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.
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.
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.
•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.
Repeated testing for masculine sexual behavior influences female sex preference in males. Males perinatally treated with aromatase inhibitors show male preference, but also copulate with the ...receptive female. Such copulation modifies sex preference most likely because of its rewarding properties. In this study, we intended to equal the incentive value of both stimuli -in the sex preference test- by using receptive females with vaginal occlusion. Vehicle and letrozole-treated (0.56 μg/kg, gestation days 10–21) males were repeatedly tested for sex preference at 40, 55, 70, 85 and 100 days of age. These ages were selected because males of 40 days are unable to copulate, while by 100 days of age almost all males show the complete repertoire of masculine sexual behavior. At 40 days of age, males of all groups fail to show sex preference and none of them was able to copulate. In controls of 100 days of age all males showed female-sex preference and all intromitted the female. A large proportion (44%) of vehicle-treated males that could not copulate the female showed male preference. Twenty to 30% of the prenatally letrozole treated males also had same-sex preference even if they could copulate; and most of them (67%) had a male preference when copulation was precluded. These data support the idea that copulation is crucial for developing a female preference in control animals. The results suggest that brain changes produced by estrogens along early development and stimuli coming from the partner are essential for shaping sex preference.
•Copulation is essential for establishing partner preference in rats.•20–30% of letrozole-treated males retain male preference even if they can copulate.•Estrogens during development and sexual experience shape partner preference in rats.
Connectomics research has made it more feasible to explore how neural circuits can generate multiple outputs. Female sexual drive provides a good model for understanding reversible, long-term ...functional changes in motivational circuits. After emerging, female flies avoid male courtship, but they become sexually receptive over 2 d. Mating causes females to reject further mating for several days. Here, we report that pC1 neurons, which process male courtship and regulate copulation behavior, exhibit increased CREB (cAMP response element binding protein) activity during sexual maturation and decreased CREB activity after mating. This increased CREB activity requires the neuropeptide Dh44 (Diuretic hormone 44) and its receptors. A subset of the pC1 neurons secretes Dh44, which stimulates CREB activity and increases expression of the TRP channel Pyrexia (Pyx) in more pC1 neurons. This, in turn, increases pC1 excitability and sexual drive. Mating suppresses
expression and pC1 excitability. Dh44 is orthologous to the conserved corticotrophin-releasing hormone family, suggesting similar roles in other species.
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