Receptive Females Research Articles

Does perception of female cues modulate male short-term fitness components in Drosophila melanogaster?

Phenotypic plasticity in reproductive behavior can be a strong driver of individual fitness. In species with high intra‐sexual competition, changes in socio‐sexual context can trigger quick adaptive plastic responses in males. In particular, a recent study in the vinegar fly (Drosophila melanogaster) shows that males derive net fitness benefits from being shortly exposed to female cues ahead of access to mating (termed sexual perception), but the underlying mechanisms of this phenomenon remain unknown. Here, we investigated the short‐term effects of female perception on male pre‐ and post‐copulatory components of reproductive performance: (a) mating success, (b) mating latency and duration, (c) sperm competitiveness, and (d) ejaculate effects on female receptivity and reproductive rate. We found that brief sexual perception increased mating duration, but had no effect on the other main pre‐ and post‐copulatory fitness proxies recorded. This suggests that perception of female cues may not yield net fitness benefits for males in the short‐term, but we discuss alternative explanations and future avenues of research.

Adaptive Party Choice of Low-Ranking Males in Fission-Fusion Dynamics of Chimpanzees in Kalinzu Forest Reserve, Uganda.

Simple SummaryVarious mammalian species, including primates, exhibit fission–fusion dynamics (FFD), which alters the size of subgroups through splitting and merging. Among primates, chimpanzees (Pan troglodytes) have been particularly studied as a species that exhibits a high degree of FFD, wherein members of the same group form temporary subgroups (parties) that vary in both size and composition. Most studies on the FFD of chimpanzees have focused on its role in reducing food competition among individuals. In this study, we focused on the association patterns of each adult male chimpanzee and examined whether the social factors, including male dominance rank and aggression from other males, affect their party attendance behavior. Low-ranking males spent more time alone than other males when mating opportunities were absent. When females were available for mating, males of all ranks showed a similar party attendance behavior. The aggression increased with the number of males in the party, and low-ranking males received more aggression than higher-ranking males. These results suggest that low-ranking males frequently traveled alone to avoid aggression from other males unless they attended parties to seek mating opportunities. The FFD seemed to offer alternative tactics for low-ranking males to balance the costs and benefits of attending parties.Several studies have examined factors that regulate fission–fusion dynamics (FFD) in chimpanzee communities, such as receptive females, predation risks, and food availability. However, the effects of these factors vary between populations. In this study, we conducted focal animal observations of adult males in the M group in Kalinzu to examine the influence of male dominance rank, aggression from other males, the presence of females exhibiting maximum sexual swelling (MS), and fruit abundance on male tendencies of party attendance. We found that low-ranking males spent more time alone than other males when females with MS were absent. In contrast, when females with MS were present, males of all ranks showed a similar tendency of party attendance. We also found that the aggressive interactions increased with the number of males irrespective of the presence or absence of females with MS, and low-ranking males attracted aggression more frequently than higher-ranking males. These results suggest that low-ranking males frequently ranged alone to avoid aggression from other males unless they attended parties to seek mating opportunities. We conclude that low-ranking males have alternative tactics to balance the costs and benefits incurred or gained when attending parties.

Know your enemy: The dragonfly Erythrodiplax fusca (Libellulidae) uses eavesdropping to obtain information about potential rivals

Animals can eavesdrop on other competitors during territorial defense disputes to better choose rivals weaker than themselves and increase the chances of monopolizing resources. In dragonflies, males often compete for access to water bodies, which attract sexually receptive females to mate and lay eggs. During the breeding season, satellite males can observe fights between territory owners and intruders and, therefore, obtain information about potential rivals through visual cues. Consequently, weaker competitors may face more intense competition than stronger ones when defending a territory. In this study, we conducted field experiments with the dragonfly Erythrodiplax fusca to investigate whether eavesdropping on territorial disputes, using visual cues, affects the intensity of competition that territory owners face. We recorded the number of intruders that engage in disputes against males that recently occupied territories in two groups: the “eavesdropping” group (i.e., individuals with access to rivals’ prior information) and the control group (i.e., competitors with no access to prior information). The number of intruders was greater in the eavesdropping group compared to the control group. This effect depended on the interaction between the size of the territory owners and the presence of eavesdropping. The number of intruders decreased with increase in the size of the owners in the presence of eavesdropping, but this relationship did not occur in the control group. We discuss the implications of our findings for the male decision-making process to initiate agonistic disputes and how investigating eavesdropping behavior can improve current models of conflict resolution in animals.

Movement and olfactory signals: Sexually dimorphic antennae and female flightlessness in moths

Darwin argued a role for sexual selection in the evolution of male sensory structures, including insect antennae, the strength of which will depend upon the importance of early arrival at receptive females. There is remarkable variation in the nature and degree of sexual dimorphism in moth antennae, with males of some species having spectacular, feathery antennae. Although it is widely assumed that these elaborate structures provide greater sensitivity to chemical signals (sex pheromones), the factors underlying the interspecific diversity in male antennal structure and size are poorly understood. Because male antennal morphology may be affected by several female life–history traits, including flight ability, we conducted a phylogenetic comparative analysis to test how these traits are linked, using data from 93 species of moths across 11 superfamilies. Our results reveal that elaborate antennae in males have evolved more frequently in species where females are monandrous. Further, female loss of flight ability evolved more frequently in species where males have elaborate antennae. These results suggest that elaborate antennae have evolved in response to more intense male competition, arising from female monandry, and that the evolution of elaborate antennae in males has, in turn, shaped the evolution of female flightlessness.

Sexual experience increases oxytocin, but not vasopressin, receptor densities in the medial preoptic area, ventromedial hypothalamus, and central amygdala of male rats

Oxytocin (OT) and vasopressin (VP) are considered to be principal neurochemical substrates of bonding in monogamous species. We have reported previously that conditioning of a sexual partner preference in male rats resulted in conditioned activation of OT and VP neurons in hypothalamic paraventricular and supraoptc nuclei. Here we asked whether such conditioning would also alter OT or VP receptor densities. Sexually naïve male rats were assigned to one of three groups (n = 15/group). The Paired group received 9 copulatory training trials with sexually receptive females scented with a neutral almond odor. The Unpaired group received 9 copulatory training trials with unscented sexually receptive females. The Naïve group were not given sexual experience. Paired and Unpaired males were given a final test in an open field with two receptive females, one scented and the other unscented, to assess the development of conditioned ejaculatory preference (CEP), which was expressed significantly in the Paired group. Brains from rats in the three groups were then assessed for OT receptor (OTR) or VP1a receptor (VPR) densities within cortical, limbic and hypothalamic structures using autoradiography with selective 125I-labeled receptor ligands. Sexual experience alone increased OTR significantly in the medial preoptic area (mPOA), ventromedial hypothalamus (VMH), and central nucleus of the amygdala (CeA) in both Paired- and Unpaired-trained males compared to sexually Naïve males. No differences were found for experience on VPR densities in any region. These data add to a growing body of evidence that sexual experience alters brain function and processing of sex-related cues, and suggest that enhanced activation of OTRs in the mPOA, VMH, and CeA by conditioned OT release in those regions may underlie CEP in the male rat.

The Functional Morphology of the Bursa Copulatrix of a Butterfly That Does Not Digest Spermatophores (Leptophobiaaripa, Pieridae).

The bursa copulatrix of female Lepidoptera is a complex organ where crucial male-female reproductive interactions occur during and after copulation. The bursa copulatrix receives, stores, and digests the spermatophore and other substances transferred by the male during copulation, and is involved in changes in female receptivity, ovogenesis, and oviposition. Although females of the butterfly Leptophobia aripa do not digest the spermatophore, they possess a prominent signum. Since, in general, the function of the signum is considered to be the piercing or tearing of the spermatophore to initiate its digestion, its presence in L. aripa poses a conundrum. We undertook a microscopic study of the different components of the bursa copulatrix (ductus bursae and corpus bursae) and found structural differences that we interpreted in functional terms. We provide a detailed description of the signum and present experimental data regarding its effect on the spermatophore. Our observations led us to propose a novel hypothesis regarding the function of the signum.

Male rats exhibit higher prefrontal-parietal EEG synchronization during the sexually-motivated state

Sexual motivation (SM) is a physiological state generated by the adequate processing of sexually-relevant stimuli. Induction and maintenance of this state requires the coordinated functioning of various cortical and subcortical areas. The medial prefrontal (mPFC, the prelimbic area in rats) and posterior parietal cortices (pPC) form an attentional network involved in processing incentive stimuli. Given that the sexual incentive stimuli emitted by a receptive female are highly relevant for the male rat, it is probable that these cortices interact functionally in processing the sexual stimuli that produce SM. Thus, the objective of this study was to characterize the cortical activation and degree of electroencephalographic coupling (coherence, hEEG) between the mPFC and pPC during a sexually-motivated state in male rats. Only rats that reached this state after 1 intromission prior to EEG recording, presented a higher frequency and duration of nose pokes, and showed higher prefronto-parietal activation and EEG synchronization while close to an inaccessible receptive female. Results show that both cortices are activated and that they are functionally coupled during the processing of sexually-relevant stimuli mainly in the right hemisphere, a key condition for inducing SM. We conclude that the attentional network made up of the prefrontal and parietal cortices participates in the adequate attention to, and processing of, sexual incentive stimuli and, hence, in inducing SM in male rats.

Why bonobos show a high reproductive skew towards high-ranking males: analyses for association and mating patterns concerning female sexual states.

Among non-human primates, male dominance rank is not necessarily a good indicator of mating success, and relationships between male dominance rank and mating or reproductive success are affected by female behavior and sexual states implying their probability of conception. Although comparisons of the behavior of male chimpanzees (Pan troglodytes) and bonobos (Pan paniscus) suggest that the effect of male dominance rank on mating success is expected to be less prominent in bonobos, recent genetic studies have shown that high-ranking male reproductive skew is higher in bonobos than in chimpanzees. One possible reason for the higher reproductive skew in bonobos could be that female behavior and their sexual states may have much more influence on male mating and reproductive success in bonobos than in chimpanzees. In the current study on bonobos, we conducted focal animal observation of females and analyzed the influence of female sexual swelling, the number of days after parturition, and dominance rank of males on female associations, and copulation with adult males. Our results showed that females with maximum swelling (MS) had more proximity with high-ranking males and copulated more frequently with higher-ranking males than with lower-ranking males. Females for whom longer time had elapsed since parturition, and therefore had higher probabilities of conception, had 5-m proximity with adult males more frequently than females whom shorter time had elapsed since parturition, but did not have more copulation with adult males. Females with MS had proximity and copulated with high-ranking males frequently, which partly explains why the reproductive skew is so high in bonobos. These results are discussed in relation to previous hypotheses on the influence of long-lasting mother-son relationships on mating success of males and on the contribution of female receptivity during non-conceptive nursing periods to moderate intermale aggression in bonobos.

Evidence of male alliance formation in a small dolphin community

The photo-identification of uniquely marked individuals has revealed much about mammalian behaviour and social structure in recent decades. In bottlenose dolphins (Tursiops spp.), for example, the long-term tracking of individuals has unveiled considerable variation in social structure among populations and various spatio-temporal aspects of group formation. In this study, we investigated associations among individual males in a small community of Indo-Pacific bottlenose dolphins (T. aduncus) residing in an urbanized estuary in southwestern Australia. Given the relative proximity of our study area to other populations in which complex male alliances form for the purpose of mate acquisition, we used long-term photo-identification records and social analyses to assess whether such alliances also occur in smaller and more isolated settings. Our work revealed strong social bonds and long-term, non-random associations among individual males, suggesting the occurrence of male alliances. Behavioural observations of alliances interacting with potentially receptive adult females from the estuary community and from adjacent communities, and exhibiting sexual display behaviours near females, suggest that these alliances occur in a reproductive context. As the first formal analysis indicating the occurrence of male alliances outside Shark Bay along the vast western coastline of Australia, this study complements previous research and extends our understanding of the evolutionary and ecological processes that drive alliance formation.

A male steroid controls female sexual behaviour in the malaria mosquito

Insects, unlike vertebrates, are widely believed to lack male-biased sex steroid hormones1. In the malaria mosquito Anopheles gambiae, the ecdysteroid 20-hydroxyecdysone (20E) appears to have evolved to both control egg development when synthesized by females2 and to induce mating refractoriness when sexually transferred by males3. Because egg development and mating are essential reproductive traits, understanding how Anopheles females integrate these hormonal signals can spur the design of new malaria control programs. Here we reveal that these reproductive functions are regulated by distinct sex steroids through a sophisticated network of ecdysteroid-activating/inactivating enzymes. We identify a male-specific oxidized ecdysteroid, 3-dehydro-20E (3D20E), which safeguards paternity by turning off female sexual receptivity following its sexual transfer and activation by dephosphorylation. Notably, 3D20E transfer also induces expression of a reproductive gene that preserves egg development during Plasmodium infection, ensuring fitness of infected females. Female-derived 20E does not trigger sexual refractoriness but instead licenses oviposition in mated individuals once a 20E-inhibiting kinase is repressed. Identifying this male-specific insect steroid hormone and its roles in regulating female sexual receptivity, fertility and interactions with Plasmodium parasites suggests the possibility for reducing the reproductive success of malaria-transmitting mosquitoes.

Not just females: the socio-ecology of social interactions between spider monkey males.

Male-male relationships are mostly characterized by competition. However, males also cooperate with one another if socio-ecological conditions are suitable. Due to their male philopatry, the need for cooperation in home range defence and high degree of fission-fusion dynamics, spider monkeys provide an opportunity to investigate how male-male interactions are associated with socio-ecological factors, such as the presence of potentially receptive females, the degree of food availability and the likelihood of home range defence. We tested predictions about changes in social interactions between wild spider monkey males in relation to these factors. First, males did not change their interaction patterns when potentially receptive females were in the subgroup compared to when they were absent. Second, males tended to be less tolerant of one another when feeding, but spent more time grooming, in contact and proximity with one another when food availability was lower than when it was higher. Third, males exchanged fewer embraces, spent less time grooming, in proximity and in contact with one another, and spent more time vigilant at the home range boundary area than at other locations. Our findings contribute to the understanding of social flexibility and the importance of considering males in socio-ecological models of any group-living species.

Serotonin Signaling Modulates Sexual Receptivity of Virgin Female Drosophila

The choice of females to accept or reject male courtship is a critical decision for animal reproduction. Serotonin (5-hydroxytryptamine; 5-HT) has been found to regulate sexual behavior in many species, but it is unclear how 5-HT and its receptors function to regulate different aspects of sexual behavior. Here we used Drosophila melanogaster as the model animal to investigate how 5-HT and its receptors modulate female sexual receptivity. We found that knockout of tryptophan hydroxylase (Trh), which is involved in the biosynthesis of 5-HT, severely reduced virgin female receptivity without affecting post-mating behaviors. We identified a subset of sexually dimorphic Trh neurons that co-expressed fruitless (fru), in which the activity was correlated with sexual receptivity in females. We also found that 5-HT1A and 5-HT7 receptors regulate virgin female receptivity. Our findings demonstrate how 5-HT functions in sexually dimorphic neurons to promote virgin female receptivity through two of its receptors.

Sexual coercion in a natural mandrill population

Increasing evidence indicates that sexual coercion is widespread. While some coercive strategies are conspicuous, such as forced copulation or sexual harassment, less is known about the ecology and evolution of intimidation, where repeated male aggression promotes future rather than immediate mating success with targeted females. Although known in humans, intimidation was recently reported in chimpanzees (Pan troglodytes) and chacma baboons (Papio ursinus), where males are regularly violent against females. Here, we investigate the nature of male coercive strategies in wild mandrills (Mandrillus sphinx), a primate living in large polygynandrous groups where severe male aggression towards females is rare and females can form coalitions against males. Yet, we found support for all three predictions of the sexual coercion hypothesis, namely that male aggression (1) specifically targets sexually receptive females, (2) inflicts costs to these females, and (3) increases male mating success in the long-term. These results hold true when considering only non-physical threats, or only severe aggression. Finally, we show that high-ranking females are most targeted by males, probably because of their higher reproductive performances, while high-ranking males are most coercive. These results indicate that sexual intimidation is widespread in sexually dimorphic and group-living mammals, and that males and females vary in their propensities to use, and to be exposed to sexual coercion, respectively.

Functional Dissection of Protein Kinases in Sexual Development and Female Receptivity of Drosophila.

Protein phosphorylation is crucial for a variety of biological functions, but how it is involved in sexual development and behavior is rarely known. In this study, we performed a screen of RNA interference targeting 177 protein kinases in Drosophila and identified 13 kinases involved in sexual development in one or both sexes. We further identified that PKA and CASK promote female sexual behavior while not affecting female differentiation. Knocking down PKA or CASK in about five pairs of pC1 neurons in the central brain affects the fine projection but not cell number of these pC1 neurons and reduces virgin female receptivity. We also found that PKA and CASK signaling is required acutely during adulthood to promote female sexual behavior. These results reveal candidate kinases required for sexual development and behaviors and provide insights into how kinases would regulate neuronal development and physiology to fine tune the robustness of sexual behaviors.

Mating system in a small pelagic spawner: field case study of the mandarinfish, Synchiropus splendidus

Mating systems in fishes are extremely diverse, ranging from monogamy to multiple polygamous forms, some of which include alternative male mating tactics within species. The major reproductive mode across approximately 33,000 bony fishes is pelagic-spawning with external fertilization. Despite the dominance of this mode, it is relatively little studied in the field because the greater mobility of larger species typically makes individuals difficult to follow for extensive periods, or to catch and mark. However, smaller, more sedentary pelagic spawners provide excellent opportunities to examine mating system variability in response to environmental conditions. The mandarinfish, Synchiropus splendidus, is a small sedentary pelagic spawner which is accessible to divers. Its complex body markings are distinctive and variable allowing individuals to be identified and followed repeatedly without the need for capturing and marking fish. In over 400 h of underwater surveys, we recorded movements, inter- and intra-sexual behaviors, sex ratios, and the timing and duration of spawning activity of focal fish in predetermined study areas. We concluded that the mandarinfish has a polygamous mating system with pair-spawning. Females are sequentially polyandrous, spawning once nightly or not at all, while males are polygynous, spawning up to 8 times a night. Males and females use loosely defined spawning sites on a daily basis and show flexibility in their tactics through differential movements according to dispersion of individuals, distances between spawning sites and temporally limited daily female receptivity. These results reveal the mandarinfish to be an excellent model species for studying small pelagic spawners in the field.

Effect of vibrational mating disruption on flight activity and oviposition to control the grapevine pest, Scaphoideustitanus

The increasing demand for safe and sustainably produced food is leading to the development of strategies of pest control alternative to chemicals. One innovative method is Vibrational Mating Disruption (VMD) to disrupt insect communication in plants. VMD was proven effective in preventing mating of the grapevine pest Scaphoideus titanus, vector of flavescence dorée. However, the stress induced by VMD on the target species has the potential to influence other crucial aspects of the insect biology and ethology. Therefore, the goal of this study was to understand side effects of VMD on the flight activity and oviposition of S. titanus. The results of our experiments conducted in the greenhouse showed that in the presence of a receptive female, males fly more if exposed to vibrations than in the silent control but not differently from singles males in silence. Surprisingly, we found that also females subjected to VMD fly more than in the silence. Regarding oviposition, we found that mated females exposed to vibrations and single females (unmated) laid significantly fewer eggs than mated females in silence. In conclusion, this study shows the potential of VMD to interfere, besides with mating, with other important biological aspects of the pest species.

A Protocol for the Non-invasive Method of Ultrasound Separation During the Sociosexual Vocal-Non-contact Model in Rats.

Ultrasonic vocalization (USV) is one of the measurable behavioral parameters of sociosexual interactions in rats. To precisely and accurately describe the neurobehavioral properties of USV and the potentially related specific emotional responsiveness of animals, we need to know which animals vocalize and what is their exact behavioral and physiological response. To this end, we modified the non-contact cage [non-contact erection model (NCE)] by adding a modification [vocalization-non-contact erection (VOC-NCE)] that makes it possible to assign emitted ultrasonic signals to a particular animal. Typically, the NCE cage consists of two compartments separated by perforated baffles. A male is placed in one section, and a receptive female is placed in the other section. This makes possible the accurate description of sexual parameters related to the cues controlled by the experimenter. In VOC-NCE, we completely separated the male USV from the female USV by three appropriately perforated baffles and located microphones combined with ultrasonic screening. We recorded emission in both typical bands, the so-called 22- and 50-kHz bands, with various subtypes, thus highlighting the utility of our protocol to investigate the sexual dimorphism of vocalization. Similar to the anticipatory model, we showed that emission can occur without acoustic feedback from concomitants during the VOC-NCE test. Therefore, we propose a relatively simple method for assigning individual vocalization. We discuss its usefulness and limitations in assessing vocal differentiation related to sexual parameters, adaptive changes during conditioning procedures, and further applications.

Modelling sexual violence in male rats: the sexual aggression test (SxAT)

Sexual assault and rape are crimes that impact victims worldwide. Although the psychosocial and eco-evolutionary factors associated with this antisocial behavior have repeatedly been studied, the underlying neurobiological mechanisms are still largely unknown. Here, we established a novel paradigm to provoke and subsequently assess sexual aggression (SxA) in adult male Wistar rats: the sexual aggression test (SxAT). Briefly, male Wistar rats are sexually aroused by a receptive female, which is exchanged by a non-receptive female immediately after the first intromission. This protocol elicits forced mounting and aggressive behavior toward the non-receptive female to different degrees, which can be scored. In a series of experiments we have shown that SxA behavior is a relatively stable trait in rats and correlates positively with sexual motivation. Rats with innate abnormal anxiety and aggressive behavior also show abnormal SxA behavior. In addition, central infusion of oxytocin moderately inhibits aggressive behavior, but increases forced mounting. Finally, we identified the agranular insular cortex to be specifically activated by SxA, however, inhibition of this region did not significantly alter behavior in the SxAT. Altogether, the SxAT is a paradigm that can be readily implemented in behavioral laboratories as a valuable tool to find answers regarding the biological mechanisms underlying SxA in humans, as well as social decision-making in general.

Drosulfakinin signaling modulates female sexual receptivity in Drosophila

Female sexual behavior as an innate behavior is of prominent biological importance for survival and reproduction. However, molecular and circuit mechanisms underlying female sexual behavior is not well understood. Here, we identify the Cholecystokinin-like peptide Drosulfakinin (DSK) to promote female sexual behavior in Drosophila. Loss of DSK function reduces female receptivity while overexpressing DSK enhances female receptivity. We identify two pairs of Dsk-expressing neurons in the central brain to promote female receptivity. We find that the DSK peptide acts through one of its receptors, CCKLR-17D3, to modulate female receptivity. Manipulation of CCKLR-17D3 and its expressing neurons alters female receptivity. We further reveal that the two pairs of Dsk-expressing neurons receive input signal from pC1 neurons that integrate sex-related cues and mating status. These results demonstrate how a neuropeptide pathway interacts with a central neural node in the female sex circuitry to modulate sexual receptivity.

Long duration advertisement calls of nesting male plainfin midshipman fish are honest indicators of size and condition.

The plainfin midshipman fish (Porichthys notatus) has long served as a model organism for neuroethology research on acoustic communication and related social behaviors. Type I or 'singing' males produce highly stereotyped, periodic advertisement calls that are the longest known uninterrupted vertebrate vocalizations. Despite the extensive literature on the acoustic behaviour of this species, it remains unclear whether reproductive males signal their quality via their highly energetic, multiharmonic advertisement calls. Here, we recorded the advertisement calls of 22 reproductive type I males at night in a controlled laboratory setting in which males were housed in aquaria maintained at a constant temperature (13.9±0.3°C). The duration of the advertisement calls from type I males was observed to increase from the first call of the night to the middle call after which call duration remained steady until the early morning hours and first light. A strong positive correlation was observed between loudness (sound pressure level and maximum sound pressure level) of the advertisement call and body size (mass and standard length; rs>0.8). In addition, an asymptotic relationship was observed between the harmonic frequencies (f0-f10) of the advertisement calls and male body condition, with harmonic frequencies initially increasing with body condition indices, but then plateauing when body condition measures were high. Taken together, our results suggest that type I male advertisement calls provide reliable honest information about male quality regarding size and body condition. Such condition-dependent information of calling males could potentially be used by receptive females to help facilitate mate choice decisions.