Female Copulation Research Articles

The function of juvenile-adult transition axis in female sexual receptivity of Drosophila melanogaster.

Female sexual receptivity is essential for reproduction of a species. Neuropeptides play the main role in regulating female receptivity. However, whether neuropeptides regulate female sexual receptivity during the neurodevelopment is unknown. Here, we found the peptide hormone prothoracicotropic hormone (PTTH), which belongs to the insect PG (prothoracic gland) axis, negatively regulated virgin female receptivity through ecdysone during neurodevelopment in Drosophila melanogaster. We identified PTTH neurons as doublesex-positive neurons, they regulated virgin female receptivity before the metamorphosis during the third-instar larval stage. PTTH deletion resulted in the increased EcR-A expression in the whole newly formed prepupae. Furthermore, the ecdysone receptor EcR-A in pC1 neurons positively regulated virgin female receptivity during metamorphosis. The decreased EcR-A in pC1 neurons induced abnormal morphological development of pC1 neurons without changing neural activity. Among all subtypes of pC1 neurons, the function of EcR-A in pC1b neurons was necessary for virgin female copulation rate. These suggested that the changes of synaptic connections between pC1b and other neurons decreased female copulation rate. Moreover, female receptivity significantly decreased when the expression of PTTH receptor Torso was reduced in pC1 neurons. This suggested that PTTH not only regulates female receptivity through ecdysone but also through affecting female receptivity associated neurons directly. The PG axis has similar functional strategy as the hypothalamic-pituitary-gonadal axis in mammals to trigger the juvenile-adult transition. Our work suggests a general mechanism underlying which the neurodevelopment during maturation regulates female sexual receptivity.

Metabolic pathways that mediate the effects of food deprivation on reproductive behavior in female Drosophila melanogaster.

In most species studied, energy deficits inhibit female reproductive behavior, but the location and nature of energy sensors and how they affect behavior are unknown. Progress has been facilitated by using Drosophila melanogaster, a species in which reproduction and food availability are closely linked. Adult males and females were either fed or food deprived (FD) and then tested in an arena with a fed, opposite-sex conspecific with no food in the testing arena. Only FD females (not FD males) significantly decreased their copulation rate and increased their copulation latency, and the effects of FD were prevented in females fed either yeast alone or glucose alone, but not sucralose alone, cholesterol alone, or amino acids alone. It is well-known that high-fat diets inhibit copulation rate in this species, and the effects of FD on copulation rate were mimicked by treatment with an inhibitor of glucose but not free fatty acid oxidation. The availability of oxidizable glucose was a necessary condition for copulation rate in females fed either yeast alone or fed a nutritive fly medium, which suggests that the critical component of yeast for female copulation rate is oxidizable glucose. Thus, female copulation rate in D. melanogaster is sensitive to the availability of oxidizable metabolic fuels, particularly the availability of oxidizable glucose or substrates/byproducts of glycolysis.NEW & NOTEWORTHY Copulation rate was decreased in food-deprived female but not in male adults when tested without food in the testing arena. Copulation rate was 1) maintained by feeding glucose alone, yeast alone, nutritive medium lacking yeast, but not sucralose, amino acids, or cholesterol alone; 2) decreased by inhibition of glycolysis in females fed either nutritive medium or yeast alone; and 3) not affected by inhibition of fatty acid oxidation. Thus, female copulation rate was linked to glycolytic status.

Latitudinal cline in reproductive traits in the red flour beetle Tribolium castaneum

Several previous studies have reported geographic variation and/or latitudinal clines of morphological sexual characteristics, but there are few studies that consider reproductive traits that are not morphological. Here, we measured the proportion of females fertilized by males, frequency of reproductive failure in males, and number of female copulations of the red flour beetle Tribolium castaneum collected from fields in Japan to investigate the relationship between reproductive traits and latitude. Our results show substantial differences in the reproductive traits of both sexes among field populations. We identified latitudinal clines for reproductive traits in males, but not females. Moreover, female, but not male, reproductive traits were correlated with body size. Our study suggests that selection for male reproductive traits varies with latitude in T. castaneum.Significance statementIt has been established that latitudinal gradients are frequently observed in the traits of numerous animal species, of which body size is a prime example. Analogously, latitudinal gradients have been documented in the reproductive traits of several animal species, indicating that sexual selection may be influenced by latitude, although the specific understanding thereof remains elusive. In this study, we quantified the male and female reproductive traits and analyzed their relationship with latitude in the red flour beetle Tribolium castaneum. Our findings indicate that male mating efficacy was superior at lower than at higher latitudes, but no discernible latitudinal gradient was observed in female mating frequency. These results imply that selective pressure on males of this species is stronger at lower than at higher latitudes.

Out on a limb: female chameleons (Bradypodion pumilum) position themselves to minimise detection, whereas males maximise mating opportunity

ABSTRACT Although reproductive strategies are poorly documented in chameleons, sperm storage has been confirmed among some species for which male reproductive success may be maximised by increasing the number of females inseminated and/or preventing subsequent female copulation with rival males. Behaviour, such as mate searching, may enable males to maximise the number of mating opportunities with different partners and mate guarding may increase the likelihood that a male will sire offspring with a particular female. In this study, we investigated behavioural differences in movement (distance travelled) and perch choice between sexes of the Cape Dwarf Chameleon, Bradypodion pumilum, to offer data for a better understanding of mate searching and mate guarding behaviours. Wild chameleons were radio-tracked in 2010 (n = 8) and 2014 (n = 5) for approximately two weeks. The geographic location and perch height above ground were recorded multiple times per day to capture both the scale of movement and their perch use. Linear mixed effect models were used to assess differences between sexes. Our results indicated that females perched lower than males and moved shorter distances, offering support of a mate searching strategy in males. Ad hoc field observations revealed behaviours consistent with mate guarding by some males, and mate avoidance by some unreceptive females. Our results could indicate that males increase their reproductive fitness by using higher perches in both a mate guarding and mate searching context and moving further distances in search of receptive females.

Evolution of reproductive structures for in-flight mating in thynnine wasps (Hymenoptera: Thynnidae: Thynninae).

Thynnine wasps have an unusual mating system that involves concurrent in-flight copulation and nuptial feeding of wingless females by alate males. Consequently, thynnine genitalia play a multifunctional role and have likely been subject to various different selective pressures for both reproductive success and food provisioning. Here, we present a new molecular phylogeny for the Australian Thynninae and use 3D-geometric morphometrics and comparative methods to investigate the morphological evolution of select genital structures across the group. We found significant morphological integration between all male and female structures analysed, which is likely influenced by sexual selection, but also reproductive isolation requirements and mechanical constraints. The morphology of the primary male and female coupling structures was correlated with female body size, and female genitalia exhibited strong negative size allometry. Those male and female coupling structures have evolved at similar evolutionary rates, whereas female structures appear to have evolved a higher degree of morphological novelty over time. We conclude that the unique reproductive strategies of thynnine wasps have resulted in complex evolutionary patterns in their genital morphology, which has likely played a central role in the extensive diversification of the subfamily across Australasia and South America. Our study reinforces the need to treat composite characters such as genitalia by their component parts, and to consider the roles of both male and female reproductive structures in evolutionary studies.

Copulation Song in Drosophila: Do Females Sing to Change Male Ejaculate Allocation and Incite Postcopulatory Mate Choice?

Drosophila males sing a courtship song to achieve copulations with females. Females were recently found to sing a distinct song during copulation, which depends on male seminal fluid transfer and delays female remating. Here, it is hypothesized that female copulation song is a signal directed at the copulating male and changes ejaculate allocation. This may alter female remating and sperm usage, and thereby affect postcopulatory mate choice. Mechanisms of how female copulation song is elicited, how males respond to copulation song, and how remating is modulated, are considered. The potential adaptive value of female signaling during copulation is discussed with reference to vertebrate copulation calls and their proposed function in eliciting mate guarding. Female copulation song may be widespread within the Drosophila genus. This newly discovered behavior opens many interesting avenues for future research, including investigation of how sexually dimorphic neuronal circuits mediate communication between nervous system and reproductive organs.

Female copulation calls vary with male ejaculation in captive olive baboons

Abstract Copulation calls are mating-associated vocalizations that are common in primates, with females vocalizing after copulation in several Old World monkeys and apes. Baboon females typically produce copulation calls that correlate with fertile phase. Calls are, thus, regarded as an upshot of cycle physiology and sexually selected calls. Here, we describe three captive troops of olive baboons wherein, against expectation, females suppressed vocalizing during copulations. Vaginal cytology, together with sexual swelling observations, confirmed that females experienced full receptive cycles. Ovulation did not affect vocal probability during sex, while copulation calls were predicted by male ejaculation just as in other Old World primate species. Results cast doubt on the existence of physiological triggers for baboon copulation calls. Social factors may instead play a larger role. Alterations in social structure (as typically observed in the wild) may be implemented strategically as captive enrichment in order to reveal how females in highly social primates change sexual strategies and, therefore, the use of their copulation calls.

Female copulation song is modulated by seminal fluid

In most animal species, males and females communicate during sexual behavior to negotiate reproductive investments. Pre-copulatory courtship may settle if copulation takes place, but often information exchange and decision-making continue beyond that point. Here, we show that female Drosophila sing by wing vibration in copula. This copulation song is distinct from male courtship song and requires neurons expressing the female sex determination factor DoublesexF. Copulation song depends on transfer of seminal fluid components of the male accessory gland. Hearing female copulation song increases the reproductive success of a male when he is challenged by competition, suggesting that auditory cues from the female modulate male ejaculate allocation. Our findings reveal an unexpected fine-tuning of reproductive decisions during a multimodal copulatory dialog. The discovery of a female-specific acoustic behavior sheds new light on Drosophila mating, sexual dimorphisms of neuronal circuits and the impact of seminal fluid molecules on nervous system and behavior.

Mating behavior in Atheloca subrufella Hulst, 1887 (Lepidoptera: Pyralidae: Phycitinae)

O comportamento de acasalamento da mariposa Atheloca subrufella Hulst, 1887 (Lepidoptera: Pyralidae) foi investigado em arenas de laboratório. As descrições de corte e cópula em machos e fêmeas foram baseadas em observações diretas de casais virgens. Os resultados dos bioensaios de corte e cópula compreendem diversos padrões comportamentais tais como, antenação, busca pela fêmea (caminhando e/ou voando), encontro da fêmea, comportamento de chamamento da fêmea, exibição da glândula de feromônio, tentativa de cópula e cópula. Para isso, foram apresentados etogramas comportamentais de corte e cópula. Os resultados também sugerem que o comportamento de acasalamento em A. subrufella é mediado por um feromônio de longa distância e pela presença de um feromônio de curta distância. De maneira geral, esta pesquisa apresenta-se como estudo base para futuras investigações sobre o feromônio sexual de A. subrufella e desenvolvimento de novas estratégias de controle comportamental.

Copulation calls in wild Mueller’s gibbons (Hylobates muelleri)

AbstractMating activity of a wild Mueller’s gibbon group (Hylobates muelleri) was observed in the Danum Valley Conservation Area, Sabah, Malaysia. The purpose of this study was to investigate the function of copulation calls in gibbons. The female emitted copulation calls at the time of intromission and pelvic thrusting. Copulation calls were composed of two notes and one of them was sung only while mating. Approximately half of copulation calls were sung near the range boundary. Mating with copulation calls sometimes occurred while singing. According to the model that female copulation calls have evolved under the selective pressures of risk of infanticide and sperm competition, copulation calls should be rare in species with little female promiscuity. As gibbons usually live in pair-living social organization and have a monogamous mating system, no vocal signals by female gibbons are considered to be needed. However, clear copulation calls were emitted by the female. It suggests that the relationship between paired gibbons is unstable. Copulation calls by the female Mueller’s gibbon may function to increase mate guarding and strengthen the pair bond.

The evolution of male and female mating preferences in Drosophila speciation.

The relative importance of male and female mating preferences in causing sexual isolation between species remains a major unresolved question in speciation. Despite previous work showing that male courtship bias and/or female copulation bias for conspecifics occur in many taxa, the present study is one of the first large-scale works to study their relative divergence. To achieve this, we used data from the literature and present experiments across 66 Drosophila species pairs. Our results revealed that male and female mate preferences are both ubiquitous in Drosophila but evolved largely independently, suggesting different underlying evolutionary and genetic mechanisms. Moreover, their relative divergence strongly depends on the geographical relationship of species. Between allopatric species, male courtship and female copulation preferences diverged at very similar rates, evolving approximately linearly with time of divergence. In sharp contrast, between sympatric species pairs, female preferences diverged much more rapidly than male preferences and were the only drivers of enhanced sexual isolation in sympatry and Reproductive Character Displacement (RCD). Not only does this result suggest that females are primarily responsible for such processes as reinforcement, but it also implies that evolved female preferences may reduce selection for further divergence of male courtship preferences in sympatry.

Different levels of polyandry in two populations of the funnel-web wolf spider Aglaoctenus lagotis from South America

Populations of a species may show variation in mating systems, especially when the species is widely distributed. Aglaoctenus lagotis is a funnel-web wolf spider distributed in South America and with a ‘central Argentina form’ (CA) and a ‘southern Uruguay form’ (SU). Both forms differ in sexual behaviour, population density and copulatory season. This study evaluates the potential level of polyandry of both forms, sequentially exposing females to different males of their form under laboratory conditions. The number of copulations each female accepted and the characteristics of these sexual encounters were registered. CA females accepted more re-copulations than SU females and seemed to maintain more sexual attractiveness after the first copulation. In neither form was female re-copulation influenced by body characteristics, duration of the first copulation, ejaculation frequency or copulatory body shaking of females. Additionally, the PCA showed that both forms could be separated by their copulation behaviours. The higher level of polyandry in the CA form compared to the SU form suggested in our results adds another difference between these forms, currently under study to determine whether they are different species. This study is the first on mating systems in funnel-web wolf spiders, adding knowledge to the discussion about the evolution of sexual strategies in this group.

Antennae sense heat stress to inhibit mating and promote escaping in Drosophila females

Environmental stress is a major factor that affects courtship behavior and evolutionary fitness. Although mature virgin females of Drosophila melanogaster usually accept a courting male to mate, they may not mate under stressful conditions. Above the temperature optimal for mating (20–25 °C), copulation success of D. melanogaster declines with increasing temperature although we observed vigorous courtship attempts by males, and no copulation takes place at temperatures over 36 °C. We attempted to identify the sensory pathway for detecting heat threat that drives a female to escape rather than to engage in mating that detects hot temperature and suppresses courtship behavior. We found that the artificial activation of warmth-sensitive neurons (‘hot cells’) in the antennal arista of females completely abrogates female copulation success even at permissive temperatures below 32 °C. Moreover, mutational loss of the GR28b.d thermoreceptor protein caused females to copulate even at 36 °C. These results indicate that antennal hot cells provide the input channel for detecting the high ambient temperature in the control of virgin female mating under stressful conditions.

Effect of mating on survival at low temperature in females of the Japanese common grass yellow, Eurema mandarina

1. In some insects that overwinter as adults, mating occurs both before and after overwintering. Two hypotheses have been proposed to explain the adaptive significance of pre‐overwintering copulation of females. One is the bet‐hedging hypothesis, which explains pre‐overwintering copulation as a preparation for less chance of mating in the following spring. The other is the nuptial gift hypothesis, which states that secretions derived from males increase overwintering success of females.2. In Eurema mandarina, both diapause autumn‐ and non‐diapause summer‐form male adults emerge with autumn‐form female adults in the last generation in a year. Most autumn‐form females mate with summer‐form males before winter, and re‐mate with autumn‐form males in the following spring. Because autumn‐form females have sufficient chances for mating after overwintering, the nuptial gift hypothesis has been regarded as the more probable hypothesis.3. To test the nuptial gift hypothesis, the survival period was compared under short‐day conditions at 10 °C between mated and unmated females that had been reared on sucrose solution at 25 °C for 15–21 days. The mated females had significantly greater longevity than the unmated females, supporting the nuptial gift hypothesis. Body size also affected the survival period.4. The results suggest that the nuptial gift is an important factor for the evolution of pre‐overwintering copulation in species in which females mate both before and after overwintering.

Comparing functions of copulation calls in wild olive baboons, Papio anubis, using multimodel inference

Female copulation calls are species specific, distinct vocal signals sometimes given during or shortly after mating. Despite being common in primates and despite much empirical work, their function remains largely unclear for most species. Here, we used an information-theoretic approach to examine simultaneously three main competing hypotheses for the evolution of copulation calls. Two of the three hypotheses predict that female copulation calls function to incite competition between males, either directly (the male–male competition hypothesis) or indirectly (the sperm competition hypothesis), while the third predicts that females use calls to choose mating partners (the female choice hypothesis). We collected data on copulations of wild female olive baboons in Kibale National Park, Uganda, to compare the relative support for these hypotheses by modelling whether or not females produced copulation calls after mounts. Our analytical approach enabled us to objectively rank models corresponding to the three hypotheses according to how well our data fitted the models. Our data favoured the sperm competition hypothesis over the female choice hypothesis although much variation in calling remained unexplained. The male–male competition hypothesis seems unlikely given our data. We also discuss the possibility that copulation calls have no function, functions not included in our analysis, or that they are multifunctional, a reflection of the species' social evolution history. • Several hypotheses of female copulation calls exist with no clear consensus. • We used multimodel inference to test the main hypotheses in olive baboons. • We found strongest support for the sperm competition hypothesis. • We discuss alternative hypotheses and advantages of multimodel inference.

Mating success follows duet dancing in the Java sparrow.

Mutual interactions between sexes have multiple signalling functions. Duet singing in songbirds is related to mutual mate guarding, joint resource defence, and signalling commitment. Coordinated visual displays of mating pairs are thought to perform similar functions, but are less well understood. The current study evaluated mutual interactions in an Estrildid species to explore the relative importance of duet dancing and male singing in mating success of pairs in a first encounter. When Java sparrows (Lonchura oryzivora) court prospective mates, only males sing. However, both males and females perform courtship dances, often in a duet-like manner. These dances are typically terminated by female copulation solicitation displays (CSDs). In the current study, we observed higher mating success when courtship dances were mutually exchanged, and when males sang. However, the sex initiating the courtship did not affect mating success. Most females produced CSDs after duet dancing but before hearing the entire song, indicating that duet dancing played a crucial role in mating. This finding highlights an unexplored aspect of duetting behaviour in the process of mutual mate choice. These results conflict with the majority of past songbird research, which has interpreted songs as primary behavioural sexual signals.

Individual, social, and sexual niche traits affect copulation success in a polygynandrous mating system

In polygynandrous mating systems, the factors that mediate copulation success and the use of alternative mating tactics, such as mate guarding, are still poorly understood. In the rock hyrax (Procavia capensis), both sexes mate annually with multiple partners during a single month. In order to examine the factors that drive copulation success, we used 494 mating-related observations that were collected over a decade. In our analysis, we used the traits of individual hyraxes as well as the traits of members of their sexual niche, which we defined as their local competitors and potential mates. Using individual traits, we found that overall, female hyraxes rejected copulation attempts more frequently than males, supporting predictions from sexual selection theory. Females who had been mothers in previous years were mate-guarded more by resident males. When we considered the traits of competitors and potential mates in individuals’ sexual niche, we found that when resident males had higher-ranking competitors, their copulation success decreased, irrespective of their own traits. Bachelor male copulation success was not influenced by their competitor’s social status. Female copulation success was positively affected by maternal status and by social network position. Females that were central in the social network and those that had central female competitors had higher copulation success, supporting the benefits of social cohesion and the importance of the social niche. Thus, our results suggest that in polygynandrous mating systems, copulation success is determined not only by individual quality but also by the social and sexual niches that the individual occupies. Social networks describe with whom individuals consort. The complex patterns of sexual relationships in animal societies can also be expressed as networks of mating-related interactions. During our long-term study on the dynamic social relationships of wild rock hyraxes, we observed complex sexual interactions. Our results show that hyraxes choose mating partners from their available mate pool (or sexual niche) taking into account the traits of their actual mates, other potential mates, and those of their competitors. These findings suggest that the sexual niche, describing the subset of available mating partners, is important for mate choice, with significant implications to the study of sexual selection.

Exposure to the androgenic brominated flame retardant 1,2-dibromo-4-(1,2-dibromoethyl)-cyclohexane alters reproductive and aggressive behaviors in birds.

Detected in environmental samples, 1,2-dibromo-4-(1,2-dibromoethyl) cyclohexane (DBE-DBCH) is a bioaccumulative isomer of a current-use brominated flame retardant. All 4 structural isomers are androgen agonists; however, little toxicological information exists for this compound. The objective of the present study was to determine if β-DBE-DBCH, the isomer found most prominently in animal tissue, affects androgen-dependent behavior of breeding American kestrels (Falco sparverius). The authors hypothesized that if β-DBE-DBCH acts as an androgen agonist in kestrels, androgen-dependent behaviors (i.e., copulation, courtship, aggression) would increase and behaviors inhibited by androgens (i.e., parental care behaviors) would decrease. Sixteen captive experimental kestrel pairs were exposed to 0.239 ng β-DBE-DBCH/g kestrel/d by diet from 4 wk prior to pairing until their nestlings hatched (mean 82 d) and compared with vehicle only-exposed control pairs (n = 15). Androgen-dependent behaviors were significantly increased in β-DBE-DBCH-exposed birds, consistent with the authors' hypothesis. These behavioral changes included copulation and other sexual behaviors in males and females and aggression in males, suggesting that β-DBE-DBCH may have acted like an androgen agonist in these birds. Parental behaviors were not reduced in exposed birds as predicted, although dietary exposure had ceased before chicks hatched. Further assessment of β-DBE-DBCH is recommended given these behavioral changes and the previously reported reproductive changes in the same birds.

Volatiles from the burnet moth Zygaena filipendulae (Lepidoptera) and associated flowers, and their involvement in mating communication

AbstractThe burnet moth Zygaena filipendulae L. contains the cyanogenic glucosides linamarin and lotaustralin, which can be degraded to the volatiles hydrogen cyanide (HCN), acetone and 2‐butanone. Linamarin and lotaustralin are transferred from the male to female during mating and thus are considered to be involved in mating communication. Because volatile semiochemical cues play a major role in mating communication in many insect species, the emissions of HCN, acetone and 2‐butanone from Z. filipendulae are characterized in the present study, aiming to determine the interplay between the degradation products of cyanogenic glucosides and pheromones. The volatile emissions from Z. filipendulae and flowers inducing mating are measured using headspace solid‐phase micro‐extraction and gas chromatography‐mass spectrometry analysis. All Z. filipendulae life stages emit HCN, acetone and 2‐butanone. Virgin females show higher emissions than mated females, whereas mated males have higher emissions than virgin males. Hydrogen cyanide is only rarely detected in the course of male–female copulation. These observations indicate a role for the cyanogenic glucoside derived volatiles in female calling and male courtship behaviours, although not as a defence during copulation. Males rejected for mating by a female are accepted after injection of linamarin or lotaustralin, demonstrating that cyanogenic glucosides are also important for female assessment of the fitness of the male. Volatiles from flowers occupied during mate calling are also analyzed, and emissions from males and females result in the identification of novel putative pheromones for Z. filipendulae.

Taxonomic utility of female copulation organs in Sericini chafers (Coleoptera, Scarabaeidae), with special reference to asymmetry

Female genitalia are widely underrepresented in taxonomic studies. Here we investigate the morphological variation among female copulation organs for a group of scarab beetles (Sericini) with similar ecology, external morphology and copulation mechanics. We examined traits qualitatively and quantitatively based on 80 and 18 species (genus Pleophylla), respectively. Additionally we explored whether female genitalia are affected by asymmetry. The vast diversity of slerotised structures including their shapes illustrated the high taxonomic and phylogenetic utility of female genitalia in this group. The morphometric analysis of Pleophylla, confirmed that sclerotisations in the ductus bursae are very suitable for species-level taxonomic purposes. Stable interspecific variation is more hardly discernable in other parts such as the vaginal palps (shape and size) or the other membranous structures such as the shape of the bursa copulatrix. Asymmetric genitalia that arose multiple times independently among insects are found in most of the examined Sericini species. Asymmetries regarded either the bursa copulatrix, or both the bursa copulatrix and ductus bursae and comprised sclerotised and non-sclerotised structures being most common in modern Sericini. Here, highly asymmetric sclerotised structures are linked with strong asymmetry of the male copulation organs. Widespread asymmetry among megadiverse Sericini with a complex male-female genital asymmetry suggests that the shift to asymmetry is phylogenetically rather conserved. From the range of hypotheses, sexual selection seems to be the most reasonable to explain the evolution and stability of asymmetry in chafer genitalia.