control of sexual selection.     

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.     

Paternity Analysis in a Hexapod (Orchesella cincta; Collembola) with Indirect Sperm Transfer

In species where males and females interact during mating, the role of females in sexual selection cannot always be demonstrated unambiguously. Here we present a model system to study female choice for mates. Orchesella cinca is a soil-dwelling hexapod with indirect sperm transfer. Females and males do not interact physically for reproduction. We gave females the choice between spermatophores produced by two different males. Paternity analysis based on microsatellite variation revealed that offspring in one clutch were sired by one male only. Direct observations showed that after a female has taken up a spermatophore, the female's receptivity to further spermatophore uptake seem to end. Our results imply that the female is in full control of paternity.     

Male Condition, Female Choice, and Extreme Variation in Repeated Mating in a Scaly Cricket, Ornebius aperta (Orthoptera: Gryllidae: Mogoplistinae)

Mating in the scaly cricket Ornebius aperta often includes the transfer of many spermatophores to individual females during extended copulatory interactions. We manipulated male condition in staged matings to determine whether this could explain variation in the number of repeated copulations seen across pairs. Males on a high nutrient diet were in good condition, were more likely to mate repeatedly, and transferred more spermatophores on average than low-diet males (in poor condition). High-diet males were more likely to produce a vibratory signal that increased female receptivity to repeated mating attempts. Courtship and copulatory interactions were always terminated by females, and in every case males had already formed a spermatophore when deserted by females. We conclude that variation in male repeated mating success may be due to female choice rather than an inability or unwillingness of low-diet males to produce spermatophores.     

Behavioral and electrophysiological responses of Helicoverpa assulta, H. armigera (Lepidoptera: Noctuidae), their F1 hybrids and backcross progenies to sex pheromone component blends

Two sibling species, Helicoverpa assulta and Helicoverpa armigera both use (Z)-9-hexadecenal and (Z)-11-hexadecenal as their sex pheromone components but in almost reversed ratios, 93:7 and 3:97, respectively. H. assulta and H. armigera males performed upwind flight in response to the H. assulta sex pheromone blend (93:7). H. armigera responded strongly to the H. armigera blend (3:97), whereas H. assulta males remained inactive upon exposure to this blend. Both species gave clear dose-dependent electrophysiological responses to (Z)-11-hexadecenal. However, (Z)-9-hexadecenal evoked strong dose-dependent electrophysiological responses in H. assulta males but not in H. armigera. The two male F₁ hybrids exhibited similar behavioral responses to two sex pheromone blends and electrophysiological responses to two pheromone components as H. armigera males. This indicated that H. armigera genes appear dominant in determining the behavioral response and electrophysiological responses. Behavioral and electrophysiological responses of backcrosses of male F₁ hybrids (H. armigera female × H. assulta male) with female H. assulta and H. armigera were close to that of H. assulta and H. armigera, respectively. However, backcrosses of female F₁ hybrids (H. assulta female × H. armigera male) with male H. assulta and H. armigera showed reduced behavioral responses but normal electrophysiological responses compared to males of the respective parental line.     

Male and female condition influence mating performance and sexual receptivity in two tropical fruit flies (Diptera: Tephritidae) with contrasting life histories

Recent recognition of widespread polyandry in insects has generated considerable interest in understanding why females mate multiple times and in identifying factors that affect mating rate and inhibit female remating. However, little attention has been paid to understanding the question from both a female and male perspective, particularly with respect to factors that may simultaneously influence female remating rates. Here, we report on a study aimed at ascertaining the possible interactive effects that male and female size and diet, and female access to a host could have on mating latency, probability, and duration and female refractory period using two tropical fruit fly species with contrasting life histories. Of all factors tested, adult diet played the most significant role. Both Anastrepha ludens and Anastrepha obliqua males which had constant access to protein and sucrose mated more often, had shorter copulations and induced longer refractory periods in females than males fed a low quality diet (sucrose offered every third day). Female size and the interaction with male diet determined how quickly female A. ludens mated for the first time. Smaller females mated sooner with low quality fed males than with high quality fed males while there was no difference for large females, suggesting that male choice may be at play if high quality fed males discriminate against smaller females. Copulation duration also depended on both male and female nutritional condition, and the interaction between male diet and female size and diet. Large and high quality fed females had shorter copulations regardless of male condition. Importantly, for A. ludens, female refractory period depended on male size and the nutritional condition of both males and females, which could indicate that for this species, female receptivity does not depend only on the condition of the male ejaculate. For A. obliqua refractory period was associated with the interaction between male size and diet and male diet and host presence. We discuss our results in terms of male ability to inhibit female remating and the relative contribution of female condition to this behavior. We also address the importance of studying effects simultaneously on species with contrasting life histories.     

Daily production of spermatophores, sperm number and spermatophore size in two eriophyoid mite species

Under dissociated sperm transfer, (non-pairing) males deposit spermatophores on a substrate, while females seek spermatophores and pick up sperm on their own. Spermatophore expenditures of non-pairing males should be high, due to the increased uncertainty of sperm uptake by a female. In this study I examined spermatophore expenditures in two eriophyoid species that differed in the degree of dissociation between sexes: (1) Aculus fockeui (Nalepa and Trouessart) males rarely visit quiescent female nymphs (QFNs), and mostly deposit spermatophores all over the leaves, whereas (2) Aculops allotrichus (Nalepa) males guard QFNs for many hours and deposit several spermatophores beside them. Males of both species were collected from the field and tested in solitude. Aculus fockeui males deposited on average 19.1 spermatophores per day, whereas A. allotrichus deposited only 3.6 spermatophores per day, and had a very large coefficient of variation. Males and spermatophores of A. allotrichus were significantly smaller and contained less sperm than those of A. fockeui. In both eriophyoids, spermatophore size was fitted to the size of female genitalia and the height of females. The ratio between the diameter of spermatophore head and the width of a female genital coverflap was 0.6, whereas the ratio between the female leg and the length of spermatophore stalk was 0.5. Several factors could be responsible for the discrepancy in spermatophore expenditures between species. Among other factors, the effects of male size, male reproductive strategy and female genitalia size on spermatophore output and size of spermatophores are discussed.     

The effect of the presence of quiescent female nymphs, males and their spermatophores on spermatophore placement in two species of eriophyoid mites

Under sex dissociated sperm transfer, females seek spermatophores and pick up sperm without male assistance. In several species males adjust spermatophore deposition rate to the presence of conspecifics. It is not known, however, which factors could favor such elasticity in non-pairing males. In this paper, we compare male response towards conspecifics between the sex dissociated eriophyoid mites Aculus fockeui (Nalepa and Trouessart) and Aculops allotrichus (Nalepa). The species differ significantly in male reproductive strategies and, consequently, the intensity of male–male-competition. Aculus fockeui males deposit spematophores all over the leaves and occasionally leave single spermatophores beside quiescent female nymphs (QFNs). In contrast, A. allotrichus males guard QFNs and encircle them with spermatophores. In this study, males of both species deposited spermatophores close to and apart from the rival spermatophores. Aculops allotrichus males had similar spermatophore output whether they were kept alone or in a group of seven males. They did not change spermatophore output in the presence of five rival spermatophores, a QFN or a QFN and varying number of rivals, either. In contrast, A. fockeui males increased spermatophore output in the presence of rival spermatophores or when on the arena with a QFN the male number increased to eight males. They did not respond, however, to the presence of a QFN and one rival or a QFN alone. The possible effect of the species-specific intensity of male–male competition, population density, the availability of receptive females and the rate of spermatophore output on the flexibility of eriophyoid spermatophore deposition is discussed.     

Change of external sexual characteristics during consecutive moults in Crangon crangon L

Adult males of the North Sea shrimp, Crangon crangon, were maintained for 8 months in the laboratory under natural temperature and light cycles. Successive moults were analysed for morphological changes. Out of the 70 shrimps, one male performed morphological sex reversal by reducing the male characteristics and developing female characteristics. The morphological changes including the loss of the appendix masculina appeared within a single moult cycle. This observation proves that C. crangon males may be capable of changing sex. The low number of sex reversals indicates that C. crangon is a facultative rather than an obligate protandric hermaphrodite.     

Epigenetic control of sexual phenotype in a dioecious plant,Melandrium album

Melandrium album (syn.Silene latifolia) is a model dioecious species in which theY chromosome, present only in heterogametic males, plays both a male-determining and a strict female-suppressing role. We showed that treatment with 5-azacytidine (5-azaC) induces a sex change to androhermaphroditism (andromonoecy) in about 21% of male plants, while no apparent phenotypic effect was observed in females. All of these bisexual androhermaphrodites (with the standard male 24,AA +XY karyotype) were mosaics possessing both male and hermaphrodite flowers and, moreover, the hermaphrodite flowers displayed various degrees of gynoecium development and seed setting. Southern hybridization analysis with a repetitive DNA probe showed that the 5-azacytidine-treated plants were significantly hypomethylated in CG doublets, but only to a minor degree in CNG triplets. The bisexual trait was transmitted to two successive generations, but only when androhermaphrodite plants were used as pollen donors. The sex reversal was inherited with incomplete penetrance and varying expressivity. Based on the uniparental inheritance pattern of androhermaphroditism we conclude that it originated either by 5-azaC induced inhibition ofY-linked female-suppressing genes or by a heritable activation of autosomal female-determining/promoting genes which can be reversed, on passage through female meiosis, by a genomic imprinting mechanism. The data presented indicate that female sex suppression inM. album XY males is dependent on methylation of specific DNA sequences and can be heritably modified by hypomethylating drugs.     

Dietary constraints on sexual activity, mating success, and survivorship of male Delia antiqua

The effects of protein-deprivation on the sexual activity and reproductive fitness of male onion flies, Delia antiqua (Meigen) (Diptera: Anthomyiidae), were investigated under laboratory conditions. The percentage of males inseminating gravid females, the magnitude of ovipositional response, and the total numbers of eggs deposited in 1:1 or 1:10 male:female matchings over two days was unaffected by deprivation of dietary protein. The LT₅₀'s (median survival time) for solitary males provided proteinaceous, sucrose, or water diets were 38.0, 25.8, and 6.0 days, respectively. Yet independent of diet effects, males lost 50% of their wing tissue by fragmentation after 26 days, suggesting that wing condition is more important in determining male reproductive fitness than longevity. Male mating frequency in single pairings with previtellogenic females deprived of proteinaceous diet for ten days was similar to that of gravid, protein-fed females. In no-choice and choice mating bioassays at a 10:1 female:male ratio, however, males inseminated significantly fewer previtellogenic than gravid females over 24 h. Despite evidence for male autogeny, removal of exogenous protein resources in the Allium agroecosystem may have important effects on the reproductive competency and fecundity of D. antiqua.     

Spermatophore transfer in Euchaeta species in a 2000 m water column

The numbers and placement of spermatophores transferred by males to females in the genus Euchaeta are examined in the northeastern Atlantic Ocean. Multiple placement of spermatophores is present in the five diel, vertically migrating species, E. acuta, E. pseudotonsa, E. gracilis, E. norvegica and E. hanseni. Direct placement covering the genital opening is usually, but not always the primary placement site. Males produce two sizes of spermatophores corresponding to the small directly placed and the large indirectly placed ones attached to the females. Females of the other species, E. barbata, E. barbata f. farrani, E. scotti, E. bisinuata, E. sarsi, E. abbreviata, E. longissima and E. bradyi, all meso- or bathypelagic non-vertically migrating species, have a single spermatophore attached to the genital opening. Spermatophore size is related to male and female prosome lengths and to the depth at which the species lives. Size variation of spermatophores within species decreases with increasing depth. Spermatophore transfer in deep-sea species, a single spermatophore directly placed, appears to be more efficient than in the epipelagic and mesopelagic vertical migrators where multiple placement involves a proportion of spermatophores with no direct connection to the genital opening.     

Competing Females and Caring Males. Polyandry and Sex-Role Reversal in African Black Coucals, Centropus grillii

Most species of birds show bi‐parental or female‐only care. However, a minority of species is polyandrous and expresses male‐only care. So far, such reversals in sex roles have been demonstrated only in precocial bird species, but there was suggestive evidence that such a mating system may occur in one altricial bird species, the black coucal, Centropus grillii. In a field study in Tanzania we investigated whether black coucals are sex‐role reversed and polyandrous. We found that males were mated to one female, rarely vocalized and provided all parental care from incubation of eggs to feeding of young. In contrast, female black coucals were about 69% heavier and 39% larger than males and polyandrous. They spent a large proportion of time calling from conspicuous perches, defended breeding territories, did not help in provisioning young and had a higher potential reproductive rate than males. We conclude that the black coucal currently represents the only altricial bird species with sole male parental care and a classical polyandrous mating system. High nest predation pressure and small territory sizes due to high food abundance may have been important factors in the evolution of sex‐role reversal and polyandry in this species.     

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.

     

The Role of Courtship Behavior and Size in Mate Preference in the Sex‐Role‐Reversed Gulf Pipefish,Syngnathus scovelli

In sex‐role‐reversed species, sexual selection acts more strongly on females than on males, a situation that can result in the evolution of secondary sexual traits in females and strong mating preferences in males. While some research exploring mating preferences in sex‐role‐reversed species has been conducted, overall, this topic remains relatively unexplored. The Gulf pipefish, Syngnathus scovelli, is a highly polyandrous pipefish species. Sexual selection is significantly stronger in females than in males, which has led to the evolution of both morphological and behavioral female secondary sexual traits. However, because males gestate the offspring in specialized pouches and make a substantial investment in embryos during development, females may also benefit from being choosy. The goal of this study was to examine both male and female mating preferences in this species. We found that male mating preference was significantly associated with female courtship behavior. Larger females were also able to maintain these behaviors for longer intervals than smaller females. No evidence of female mating preference in regard to male size was observed but the data suggest that male behaviors may be providing positive reinforcement to courting females. This research provides further insight into how mate preferences vary among sex‐role‐reversed species.     

Differential introgression of a female competitive trait in a hybrid zone between sex‐role reversed species

Mating behavior between recently diverged species in secondary contact can impede or promote reproductive isolation. Traditionally, researchers focus on the importance of female mate choice and male–male competition in maintaining or eroding species barriers. Although female–female competition is widespread, little is known about its role in the speciation process. Here, we investigate a case of interspecific female competition and its influence on patterns of phenotypic and genetic introgression between species. We examine a hybrid zone between sex‐role reversed, Neotropical shorebird species, the northern jacana (Jacana spinosa) and wattled jacana (J. jacana), in which female–female competition is a major determinant of reproductive success. Previous work found that females of the more aggressive and larger species, J. spinosa, disproportionately mother hybrid offspring, potentially by monopolizing breeding territories in sympatry with J. jacana. We find a cline shift of female body mass relative to the genetic center of the hybrid zone, consistent with asymmetric introgression of this competitive trait. We suggest that divergence in sexual characteristics between sex‐role reversed females can influence patterns of gene flow upon secondary contact, similar to males in systems with more typical sex roles.