Female behavior changes profoundly after mating. In Drosophila, the mechanisms underlying the long-term changes led by seminal products have been extensively studied. However, the effect of the ...sensory component of copulation on the female’s internal state and behavior remains elusive. We pursued this question by dissociating the effect of coital sensory inputs from those of male ejaculate. We found that the sensory inputs of copulation cause a reduction of post-coital receptivity in females, referred to as the “copulation effect.” We identified three layers of a neural circuit underlying this phenomenon. Abdominal neurons expressing the mechanosensory channel Piezo convey the signal of copulation to female-specific ascending neurons, LSANs, in the ventral nerve cord. LSANs relay this information to neurons expressing myoinhibitory peptides in the brain. We hereby provide a neural mechanism by which the experience of copulation facilitates females encoding their mating status, thus adjusting behavior to optimize reproduction.
•Mating non-ejaculatory males induce a copulation effect reducing female receptivity•Activity of LSAN neurons is necessary and sufficient for copulation effect•Neurons expressing mechanosensory channel Piezo relay copulation effect to LSANs•Neurons expressing MIP mediate copulation effect downstream of LSANs
Female fruit flies are less receptive after mating because of ejaculate from previous mating partners and the act of copulation itself. Shao et al. characterize a neural circuit mediating the sensory signals of copulation that lead to reduced female receptivity.
The developing mammalian brain is destined for a female phenotype unless exposed to gonadal hormones during a perinatal sensitive period. It has been assumed that the undifferentiated brain is ...masculinized by direct induction of transcription by ligand-activated nuclear steroid receptors. We found that a primary effect of gonadal steroids in the highly sexually dimorphic preoptic area (POA) is to reduce activity of DNA methyltransferase (Dnmt) enzymes, thereby decreasing DNA methylation and releasing masculinizing genes from epigenetic repression. Pharmacological inhibition of Dnmts mimicked gonadal steroids, resulting in masculinized neuronal markers and male sexual behavior in female rats. Conditional knockout of the de novo Dnmt isoform, Dnmt3a, also masculinized sexual behavior in female mice. RNA sequencing revealed gene and isoform variants modulated by methylation that may underlie the divergent reproductive behaviors of males versus females. Our data show that brain feminization is maintained by the active suppression of masculinization via DNA methylation.
Mating and egg laying are tightly cooordinated events in the reproductive life of all oviparous females. Oviposition is typically rare in virgin females but is initiated after copulation. Here we ...identify the neural circuitry that links egg laying to mating status in Drosophila melanogaster. Activation of female-specific oviposition descending neurons (oviDNs) is necessary and sufficient for egg laying, and is equally potent in virgin and mated females. After mating, sex peptide-a protein from the male seminal fluid-triggers many behavioural and physiological changes in the female, including the onset of egg laying
. Sex peptide is detected by sensory neurons in the uterus
, and silences these neurons and their postsynaptic ascending neurons in the abdominal ganglion
. We show that these abdominal ganglion neurons directly activate the female-specific pC1 neurons. GABAergic (γ-aminobutyric-acid-releasing) oviposition inhibitory neurons (oviINs) mediate feed-forward inhibition from pC1 neurons to both oviDNs and their major excitatory input, the oviposition excitatory neurons (oviENs). By attenuating the abdominal ganglion inputs to pC1 neurons and oviINs, sex peptide disinhibits oviDNs to enable egg laying after mating. This circuitry thus coordinates the two key events in female reproduction: mating and egg laying.
In species that copulate during non-conceptive periods, such as humans and bonobos, sexual intercourse is known to be pleasurable for females. Dolphins also copulate throughout the year, largely to ...establish and maintain social bonds1. In dolphins, the clitoris is positioned in the anterior aspect of the vaginal entrance2, where physical contact and stimulation during copulation is likely. Clitoral stimulation seems to be important during female–female sexual interactions in common bottlenose dolphins (Tursiops truncatus), which rub each other’s clitorises using snouts, flippers, or flukes3. Determining a sexual pleasure response in animals not amenable to neurobehavioral examination is difficult, but investigation of the clitoris may elucidate evidence of functionality. In this study, we assessed macro- and micromorphological features of the clitoris in common bottlenose dolphins to examine functional features, including erectile bodies with lacunae, extensible collagen and/or elastin fibers, and the presence and location of sensory nerves. Our observations suggest the clitoris of dolphins has well-developed erectile spaces, is highly sensitive to tactile stimulation, and is likely functional.
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Brennan et al. describe morphological features of the bottlenose dolphin clitoris, such as abundant innervation and functional erectile spaces. These findings suggest that the clitoris functions in providing pleasure during sexual interactions, which are common in this species, and can help to understand the evolutionary significance of sexual pleasure.
•Anasa tristis copulate for highly variable durations and up to 23.1 h.•Female fecundity, fertility, and longevity are not affected by prolonged copulation duration.•Sperm transfer occurs within the ...first 30 min of copulation.•Females can store viable sperm for up to 4 weeks after a single copulation.
Within promiscuous mating systems, copulation often functions as more than a means of fertilization, and copulation durations can vary widely. Copulating for prolonged durations can enhance both female and male reproductive success, but can also result in costs: females of some insect species experience increased fecundity and fertility through male-provided nutrition during prolonged copulations, but also decreased longevity due to male-driven mechanisms. Here, for a common, promiscuous insect species (the squash bug, Anasa tristis), we first describe the range of copulation duration, which spans from 2 min to over 23 h. To investigate whether female A. tristis benefit from prolonged copulation, we next manipulated copulation duration and female diet, and we documented the resulting fecundity, fertility, and longevity of each female. We found no evidence that prolonged copulation durations affect female reproductive success. Females produced fertile eggs after a single 30 min copulation, and they subsequently produced fertile eggs for an additional 4 weeks. Our findings suggest that females do not benefit from prolonged copulations, that sperm transfer occurs very early during copulations, and that females can store sperm for long durations. Consequently, we suggest that female harassment avoidance and male mate-guarding may explain prolonged copulations in this species.
Mating with close kin can have considerable negative fitness consequences, which are expected to result in selective pressure for inbreeding avoidance mechanisms, such as dispersal, mate choice and ...post-copulatory biases. Captive studies have suggested that inbreeding avoidance through mate choice is far less widespread than expected and may be absent where other mechanisms already limit inbreeding. However, few studies have examined multiple mechanisms of inbreeding avoidance simultaneously, particularly in the wild. We use 13 years of detailed dispersal, copulation and paternity data from mountain gorillas to examine inbreeding avoidance. We find that partial dispersal of both sexes results in high kinship in multimale groups, but that copulations between close kin occur 40% less than expected. We find strong kin discrimination in mate choice, with significant avoidance of maternal kin but more limited avoidance of paternal kin. We find no evidence for post-copulatory inbreeding avoidance. Our analyses support familiarity-based mechanisms of kin identification and age-based avoidance that limits mating between fathers and daughters in their natal group. Our findings demonstrate that multiple complementary mechanisms for inbreeding avoidance can evolve in a single species and suggest that inbreeding avoidance through mate choice may enable more flexible dispersal systems to evolve.
Increased turbidity due to Palm Oil Mill Effluent (POME) contamination has been reported in several water bodies. However, the impact of POME-derived turbidity on the reproductive behaviour of fish ...is still unexplored. Hence, this study was aimed to investigate the alteration in reproductive behavior of siamese fighting fish (Betta splendens) after exposure to different levels of turbidity derived from POME. In total, 12 sexually mature pairs of siamese fighting fish were exposed to the different levels of turbidity, namely <1 NTU (control), 20 NTU (Treatment A), 40 NTU (Treatment B), and 60 NTU (Treatment C) with three replicates. Reproductive performance (total released egg, relative weight of released eggs, and nest area) and behaviour parameters (fin spreads, tail beats, chasing, leads, circling, and copulation) were measured. Results showed that an increase in turbidity (>40 NTU) due to POME contamination significantly decreased total released egg but did not have significant impact on relative weight of released eggs and nest area. Decreased total released eggs was occurred due to several alterations in the reproductive behaviour of siamese fighting fish during both the premating and mating stages. Duration of premating and mating stage was significantly decreased at turbidity level of 60 NTU. During premating stage, the number and average time of fin spreads behaviour at turbidity level of 60 NTU were significantly increased. In addition to, the number of chasing behaviour was significantly decreased with increasing turbidity levels. Furthermore, several alterations in reproductive behavior was also observed in mating stage, including increasing number and average time of lead, copulation interval, number of tail beat, average time of lead, and average time of circlings, followed by decreasing number of leads and number of circlings. In addition to, number of copulation and eggs per copulation showed an increasing and decreasing pattern at turbidity level of 40 and 60 NTU, respectively. The study suggests that reproductive behavior of fish might consider as alternative approach to support POME remediation management, mainly for turbidity parameters.
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•Total released eggs of fish significantly decreased at turbidity level of ≥40 NTU.•No significant effect on the relative weight of released egg and nest area.•Behaviour alteration was recorded during premating and mating stage at turbidity levels of ≥40 NTU.