•The medial amygdala (MeA) is involved in the regulation of ejaculation.•Both silencing and stimulation of the MeA delays ejaculation.•The MeA does not seem to be involved in the regulation of ...copulation patterns.•The MeA may be involved in processing sensory feedback required for ejaculation.•The MeA does not seem to be involved in sexual incentive motivation.
The medial amygdala (MeA) is a sexually dimorphic brain region that integrates sensory information and hormonal signaling, and is involved in the regulation of social behaviors. Lesion studies have shown a role for the MeA in copulation, most prominently in the promotion of ejaculation. The role of the MeA in sexual motivation, but also in temporal patterning of copulation, has not been extensively studied in rats. Here, we investigated the effect of chemogenetic inhibition and stimulation of the MeA on sexual incentive motivation and copulation in sexually experienced male rats. AAV5-CaMKIIa viral vectors coding for Gi, Gq, or no DREADDs (sham) were bilaterally infused into the MeA. Rats were assessed in the sexual incentive motivation test and copulation test upon systemic clozapine N-oxide (CNO) or vehicle administration. We report that MeA stimulation and inhibition did not affect sexual incentive motivation. Moreover, both stimulation and inhibition of the MeA decreased the number of ejaculations in a 30 min copulation test and increased ejaculation latency and the number of mounts and intromissions preceding ejaculation, while leaving the temporal pattern of copulation intact. These results indicate that the MeA may be involved in the processing of sensory feedback required to reach ejaculation threshold. The convergence of the behavioral effects of stimulating as well as inhibiting the MeA may reflect opposing behavioral control of specific neuronal populations within the MeA.
Peripheral sensory neurons are the gateway to the environment across species. In Drosophila, olfactory and gustatory senses are required to initiate courtship, as well as for the escalation of ...courtship patterns that lead to copulation. To be successful, copulation must last long enough to ensure the transfer of sperm and seminal fluid that ultimately leads to fertilization. The peripheral sensory information required to regulate copulation duration is unclear. Here, we employed genetic manipulations that allow driving gene expression in the male genitalia as a tool to uncover the role of these genitalia specific neurons in copulation. The fly genitalia contain sex-specific bristle hairs innervated by mechanosensory neurons. To date, the role of the sensory information collected by these peripheral neurons in male copulatory behavior is unknown. We confirmed that these MSNs are cholinergic and co-express both fru and dsx. We found that the sensory information received by the peripheral sensory neurons from the front legs (GRNs) and mechanosensory neurons (MSNs) at the male genitalia contribute to the regulation of copulation duration. Moreover, our results show that their function is required for copulation persistence, which ensures copulation is undisrupted in the presence of environmental stress before sperm transfer is complete.
Male mice with homozygous loss of function mutations of the transcription factor gene Pea3 (Pea3 null) are infertile due to their inability to inseminate females, however the specific deficits in ...male sexual behaviors that drive this phenotype are unknown. Here, the copulatory behavior of male mice (Pea3 null and control) with hormonally primed ovariectomized females was monitored via high-speed and high-resolution digital videography to assess for differences in female-directed social behaviors, gross sexual behaviors (mounting, thrusting), and erectile and ejaculatory function. Pea3 null male mice exhibit greatly reduced erectile function, with 44% of males displaying no visible erections during copulation, and 0% achieving sustained erections. As such, Pea3 null males are incapable of intromission and copulatory plug deposition, despite displaying largely normal female-directed social behaviors, mounting behaviors, and ejaculatory grasping behavior. Additionally, the organization and timing of thrusting behaviors is impaired in Pea3 null males. Our results show that the transcription factor gene Pea3 regulates the ability to achieve and maintain erections during copulation in mice.
The study of alternative reproductive tactics (the behavioural strategies used by individuals to increase their reproductive success) is an evolutionary puzzle, and one of great interest to ...researchers. For instance, why do some males guard both nest and eggs, while others sneak into nests while pairs are spawning and fertilise those eggs? The field offers a special opportunity to study the evolution and functional causes of phenotypic variation, which is a general problem in the field of evolutionary biology. By integrating both mechanistic (psychological) and evolutionary (behavioural ecology) perspectives and by covering a great diversity of species, Alternative Reproductive Tactics addresses this integrated topic of longstanding interest, bringing together a multitude of otherwise scattered information in an accessible form that is ideal for graduate students and researchers.
Mating plugs are produced by many sexually reproducing animals and are hypothesized to promote male fertilization success under promiscuous mating. However, tests of this hypothesis have been ...constrained by an inability to discriminate ejaculates of different males in direct competition. Here, we use stable isotope labeling in vivo and proteomics to achieve this in a promiscuous rodent, Myodes glareolus. We show that, although the first male’s plug is usually dislodged, it can be retained throughout the second male’s copulation. Retained plugs did not completely block rival sperm but did significantly limit their numbers. Differences in the number of each male’s sperm progressing through the female reproductive tract were also explained by natural variation in the size of mating plugs and reproductive accessory glands from which major plug proteins originate. Relative sperm numbers in turn predicted the relative fertilization success of rival males. Our application of stable isotopes to label ejaculates resolves a longstanding debate by revealing how rodent mating plugs promote fertilization success under competitive conditions. This approach opens new opportunities to reveal cryptic mechanisms of postcopulatory sexual selection among diverse animal taxa.
In many slowly developing mammal species, males reach sexual maturity well before they develop secondary sexual characteristics. Sexually mature male orangutans have exceptionally long periods of ...developmental arrest. The two male morphs have been associated with behavioral alternative reproductive tactics, but this interpretation is based on cross‐sectional analyses predominantly of Northwest Sumatran populations. Here we present the first longitudinal analyses of behavioral changes of 10 adult males that have been observed in both unflanged and flanged morph. We also analyzed long‐term behavioral data on an additional 143 individually identified males from two study sites, Suaq (Sumatra, Pongo abelii) and Tuanan (Borneo, Pongo pygmaeus wurmbii), to assess male mating tactics cross‐sectionally in relation to population, male morph (unflanged and flanged), and other socio‐ecological factors. Both our longitudinal and cross‐sectional results confirm and refine previous cross‐sectional accounts of the differences in mating tactics between the unflanged and the flanged male morphs. In the unflanged morph, males exhibit higher sociability, particularly with females, and higher rates of both copulation and sexual coercion than in the flanged morph. Based on our results and those of previous studies showing that females prefer flanged males, and that flanged males have higher reproductive success, we conclude that unflanged males face a trade‐off between avoiding male‐male contest competition and gaining mating access to females, and thus follow a “best‐of‐a‐bad‐job” mating strategy.
Illustration of behavioral changes by individual male Bornean and Sumatran orang‐utans from the unflanged to the flanged morph (right). Pictures taken by A. Marzec, Suwi, C. Schuppli, G. Duvot (top left to bottom right)
HIGHLIGHTS
Longitudinal data confirm alternative reproductive tactics (ARTs) in orangutans
Within‐male behavioral changes after transition reflect differences between morphs
ARTs were consistent between a Sumatran and a Bornean population
Sexual coercion is neither an individual male trait nor an unflanged male default
Post-copulatory sexual selection (PSS) is an important selective force that determines fitness in polyandrous species. PSS can be intense in some cases and can drive the evolution of remarkable ...ejaculate properties. In males, investment in ejaculate plays an important role in the outcome of PSS. Thus, males are expected to adaptively tailor their ejaculate according to the perceived competition in their vicinity. Plastic responses in ejaculate investment to variation in intrasexual competition are disparate and widespread in males. We investigated the evolution of plasticity in reproductive traits using Drosophila melanogaster populations evolving for more than 150 generations under male- or female-biased sex ratios. When exposed to different numbers of competitors early in their life, males from these two regimes responded differently in terms of their copulation duration and sperm competitive ability. In addition, the effect of this early life experience wore off at different rates in males of male-biased and female-biased regimes with increasing time from the removal of competitive cues. Furthermore, our study finds that males change their reproductive strategies depending upon the identity of rival males. Together, our results provide evidence of the evolution of male reproductive investment that depends on socio-sexual cues experienced early in life.
males perform a series of courtship behaviors that, when successful, result in copulation with a female. For over a century, mutations in the
gene, named for its effects on pigmentation, have been ...known to reduce male mating success. Prior work has suggested that
influences mating behavior through effects on wing extension, song, and/or courtship vigor. Here, we rule out these explanations, as well as effects on the nervous system more generally, and find instead that the effects of
on male mating success are mediated by its effects on pigmentation of male-specific leg structures called sex combs. Loss of
expression in these modified bristles reduces their melanization, which changes their structure and causes difficulty grasping females prior to copulation. These data illustrate why the mechanical properties of anatomy, not just neural circuitry, must be considered to fully understand the development and evolution of behavior.
Abstract
Insects use sex pheromones as a reproductive isolating mechanism to attract conspecifics and repel heterospecifics. Despite the profound knowledge of sex pheromones, little is known about ...the coevolutionary mechanisms and constraints on their production and detection. Using whole-genome sequences to infer the kinship among 99 drosophilids, we investigate how phylogenetic and chemical traits have interacted at a wide evolutionary timescale. Through a series of chemical syntheses and electrophysiological recordings, we identify 52 sex-specific compounds, many of which are detected via olfaction. Behavioral analyses reveal that many of the 43 male-specific compounds are transferred to the female during copulation and mediate female receptivity and/or male courtship inhibition. Measurement of phylogenetic signals demonstrates that sex pheromones and their cognate olfactory channels evolve rapidly and independently over evolutionary time to guarantee efficient intra- and inter-specific communication systems. Our results show how sexual isolation barriers between species can be reinforced by species-specific olfactory signals.
Innate behaviors are often executed in concert with accompanying physiological programs. How this coordination is achieved is poorly understood. Mating behavior and the transfer of sperm and seminal ...fluid (SSFT) provide a model for understanding how concerted behavioral and physiological programs are coordinated. Here we identify a male-specific neural pathway that coordinates the timing of SSFT with the duration of copulation behavior in Drosophila. Silencing four abdominal ganglion (AG) interneurons (INs) that contain the neuropeptide corazonin (Crz) both blocked SSFT and substantially lengthened copulation duration. Activating these Crz INs caused rapid ejaculation in isolated males, a phenotype mimicked by injection of Crz peptide. Crz promotes SSFT by activating serotonergic (5-HT) projection neurons (PNs) that innervate the accessory glands. Activation of these PNs in copulo caused premature SSFT and also shortened copulation duration. However, mating terminated normally when these PNs were silenced, indicating that SSFT is not required for appropriate copulation duration. Thus, the lengthened copulation duration phenotype caused by silencing Crz INs is independent of the block to SSFT. We conclude that four Crz INs independently control SSFT and copulation duration, thereby coupling the timing of these two processes.
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