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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 1 . Sex peptide is detected by sensory neurons in the uterus 2 – 4 , and silences these neurons and their postsynaptic ascending neurons in the abdominal ganglion 5 . 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. Neuron-tracing and labelling experiments in Drosophila females reveal the neural circuitry that coordinates mating and egg laying, and the role of sex peptide from male seminal fluid in triggering these neurons.

Copulation is essential for transferring sperm from males to females in most animals. During copulation, males and females are often static and thus prone to predation or other threats. Its duration should therefore be reduced to minimize costs but sufficient to ensure the fertilization of eggs. Here, we investigated reproductive behavior and success in the false widow spider, Steatoda grossa (Araneae: Theridiidae), when copulation was interrupted after 1, 3, 5, 10, or 20 min or was not experimentally interrupted (control). Copulation duration in this study is defined as the total duration of insertions of male pedipalps into a female’s copulatory openings. In S. grossa , uninterrupted copulations typically last 40 to 60 min. We found that within the first 5 min, copulation interruption negatively affected reproductive success (i.e., number of egg sacs, their total mass, and number of spiderlings), and delayed production of the first egg sac within the first 10 min (in some extreme instances by over 200 days). However, when copulation duration was 10 min or longer, reproductive outcome was unaffected. In the 1-min treatment, the number of egg sacs and their mass varied greatly, which indicates considerable variation among males with respect to the speed and efficiency of sperm transfer. We discuss the costs and benefits of extended copulation duration on female reproduction and on male and female fitness. Significance statement Interrupted copulation had a significant negative effect on reproductive success in the false widow spider, Steatoda grossa , but only if mating was terminated within the first 10 min of copulation. This implies that early during the copulation sequence sufficient amounts of sperm are transferred to fertilize most of the female’s eggs. When copulation duration is less than 10 min, female spiders delayed the time to first reproduction. Prolonging the latency of reproduction can significantly affect female fitness. The role of extended mating in arthropods has focused on its effects on mate guarding, male-male competition for access to females and decreasing a female’s attractiveness to other males. Preliminary data suggest that extended copulation does not reduce receptivity of S. grossa females to other males. Prolonged mating in S. grossa may play a more important role in reproductive success of the males.

The diversity of genitalia has long intrigued evolutionary and functional morphology scientists, with a primary focus on male copulatory organs. Despite extensive studies on snake genitalia, particularly hemipenes, female copulatory organs remain understudied. This research aims to fill this gap by using a recently introduced methodology for preparation with a few adjustments, and by describing female snake genitalia for seven previously undescribed species. The methodology is based on employing a two-component condensation silicone into snakes’ genitalia to create internal models for intersexual comparative morphology. We conducted a comprehensive examination of seven Old World snake species - Boidae: Eryx jaculus, Colubridae: Dolichophis caspius, Zamenis longissimus, Elaphe quatuorlineata, Coronella austriaca, and Viperidae: Vipera ammodytes, and V. berus. Our results reveal conspicuous variations in female genitalia morphology, speculating that there is also a significant variation in copulation adjustment between the different types of species’ genitalia.

Intraspecific olfactory signals known as pheromones play important roles in insect mating systems. In the model Drosophila melanogaster , a key part of the pheromone-detecting system has remained enigmatic through many years of research in terms of both its behavioral significance and its activating ligands. Here we show that Or47b-and Or88a-expressing olfactory sensory neurons (OSNs) detect the fly-produced odorants methyl laurate (ML), methyl myristate, and methyl palmitate. Fruitless ( fru ᴹ)- positive Or47b-expressing OSNs detect ML exclusively, and Or47b- and Or47b-expressing OSNs are required for optimal male copulation behavior. In addition, activation of Or47b-expressing OSNs in the male is sufficient to provide a competitive mating advantage. We further find that the vigorous male courtship displayed toward oenocyte-less flies is attributed to an oenocyte-independent sustained production of the Or47b ligand, ML. In addition, we reveal that Or88a-expressing OSNs respond to all three compounds, and that these neurons are necessary and sufficient for attraction behavior in both males and females. Beyond the OSN level, information regarding the three fly odorants is transferred from the antennal lobe to higher brain centers in two dedicated neural lines. Finally, we find that both Or47b- and Or88a-based systems and their ligands are remarkably conserved over a number of drosophilid species. Taken together, our results close a significant gap in the understanding of the olfactory background to Drosophila mating and attraction behavior; while reproductive isolation barriers between species are created mainly by species-specific signals, the mating enhancing signal in several Drosophila species is conserved. Significance Mating interactions in Drosophila melanogaster depend on a number of sensory cues targeting different modalities like hearing, taste, and olfaction. From an olfactory perspective, only negative fly-derived signals had been identified, whereas a positive signal mediating mating was missing. Here we demonstrate the presence of such a signal (methyl laurate) and dissect the neural mechanism underlying its detection. We also show that the same odorant together with two additional fly-derived odorants (methyl myristate and methyl palmitate) mediate attraction via a pathway separated from that involved in courtship. Interestingly, the odorants identified are attractive to several closely related species. Thus, we describe two highly important neural circuits involved in mating and attraction that seem to be conserved in Drosophila.

Functional explanations for forced copulation, an extreme manifestation of intersexual conflict, remain underexplored. We investigated the adaptive significance of forced extra-pair copulation (FEPC) in European blackbirds. Our results contradict the prevailing hypothesis that the primary function of FEPC is fertilization. FEPC frequency peaked at the beginning of the breeding season and declined thereafter, despite the continued presence of fertile females. Furthermore, we found no evidence that males selectively target fertile females; within the reproductive cycle, females were equally susceptible to FEPC during the pre-fertile and fertile periods. We propose that sexual aggression in blackbirds reflects competition. As predicted, the incidence of FEPC was highest early in the season, and females attempting to settle between established pairs were at higher risk of becoming victims. Females were not passive in the conflict and could significantly reduce the risk of FEPC by shifting home ranges. We conclude that FEPC is an instrument of aggression rather than an expression of sexual interest. Neighboring males attempt to deter new competitors by targeting the weaker member of a pair. For females, FEPC is part of the landscape of fear.

Hormone-induced brain masculinization occurs during a perinatal sensitive period but endures into adulthood. Researchers explored DNA methylation as a candidate mechanism. Methylation is higher in female brain and suppresses masculinization genes, which are liberated by hormone-induced reductions in DNMT activity in males. Pharmacological inhibition of DNMTs reduces methylation, masculinizes female brain and behavior and reopens the sensitive period. 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.

Romantic engagement can bias sensory perception. This ‘love blindness’ reflects a common behavioural principle across organisms: favouring pursuit of a coveted reward over potential risks 1 . In the case of animal courtship, such sensory biases may support reproductive success but can also expose individuals to danger, such as predation 2 , 3 . However, how neural networks balance the trade-off between risk and reward is unknown. Here we discover a dopamine-governed filter mechanism in male Drosophila that reduces threat perception as courtship progresses. We show that during early courtship stages, threat-activated visual neurons inhibit central courtship nodes via specific serotonergic neurons. This serotonergic inhibition prompts flies to abort courtship when they see imminent danger. However, as flies advance in the courtship process, the dopaminergic filter system reduces visual threat responses, shifting the balance from survival to mating. By recording neural activity from males as they approach mating, we demonstrate that progress in courtship is registered as dopaminergic activity levels ramping up. This dopamine signalling inhibits the visual threat detection pathway via Dop2R receptors, allowing male flies to focus on courtship when they are close to copulation. Thus, dopamine signalling biases sensory perception based on perceived goal proximity, to prioritize between competing behaviours. A state-dependent dopamine filter system in the male Drosophila brain balances threat perception against the drive to mate.

[This corrects the article DOI: 10.1371/journal.pone.0193164.].

Extra-pair copulations (EPCs) are the poorly known antecedents of extra-pair fertilizations (EPFs) in birds. EPFs occur in most bird species that have been examined, but sexual conflict will generally reward females hiding their EPCs from males attempting to protect their paternity. EPCs will be difficult for researchers to document, and necessarily underestimated, in that case. We measured EPC behaviors and EPF frequency in a colonial seabird, the Nazca booby Sula granti , in which all copulations occur in a visually open setting with numerous possible copulatory partners readily available. Females are larger and more physically powerful than males, and are the numerically limiting sex, perhaps limiting options for males to control females. We found that all copulations were voluntary, and females’ sexual activities were wholly unconstrained by male coercion. Most females had multiple copulatory partners in the weeks preceding egg-laying. Despite the commonness of EPC, EPFs did not occur. The different schedules of EPC and within-pair copulation (WPC) provided a sufficient explanation for this outcome: during the ovulation window days before laying, WPC rate increased and EPC rate approached zero. To our knowledge, this is the first robust evidence of complete sexual agency in a female bird aside from lek-mating species, contributing a valuable exemplar to the literature on sexual conflict over reproduction.

The Southern Lapwing ( Vanellus chilensis ) is a widespread bird across Southern America and commonly found in any large open areas, including agriculture and urban. Despite being a conspicuous species, little is known about its copulatory behaviour. In this research, we studied the copulation behaviour of Southern Lapwings and identified specific behaviours that preceded copulation events. Focal observations were made during one year on two pairs of lapwings that inhabit an urban area in the southeastern Pampas region, Argentina. A total of 110 intra-pair copulations were recorded (pair 1 = 64 and pair 2 = 46). Frequent copulations began 97 and 64 days before the first egg-laying, respectively, although the highest frequency occurred before the onset of the first nesting attempt. The Southern Lapwing copulated during all daylight hours, with a peak in the morning. Copulation occurred for up to five consecutive days, and the maximum number of copulations observed in a single day was four. Courtship and territory defence were the most common behaviours preceding copulation. Among the multiple hypotheses that have been proposed to explain frequent intra-pair copulation, our results seem to support two of them: the territory signalling hypothesis and the social bond hypothesis. The high population density coupled with the low availability of territories and a strong social bond based on cooperation and coordination could support both hypotheses, respectively. Given that the social environment can modify the behaviour of plovers, future research should evaluate the copulation behaviour at different population densities and the adaptive functional significance of this behaviour.