Emergence rhythms and protandry in relation to daily patterns of locomotor activity inTrichogramma species

Summary In insect parasitoids, the mating structure of the population depends on the emergence pattern of adults and on their behaviour after emergence. In order to study some aspects of these characteristics in four species of egg parasitoid of the genusTrichogramma, laboratory experiments using automatic video analysis are performed. Adult emergence is concentrated in the morning, with an earlier time for males. The variability of the time of emergence is under genetic control. The relationships between the emergence pattern and the locomotor activity are considered by measuring individually: first, the delay between the emergence and the first locomotion which is significantly greater in females than in males and, second, the activity of newly emerged males, which is maximum at the time of the emergence of females. The locomotor activity is influenced by mating; mated females are much more active than virgin ones, mated males are less active than virgin ones. The adaptive values of the rhythmicity of emergence and of protandry are discussed together with their relationship with the patterns of locomotor activity. The results are also considered with respect to mating strategies in insect parasitoids; they actually support the hypothesis of mating occurring principally among individuals native to the same host patch inTrichogramma species.     

Virgin females compete for mates in the male lekking species Ceratitis capitata

Abstract. Aggressive behaviour occurring in intrasexual competition is an important trait for animal fitness. Although female intrasexual aggression is reported in several insect species, little is known about female competition and aggressive interactions in polygynous male lekking species. The interactions of female Mediterranean fruit flies, Ceratitis capitata (a male lekking species), with other females and mating pairs under laboratory conditions are investigated. Mature, unmated (virgin) females are aggressive against each other and against mating pairs, whereas immature females are not. Female aggression against other females decreases dramatically after mating; however, mated females maintain aggression against mating pairs. In addition, higher intrasexual aggression rates are observed for mature, virgin females than for virgin males of the same age. The results show that female aggressiveness is virginity related, suggesting female competition for mates. These findings have important implications for understanding the physiological aspects of a complex social behaviour such as aggression and should stimulate further research on female agonistic behaviour in male lekking mating systems.     

Effects of female body size and age and male mating status on male combat in Anastatus disparis (Hymenoptera: Eupelmidae)

1. Aggressive behaviour is widely exhibited by animals to acquire important resources and usually shows a dangerous or nondangerous pattern. Dangerous fighting patterns are usually characterized by fights ending with contestants being severely injured or killed. Resource value is an important nonstrategic factor influencing fighting behaviour. Studies of many species addressing nondangerous fighting behaviour have shown that when resource values change, organisms usually adjust their fighting behaviour accordingly. Only a few species show dangerous fighting patterns. Thus, few relevant studies have addressed how variation in resource value affects aggression with a dangerous fighting pattern. 2. Here, an egg parasitoid wasp, Anastatus disparis, which exhibits a dangerous fighting pattern to acquire mating opportunities, was used as an experimental model to study the adjustment of fighting behaviour resulting from a change in resource value. 3. Our results show that the female properties of body size and age affect their objective resource value and that males increased their fighting intensity for relatively large and young females. However, male mating status in A. disparis may not influence the subjective value of mate resources, and fighting intensity did not significantly differ between mated and virgin males. In addition, the number of times a male had previously mated had no significant effect. These results suggest that mating opportunities are important for both virgin and mated males, resulting in neither of them showing any adjustment in fighting for mating opportunities. 4. Generally, A. disparis males with extreme fighting patterns adjust their fighting behaviour according to the variation in resource value, which avoids the meaningless costs of injury and death.     

Peripheral modulation of olfaction by physiological state in the Egyptian leaf worm Spodoptera littoralis (Lepidoptera: Noctuidae)

Insects show behavioural plasticity based on their physiological state. Deprivation from a resource will normally make them more responsive to it or to perform behaviour increasing the probability of encountering such a resource. Modulation of the olfactory system has been shown mainly in the central nervous system, but also in the periphery. In this study, antennal sensitivity of females of the Egyptian cotton leaf worm Spodoptera littoralis to different plant and sex pheromone odours was measured using electroantennography (EAG). Different mating status, age, and feeding status were used to investigate peripheral changes in olfactory responses. Virgin females were found to be more sensitive to plant odours and sex pheromone compared to mated females. Age also had an impact on antennal sensitivity, 2 and 4 days old females being more sensitive than just-emerged ones. Such an increase in sensitivity could be explained by maturation of olfactory receptor neurons after emergence or by an increase in motivation as the available expected life time remaining decreases. Finally, feeding status did not modify the antennal sensitivity of females. A peripheral modulation could thus be demonstrated in the olfactory system of female Spodoptera littoralis at certain life stages.     

Behavioural consequences of cold exposure on males and females of <Emphasis Type="Italic">Aphidius rhopalosiphi</Emphasis> De Stephani Perez (Hymenoptera: Braconidae)

Cold storage of insect parasitoids is currently used before mass release in the field in biological control programmes. The physiological consequences of constant cold storage are known in various species of parasitic wasps, but there are few reports on the behaviour of survivors and even fewer reports where both sexes were tested. In this study, we observed the consequences of a long storage of Aphidius rhopalosiphi De Stephani Perez (Hymenoptera: Braconidae), a parasitoid of the cereal aphid Sitobion avenae Fabricius (Hemiptera: Aphididae), at low temperature on some key behavioural decisions that both sexes will make when released in the field. Males are less tolerant than females and both sexes suffer from a long exposure (28 days or more) at 4°C during the pupal stage: alteration of olfactory responses, decrease in mating capacity and decrease in the efficiency of patch exploitation by females.     

Influence of mating experience on mating latency and copulation duration in <Emphasis Type="Italic">Drosophila melanogaste</Emphasis> females

Two important components of mating behavior, mating latency and duration of copulation, were examined during first and second mating in D. melanogaster females. Our results confirm the published findings of lower receptivity of previously mated D. melanogaster females, since fertilized females present significantly longer mating latencies. Duration of copulation also depends on female mating experience, as naive females copulated significantly longer than those previously mated. An important role of female D. melanogaster in the control of both examined components of mating behavior is displayed in the course of second mating, as part of behavioral and physiological changes induced by the first mating. The article is published in the original.     

Polyandrous females acquire indirect benefits in a nuptial feeding species

The relative force of direct and indirect selection underlying the evolution of polyandry is contentious. When females acquire direct benefits during mating, indirect benefits are often considered negligible. Although direct benefits are likely to play a prominent role in the evolution of polyandry, post‐mating selection for indirect benefits may subsequently evolve. We examined whether polyandrous females acquire indirect benefits and quantified direct and indirect effects of multiple mating on female fitness in a nuptial gift‐giving spider (Pisaura mirabilis). In this system, the food item donated by males during mating predicts direct benefits of polyandry. We compared fecundity, fertility and survival of singly mated females to that of females mated three times with the same (monogamy) or different (polyandry) males in a two‐factorial design where females were kept under high and low feeding conditions. Greater access to nutrients and sperm had surprisingly little positive effect on fitness, apart from shortening the time until oviposition. In contrast, polyandry increased female reproductive success by increasing the probability of oviposition, and egg hatching success indicating that indirect benefits arise from mating with several different mating partners rather than resources transferred by males. The evolution of polyandry in a male‐resource‐based mating system may result from exploitation of the female foraging motivation and that indirect genetic benefits are subsequently derived resulting from co‐evolutionary post‐mating processes to gain a reproductive advantage or to counter costs of mating. Importantly, indirect benefits may represent an additional explanation for the maintenance of polyandry.     

Female assessment of male functional fertility during mate choice in a promiscuous fish

Sexual selection should favour females that can assess the functional fertility of available sexual partners and avoid mating with recently mated, sperm‐depleted males. Our current understanding of the sensory mechanism(s) underlying female assessment of males based on their functional fertility and avoidance of sperm‐depleted males is incomplete. Female Trinidadian guppies (Poecilia reticulata) are known to avoid mating with males that they had previously observed mating with other females. Here, we investigated experimentally the proximate sensory cues that they use to distinguish between paired size‐ and colour‐matched mated and unmated males in the absence of visual public information on their prior mating histories. When only water‐borne chemical cues from the males were available, females avoided the previously mated male and preferred the unmated one, but they chose randomly when only male visual cues (and no chemical cues) were available. They also preferred unmated over mated males when freely swimming with them in a more sensorially complex environment with multiple male cues (i.e., visual, chemical and mechanical cues) concurrently available. Females exhibited no preference for either stimulus males when both were unmated, irrespectively of the sensory environment. These novel results suggest that, in the absence of prior visual public information on the recent mating histories of males, female guppies use olfactory cues putatively emitted by mated males to avoid mating with them. The source and nature of the implicated olfactory cues and the fitness benefits gained by female guppies in sexually preferring males that have not recently mated remain unknown and warrant further research.     

Consequence of emergence pattern on inbreeding risk in the aphid parasitoid Aphidius matricariae (Hymenoptera: Braconidae)

In insect parasitoids, mating strategy depends on mate availability and is influenced by the spatial and temporal emergence patterns of adults. For quasi-gregarious species, simultaneous emergence favors local mating and reduces search costs for partners while increasing the risk of inbreeding, particularly when only one female parasitizes the initial host patch. Consequently, in inbreeding sensitive species, mating on the place of adult emergence (patch mating) between siblings should be counter selected. In practice, the timing of male and female emergence and of their dispersal influences mate availability and can limit on patch mating. To test the role of these two factors, we analyzed the daily distribution of emergence and patch residence time of a cohort in the aphid parasitoid Aphidius matricariae (Hymenoptera: Braconidae). We observed that adult emergence is concentrated on the morning with males emerging on average before females with some overlaps. A more precise evaluation of emergence pattern within a brood suggests that brothers and sisters rarely emerge at the same time and rapid dispersal of males and females favors off-patch mating. The relationships between timing of emergence including differences between sex and consequences on inbreeding probability in these species are thus discussed.     

When Parasitoid Males Make Decisions: Information Used when Foraging for Females

Optimal foraging models predict how an organism allocates its time and energy while foraging for aggregated resources. These models have been successfully applied to organisms such as predators looking for prey, female parasitoids looking for hosts, or herbivorous searching for food. In this study, information use and patch time allocation were investigated using male parasitoids looking for mates. The influence of the former presence of females in absence of mates and the occurrence of mating and other reproductive behaviours on the patch leaving tendency was investigated for the larval parasitoid Asobara tabida. Although males do not modify their patch residence time based on the number of females that visited the patch, they do show an increase in the patch residence time after mating a virgin female and performing courtship behaviour such as opening their wings. These results are in concordance with an incremental mechanism, as it has been described for females of the same species while foraging for hosts. The similarities between males and females of the same species, and the conditions under which such a patch-leaving decision rule is fitted are discussed. This is the first study describing an incremental effect of mating on patch residence time in males, thus suggesting that similar information use are probably driving different organisms foraging for resource, regardless of its nature.     

Concurrent modulation of neuronal and behavioural olfactory responses to sex and host plant cues in a male moth

Mating has profound effects on animal physiology and behaviour, not only in females but also in males, which we show here for olfactory responses. In cotton leafworm moths, Spodoptera littoralis, odour-mediated attraction to sex pheromone and plant volatiles are modulated after mating, producing a behavioural response that matches the physiological condition of the male insect. Unmated males are attracted by upwind flight to sex pheromone released by calling females, as well as to volatiles of lilac flowers and green leaves of the host plant cotton, signalling adult food and mating sites, respectively. Mating temporarily abolishes male attraction to females and host plant odour, but does not diminish attraction to flowers. This behavioural modulation is correlated with a response modulation in the olfactory system, as shown by electro-physiological recordings from antennae and by functional imaging of the antennal lobe, using natural odours and synthetic compounds. An effect of mating on the olfactory responses to pheromone and cotton plant volatiles but not to lilac flowers indicates the presence of functionally independent neural circuits within the olfactory system. Our results indicate that these circuits interconnect and weigh perception of social and habitat odour signals to generate appropriate behavioural responses according to mating state.     

Learning enhances female control over reproductive investment in the Japanese quail

The adaptive significance of learning is supported by studies showing its positive effects on mating behaviour, but they rarely go beyond fertilization success. Here we studied how learning contributes to qualitative reproductive investment, by testing the hypothesis that mating in the context that predicts male appearance has positive effects on female reproductive investment compared with unsignalled mating. Using Japanese quail (Coturnix japonica), we found that effects of mating in the context predicting mating opportunity depend on female body condition and receptivity, while the outcome of unexpected mating depends on male behaviour. In particular, among females mated with the familiar male in the context predicting that he will appear, female condition positively affected the number of fertilized eggs and egg mass and more receptive females tended to produce more sons. Additionally, conditioned females laid heavier eggs for daughters than for sons. In contrast, in females that were mated unexpectedly and with a novel male, the number of fertilized eggs was highly dependent on male behaviour and was negatively related to maternal body condition. Egg mass was not related to body condition, and there were no indications of sex allocation. This is, to our knowledge, the first study demonstrating how female body condition and behaviour interact with the context of mating in shaping maternal reproductive investment.     

Age‐dependent investment in death‐feigning behaviour in the sweetpotato weevil Cylas formicarius

Because life‐history theory predicts that risky behaviours such as mating should increase as life expectancy decreases, predatory avoidance is expected to decrease with age. However, this prediction has not been examined. In the present study, the effect of age on death‐feigning behaviour, a form of predatory avoidance behaviour in the sweetpotato weevil Cylas formicarius (Summers) (Coleoptera: Brentidae), is investigated by performing a longitudinal study. Because the effects of mating history and age usually cannot be distinguished, mating history is controlled. The results show that only female weevils decrease the investment in death‐feigning behaviour with age, whereas male weevils do not show any age‐related change. In addition, death‐feigning behaviour of mated females is longer than that of virgin females, possibly because additional mating partners would be not needed by mated females.     

Quantitative aspects of the effect of mating on readiness to lay in the Australian sheep blowfly,Lucilia cuprina

Virgin females of Lucilia cuprinararely lay eggs, whereas mated females do so readily. This effect of mating is due entirely to increased readiness to lay, and not to any effect on ovarian development. An investigation was made of how readiness to lay was affected by matings which differed in terms of the male's chemical and mechanical contribution. Individual males were mated, during 1 day, to a succession of females whose readiness to lay was determined 1 or 8 days after mating. On both days, the proportion of females laying was inversely related to the number of females with which the male had previously mated. A high proportion of females that had mated with previously unmated or oncemated males laid at both 1 and 8 days after mating. However, this proportion tended to decline between day 1 and day 8 in females that had mated with males with two or more previous matings, and this effect was most evident in females mated with males that had previously mated with four or more females. When matings were manually terminated as soon as coupling had occurred, the proportion laying remained as low as in virgins. This proportion progressively increased as mating duration increased from 2 to 6 min. The proportion that laid after mating terminated at 6 or 8 min was as high as that for females from full-term matings (mean duration, 12.5 min). The results are generally similar to those obtained in parallel experiments on the effect of mating on sexual receptivity in this species and, therefore, indicate that the physiological bases for the two effects of mating might be the same.     

Behavioural switch of female Mediterranean fruit fly, Ceratitis capitata: mating and oviposition activity in outdoor field cages in Hawaii

1 Laboratory-reared normal, and wild female Mediterranean fruit flies, Ceratitis capitata (Wiedemann), were assayed in outdoor field cages to assess the impact of a mating-induced behavioural switch on mating and subsequent oviposition activity. 2 Virgin females preferred interactions with males leading to mating over attraction to, and oviposition in, artificial yellow spheres containing guava odour or green apples hung in a guava tree. Laboratory-reared females previously mated with either laboratory-reared normal males or laboratory-reared irradiated (sterile) males showed little interest in remating with males and instead, were much more likely to be found arrested on artificial and real fruit and ovipositing. Oviposition on artificial fruit was five times greater by females that had mated with either normal or irradiated males than by virgin females. Wild females showed similar qualitative changes in the mating-induced behavioural switch; however, oviposition activity was significantly less than for laboratory-reared females. 3 These results confirm that mating has a profound effect on the behaviour of female Mediterranean fruit flies and that irradiated males are functionally equal with normal males (lab-reared or wild) in their ability to alter female behaviour. These results are discussed in the context of the sterile insect technique for control of Mediterranean fruit flies in the field.     

Competitive environments induce shifts in host fidelity

Recent models support the idea of sympatric speciation as a result of the joint effects of disruptive selection and assortative mating. We present experimental data, testing models of speciation through frequency‐dependent selection. We show that under high competition on a mixture of resources/hosts, strains of the Seed beetle, Callosobruchus maculatus, change their host fidelity and evolve a more generalistic behaviour in resource utilization among females. The change in host fidelity did not result in disruptive selection and was not followed by assortative mating. This means that only one of three fundamental prerequisites for sympatric speciation evolved as a result of the frequency‐dependent selection. We conclude that for this process to work, a shift to a novel food resource as a result of selection must also lead to a loss of preference for the original resource such that individuals are only able to use either one of the two.     

Female Medflies Mate Selectively with Young Males but Gain No Apparent Fitness Benefits

Species in which female choice is not strongly shaped by male-controlled resources present a challenge to sexual selection research, because it is typically difficult to identify the male phenotypic cues used in female mate selection or the fitness benefits accruing from such selection. In such species, mate selection is presumably based on direct benefits associated with sperm quantity or quality and/or indirect benefits relating to the viability or mating probability of the progeny. Across animal taxa in general, male age has received considerable attention as a potential indicator of these fitness benefits, and the importance of male age in affecting female choice and fitness has been investigated in various insect species with highly variable results. The present study examined whether females of the Mediterranean fruit fly (medfly), Ceratitis capitata (Wied.), a lek-forming species, discriminate among potential mates on the basis of male age and whether this selectivity results in fitness benefits to the females. Both young (10 days old) and old (40 days old) females were offered males from two groups differing in age by 10, 20, or 30 days. Young females mated randomly when the age difference between the younger and older males was 10 days but mated preferentially with the younger males when the age difference was 20 or 30 days. Old females did not discriminate among males of different ages. Although young females showed mate selectivity, we found no differences in fecundity, fertility, or larval viability between young females mated to 10 versus 40 day old males.     

Host‐searching responses to herbivory‐associated chemical information and patch use depend on mating status of female solitary parasitoid wasps

1. In a tritrophic interaction system consisting of plants, herbivores, and their parasitoids, chemicals released from plants after herbivory are known to play important roles for many female parasitoids to find their hosts efficiently. On the plant side, chemical information associated with herbivory can act as an indirect defence by attracting the natural enemies of the host herbivores. 2. However, mated and virgin females of haplodiploid parasitoids might not necessarily respond to such chemical cues in the same way. Since virgin females can produce only sons, they might refrain from searching for hosts to invest eggs until copulation, in order to produce both sexes. 3. Here, we investigated differential host‐searching behaviours shown by mated and virgin females in the solitary parasitoid wasp, Cotesia vestalis, in response to herbivory‐associated chemical information from cruciferous plants infested by their host larvae, Plutella xylostella. 4. Mated females showed a significantly higher flight preference for host‐infested plants over intact plants, while no preference was observed with virgin females. Mated females also showed more intensive antennal searching and ovipositor probing behaviours to leaf squares with wounds caused by hosts than did virgin females. Furthermore, mated females stayed longer in host patches with higher parasitism rates than virgin females. 5. These results indicate that mating status of C. vestalis females clearly influences their host‐searching behaviour in response to herbivory‐associated chemical information and patch exploitation. Female parasitoids seem to forage for hosts depending on their own physiological condition in a tritrophic system.     

Competitive PCR reveals the complexity of postcopulatory sexual selection in Teleogryllus commodus

The outcome of mate choice depends on complex interactions between males and females both before and after copulation. Although the competition between males for access to mates and premating choice by females are relatively well understood, the nature of interactions between cryptic female choice and male sperm competition within the female reproductive tract is less clear. Understanding the complexity of postcopulatory sexual selection requires an understanding of how anatomy, physiology and behaviour mediate sperm transfer and storage within multiply mated females. Here we use a newly developed molecular technique to directly quantify mixed sperm stores in multiple mating females of the black field cricket, Teleogryllus commodus. In this species, female postcopulatory choice is easily observed and manipulated as females delay the removal of the spermatophore in favour of preferred males. Using twice‐mated females, we find that the proportion of sperm in the spermatheca attributed to the second male to mate with a female (S₂) increases linearly with the time of spermatophore attachment. Moreover, we show that the insemination success of a male increases with its attractiveness and decreases with the size of the female. The effect of male attractiveness in this context suggests a previously unknown episode of mate choice in this species that reinforces the sexual selection imposed by premating choice and conflicts with the outcome of postmating male harassment. Our results provide some of the clearest evidence yet for how sperm transfer and displacement in multiply mated females can lead directly to cryptic female choice, and that three distinct periods of sexual selection operate in black field crickets.