Polyandry and sperm competition in two traumatically inseminating species of Strepsiptera (Insecta).

Polyandry, the practice of females mating with multiple males, is a strategy found in many insect groups. Whether it increases the likelihood of receiving beneficial genes from male partners and other potential benefits for females is controversial. Strepsiptera are generally considered monandrous, but in a few species females have been observed copulating serially with multiple males. Here we show that the offspring of a single female can have multiple fathers in two Strepsiptera species: Stylops ovinae (Stylopidae) and Xenos vesparum (Xenidae). We studied female polyandry in natural populations of these two species by analysis of polymorphic microsatellite loci. Our results showed that several fathers can be involved in both species, in some cases up to four. Mating experiments with S. ovinae have shown that the first male to mates with a given female contributes to a higher percentage of the offspring than subsequent males. In X. vesparum, however, we found no significant correlation between mating duration and offspring contribution. The prolonged copulation observed in S. ovinae may have the advantage of reducing competition with sperm from other males. Our results show that monandry may not be the general pattern of reproduction in the insect order Strepsiptera.

Eviction-driven infanticide and sexually selected adoption and infanticide in a neotropical parrot.

Infanticide and adoption have been attributed to sexual selection, where an individual later reproduces with the parent whose offspring it killed or adopted. While sexually selected infanticide is well known, evidence for sexually selected adoption is anecdotal. We report on both behaviors at 346 nests over 27 y in green-rumped parrotlets (Forpus passerinus) in Venezuela. Parrotlets are monogamous with long-term pair bonds, exhibit a strongly male-biased adult sex ratio, and nest in cavities that are in short supply, creating intense competition for nest sites and mates. Infanticide attacks occurred at 256 nests in two distinct contexts: 1) Attacks were primarily committed by nonbreeding pairs (69%) attempting to evict parents from the cavity. Infanticide attacks per nest were positively correlated with population size and evicting pairs never adopted abandoned offspring. Competition for limited nest sites was a primary cause of eviction-driven infanticide, and 2) attacks occurred less frequently at nests where one mate died (31%), was perpetrated primarily by stepparents of both sexes, and was independent of population size. Thus, within a single species and mating system, infanticide occurred in multiple contexts due to multiple drivers. Nevertheless, 48% of stepparents of both sexes adopted offspring, and another 23% of stepfathers exhibited both infanticide and long-term care. Stepfathers were often young males who subsequently nested with widows, reaching earlier ages of first breeding than competitors and demonstrating sexually selected adoption. Adoption and infanticide conferred similar fitness benefits to stepfathers and appeared to be equivalent strategies driven by limited breeding opportunities, male-biased sex ratios, and long-term monogamy.

Desire, Marriage, and Overpopulation: The Sexual Lives of Insects in the Enlightenment.

During the eighteenth century, the discovery of sexual reproduction in insect species prompted the demise of spontaneous generation and new developments in natural history, theology, and political economy. The sexual lives of insects prompted debates on whether insects were governed by desire, free will, and even marital tendency. Fuelled by the democratisation of microscopy, early modern entomology took a new turn and breadth: the study of insects and of their sexual lives provided unexpected new insights into human sexuality, reproduction, and Malthusian fears of overpopulation. This article surveys the intellectual culture of entomology and natural history during the crucial decades when entomologists worked to quantify the reproductive capacities of insect species. Assessing the influences these entomological works had within political economy and theology, we argue that the sexual lives of insects - once analysed and delineated - influenced familiar ideological features of the intellectual landscape of the late Enlightenment, particularly in the theological philosophies of northern Europe and in the political economy of population in Britain.

Differences in expression of male aggression between wild bonobos and chimpanzees.

Researchers investigating the evolution of human aggression look to our closest living relatives, bonobos (Pan paniscus) and chimpanzees (Pan troglodytes), as valuable sources of comparative data.1,2 Males in the two species exhibit contrasting patterns: male chimpanzees sexually coerce females3,4,5,6,7,8 and sometimes kill conspecifics,9,10,11,12 whereas male bonobos exhibit less sexual coercion13,14 and no reported killing.13 Among the various attempts to explain these species differences, the self-domestication hypothesis proposes negative fitness consequences of male aggression in bonobos.2,15,16 Nonetheless, the extent to which these species differ in overall rates of aggression remains unclear due to insufficiently comparable observation methods.17,18,19,20,21,22,23 We used 14 community-years of focal follow data-the gold standard for observational studies24-to compare rates of male aggression in 3 bonobo communities at the Kokolopori Bonobo Reserve, Democratic Republic of Congo, and 2 chimpanzee communities at Gombe National Park, Tanzania. As expected, given that females commonly outrank males, we found that bonobos exhibited lower rates of male-female aggression and higher rates of female-male aggression than chimpanzees. Surprisingly, we found higher rates of male-male aggression among bonobos than chimpanzees even when limiting analyses to contact aggression. In both species, more aggressive males obtained higher mating success. Although our findings indicate that the frequency of male-male aggression does not parallel species difference in its intensity, they support the view that contrary to male chimpanzees, whose reproductive success depends on strong coalitions, male bonobos have more individualistic reproductive strategies.25.

Kisspeptin administration may promote precopulatory behavior in male rats independently or supplementally to testosterone and contribute to proceptive behavior in female partners, reducing mating failure.

Kisspeptin is a peptide that plays an important role through its effects on the hypothalamus-pituitary-gonadal (HPG) axis. It has also been implicated in sexual behavior. The present study investigated whether the relationship between kisspeptin and sexual behavior is independent of the HPG axis, i.e., testosterone. Sexual behavior was examined after the administration of kisspeptin to gonadally intact male rats and gonadectomized male rats that received testosterone supplementation. Other male rats were also observed for sexual behavior once a week from 2 to 5 weeks after gonadectomy and receiving kisspeptin for the sixth postoperative week. Sexual behavior in female rats serving as the partner for each male was also observed. Female rats were not administered kisspeptin in the present study. The results obtained showed that the administration of kisspeptin increased precopulatory behavior in gonadally intact male rats and gonadectomized male rats that received testosterone supplementation and proceptive behavior in their female partners. Precopulatory behavior in males and receptive behavior in females increased, while copulatory behavior in males and receptive behavior in females remained unchanged. Furthermore, the administration of kisspeptin increased precopulatory behavior in gonadectomized males, but did not affect receptive behavior in females. These results suggest that kisspeptin affected males independently and/or supplementally to testosterone, and also that changes in the presence of testosterone in males had an impact on proceptive behavior in their female partners. In conclusion, kisspeptin may involve an as-yet-unidentified neural pathway in sexual desire independently of the HPG axis.

Developmental neuroscience: Building sex-specific adult circuitry from common larval origins.

The development of sex-specific neural circuitry is critical for reproductive behaviors. A new study traces the developmental origin of female-specific neurons that underlie an adult mating behavior to larval neurons common to both sexes in Drosophila.

Role of neuroestrogens in the regulation of social behaviors - From social recognition to mating.

In this mini-review, we summarize the brain distribution of aromatase, the enzyme catalyzing the synthesis of estrogens from androgens, and the mechanisms responsible for regulating estrogen production within the brain. Understanding this local synthesis of estrogens by neurons is pivotal as it profoundly influences various facets of social behavior. Neuroestrogen action spans from the initial processing of socially pertinent sensory cues to integrating this information with an individual's internal state, ultimately resulting in the manifestation of either pro-affiliative or - aggressive behaviors. We focus here in particular on aggressive and sexual behavior as the result of correct individual recognition of intruders and potential mates. The data summarized in this review clearly point out the crucial role of locally synthesized estrogens in facilitating rapid adaptation to the social environment in rodents and birds of both sexes. These observations not only shed light on the evolutionary significance but also indicate the potential implications of these findings in the realm of human health, suggesting a compelling avenue for further investigation.

Small-bodied males invest in larger testes when highly ornamented.

Sperm competition and male mating rate are two non-mutually exclusive key evolutionary pressures selecting for larger testes within and across animal taxa. A few studies have tried to test the role of mating rate in the absence of sperm competition. Under the mating rate hypothesis, particular phenotypes of a given population that are expected to gain more mates (e.g., more ornamented males) are expected to make higher investments in testes size (a proxy for sperm production). We test this prediction in Polistes simillimus, a neotropical paper wasp in which females are single mated (no sperm competition) and males can mate with multiple partners. Testes size was predicted by body size (positive association), sexual ornamentation (negative association), and their interaction (among small males, testes size was positively related to ornamentation, but the opposite pattern was observed among large males). We propose that small-bodied well-ornamented males may face the highest risk of sperm depletion. Small-bodied males make relatively higher investment in testes size when highly ornamented. This strategy might be less profitable to large males, as they have overall larger testes. Our results provide strong evidence for the mating rate hypothesis.

Stress during pubertal development affects female sociosexual behavior in mice.

Puberty is a crucial phase for the development of female sexual behavior. Growing evidence suggests that stress during this period may interfere with the development of sexual behavior. However, the neural circuits involved in this alteration remain elusive. Here, we demonstrated in mice that pubertal stress permanently disrupted sexual performance without affecting sexual preference. This was associated with a reduced expression and activation of neuronal nitric oxide synthase (nNOS) in the ventrolateral part of the ventromedial hypothalamus (VMHvl). Fiber photometry revealed that VMHvl nNOS neurons are strongly responsive to male olfactory cues with this activation being substantially reduced in pubertally stressed females. Finally, treatment with a NO donor partially restored sexual performance in pubertally stressed females. This study provides insights into the involvement of VMHvl nNOS in the processing of olfactory cues important for the expression of female sexual behavior. In addition, exposure to stress during puberty disrupts the integration of male olfactory cues leading to reduced sexual behavior.

C. elegans males optimize mate-preference decisions via sex-specific responses to multimodal sensory cues.

For sexually reproducing animals, selecting optimal mates is important for maximizing reproductive fitness. In the nematode C. elegans, populations reproduce largely by hermaphrodite self-fertilization, but the cross-fertilization of hermaphrodites by males also occurs. Males' ability to recognize hermaphrodites involves several sensory cues, but an integrated view of the ways males use these cues in their native context to assess characteristics of potential mates has been elusive. Here, we examine the mate-preference behavior of C. elegans males evoked by natively produced cues. We find that males use a combination of volatile sex pheromones (VSPs), ascaroside sex pheromones, surface-associated cues, and other signals to assess multiple features of potential mates. Specific aspects of mate preference are communicated by distinct signals: developmental stage and sex are signaled by ascaroside pheromones and surface cues, whereas the presence of a self-sperm-depleted hermaphrodite is likely signaled by VSPs. Furthermore, males prefer to interact with virgin over mated, and well-fed over food-deprived, hermaphrodites; these preferences are likely adaptive and are also mediated by ascarosides and other cues. Sex-typical mate-preference behavior depends on the sexual state of the nervous system, such that pan-neuronal genetic masculinization in hermaphrodites generates male-typical social behavior. We also identify an unexpected role for the sex-shared ASH sensory neurons in male attraction to ascaroside sex pheromones. Our findings lead to an integrated view in which the distinct physical properties of various mate-preference cues guide a flexible, stepwise behavioral program by which males assess multiple features of potential mates to optimize mate preference.

Male manipulation impinges on social-dependent tumor suppression in Drosophila melanogaster females.

Physiological status can influence social behavior, which in turn can affect physiology and health. Previously, we reported that tumor growth in Drosophila virgin females depends on the social context, but did not investigate the underlying physiological mechanisms. Here, we sought to characterize the signal perceived between tumorous flies, ultimately discovering that the tumor suppressive effect varies depending on reproductive status. Firstly, we show that the tumor suppressive effect is neither dependent on remnant pheromone-like products nor on the microbiota. Transcriptome analysis of the heads of these tumorous flies reveals social-dependent gene-expression changes related to nervous-system activity, suggesting that a cognitive-like relay might mediate the tumor suppressive effect. The transcriptome also reveals changes in the expression of genes related to mating behavior. Surprisingly, we observed that this social-dependent tumor-suppressive effect is lost in fertilized females. After mating, Drosophila females change their behavior-favoring offspring survival-in response to peptides transferred via the male ejaculate, a phenomenon called "male manipulation". Remarkably, the social-dependent tumor suppressive effect is restored in females mated by sex-peptide deficient males. Since male manipulation has likely been selected to favor male gene transmission, our findings indicate that this evolutionary trait impedes social-dependent tumor growth slowdown.

Genetically identical mice express alternative reproductive tactics depending on social conditions in the field.

In many species, establishing and maintaining a territory is critical to survival and reproduction, and an animal's ability to do so is strongly influenced by the presence and density of competitors. Here we manipulate social conditions to study the alternative reproductive tactics displayed by genetically identical, age-matched laboratory mice competing for territories under ecologically realistic social environmental conditions. We introduced adult males and females of the laboratory mouse strain C57BL/6J into a large, outdoor field enclosure containing defendable resource zones under one of two social conditions. We first created a low-density social environment, such that the number of available territories exceeded the number of males. After males established stable territories, we introduced a pulse of intruder males and observed the resulting defensive and invasive tactics employed. In response to this change in social environment, males with large territories invested more in patrolling but were less effective at excluding intruder males as compared with males with small territories. Intruding males failed to establish territories and displayed an alternative tactic featuring greater exploration as compared with genetically identical territorial males. Alternative tactics did not lead to equal reproductive success-males that acquired territories experienced greater survival and had greater access to females.

Chronic MK-801 administration provokes persistent deficits in social memory in the prairie vole (Microtus ochrogaster): A potential animal model for social deficits of schizophrenia.

The prairie vole (Microtus ochrogaster) is a rodent species that has been used extensively to study biological aspects of human social bonding. Nevertheless, this species has not been studied in the context of modeling social deficits characteristic of schizophrenia. Building on studies in rodents that show that sub-chronic administration of an NMDA receptor antagonist induces persistent behavioral and neurological characteristics of schizophrenia, we administered MK-801 (0.2 mg/kg, daily, for 7 days) or physiological saline to young adult (45 days old) virgin male voles. At 69 days of age, we paired these males with virgin females. 24 h later, we assessed the males' social investigation of each female across the first 5 min of a three-hour preference test, and side-by-side contact with each female during the last hour of the test. Unlike saline-treated males, MK-801-treated males did not preferentially investigate the unfamiliar female, indicating a deficit in social memory. Although males of both groups preferentially spent time with their female partner, regression analysis revealed that deficits in social memory predicted lower partner preference in MK-801-treated males. We interpret these results in the context of recent studies of the natural history of the prairie vole as well as in the context of cognitive deficits in schizophrenia and propose that the social component of episodic memory might influence an individual's capacity to form and maintain long-term social bonds.

An automatic system for recognizing fly courtship patterns via an image processing method.

Fruit fly courtship behaviors composed of a series of actions have always been an important model for behavioral research. While most related studies have focused only on total courtship behaviors, specific courtship elements have often been underestimated. Identifying these courtship element details is extremely labor intensive and would largely benefit from an automatic recognition system. To address this issue, in this study, we established a vision-based fly courtship behavior recognition system. The system based on the proposed image processing methods can precisely distinguish body parts such as the head, thorax, and abdomen and automatically recognize specific courtship elements, including orientation, singing, attempted copulation, copulation and tapping, which was not detectable in previous studies. This system, which has high identity tracking accuracy (99.99%) and high behavioral element recognition rates (> 97.35%), can ensure correct identification even when flies completely overlap. Using this newly developed system, we investigated the total courtship time, and proportion, and transition of courtship elements in flies across different ages and found that male flies adjusted their courtship strategy in response to their physical condition. We also identified differences in courtship patterns between males with and without successful copulation. Our study therefore demonstrated how image processing methods can be applied to automatically recognize complex animal behaviors. The newly developed system will largely help us investigate the details of fly courtship in future research.

Low dose of propyl-pyrazole-triol, an agonist of estrogen receptor alpha, administration stimulates the Coolidge effect in fadrozole-treated male rats.

Estrogen receptor (ER) α is involved in male sexual function. Here, we aim to investigate how ERα activation influences sexual satiety and the Coolidge effect (i.e., when a rat, that has reached sexual satiety, experiences an increased arousal after exposure to a novel sexual partner) in estrogen-deprived male rats. Male rats (8 per group) were treated daily for 29 days with either saline (Control group) or fadrozole dissolved in saline (1 mg/kg/day) 1 h before mating. On Days 13 and 29, rats treated with fadrozole received either no additional treatment (fadrozole group) or a single injection of propyl-pyrazole-triol (ERα-agonist group, dissolved in sesame oil, 1 mg/kg). Rats mated until reaching sexual satiety on Days 13 and 29. In these sessions, the Control group displayed higher frequency of intromission and ejaculation than the other groups. The ERα-agonist group mounted more frequently but reached sexual satiety sooner than the Control group. On Day 29, when exposed to a new sexual partner, the fadrozole-treated rats were less likely to display intromission than the other groups, or ejaculation than the Control group, or mounting than the ERα-agonist group. The Control group showed more ejaculatory behavior and shorter ejaculation latency than the other groups. Body weights, testosterone levels, estradiol levels, and ERα-immunoreactive cell counts in brain regions for sexual behavior were comparable between groups after 29 days of treatments. Our data suggest that estrogen helps regulate sexual satiety and the Coolidge effect in male rats.

Estrogenic influences on agonistic behavior in teleost fishes.

Teleost fishes show an extraordinary diversity of sexual patterns, social structures, and sociosexual behaviors. Sex steroid hormones are key modulators of social behaviors in teleosts as in other vertebrates and act on sex steroid receptor-containing brain nuclei that form the evolutionarily conserved vertebrate social behavior network (SBN). Fishes also display important differences relative to tetrapod vertebrates that make them particularly well-suited to study the physiological mechanisms modulating social behavior. Specifically, fishes exhibit high levels of brain aromatization and have what has been proposed to be a lifelong, steroid hormone dependent plasticity in the neural substrates mediating sociosexual behavior. In this review, we examine how estrogenic signaling modulates sociosexual behaviors in teleosts with a particular focus on agonistic behavior. Estrogens have been shown to mediate agonistic behaviors in a broad range of fishes, from sexually monomorphic gonochoristic species to highly dimorphic sex changers with alternate reproductive phenotypes. These similarities across such diverse taxa contribute to a growing body of evidence that estrogens play a crucial role in the modulation of aggression in vertebrates. As analytical techniques and genomic tools rapidly advance, methods such as LC-MS/MS, snRNAseq, and CRISPR-based mutagenesis show great promise to further elucidate the mechanistic basis of estrogenic effects on social behavior in the diverse teleost lineage.

A tale of two males: Behavioral and neural mechanisms of alternative reproductive tactics in midshipman fish.

An amalgam of investigations at the interface of neuroethology and behavioral neuroendocrinology first established the most basic behavioral, neuroanatomical, and neurophysiological characters of vocal-acoustic communication morphs in the plainfin midshipman fish, Porichthys notatus Girard. This foundation has led, in turn, to the repeated demonstration that neuro-behavioral mechanisms driving reproductive-related, vocal-acoustic behaviors can be uncoupled from gonadal state for two adult male phenotypes that follow alternative reproductive tactics (ARTs).

A review of the reproductive biology of mormyroid fishes: An emerging model for biomedical research.

Mormyroidea is a superfamily of weakly electric African fishes with great potential as a model in a variety of biomedical research areas including systems neuroscience, muscle cell and craniofacial development, ion channel biophysics, and flagellar/ciliary biology. However, they are currently difficult to breed in the laboratory setting, which is essential for any tractable model organism. As such, there is a need to better understand the reproductive biology of mormyroids to breed them more reliably in the laboratory to effectively use them as a biomedical research model. This review seeks to (1) briefly highlight the biomedically relevant phenotypes of mormyroids and (2) compile information about mormyroid reproduction including sex differences, breeding season, sexual maturity, gonads, gametes, and courtship/spawning behaviors. We also highlight areas of mormyroid reproductive biology that are currently unexplored and/or have the potential for further investigation that may provide insights into more successful mormyroid laboratory breeding methods.

Developmental remodeling repurposes larval neurons for sexual behaviors in adult Drosophila.

Most larval neurons in Drosophila are repurposed during metamorphosis for functions in adult life, but their contribution to the neural circuits for sexually dimorphic behaviors is unknown. Here, we identify two interneurons in the nerve cord of adult Drosophila females that control ovipositor extrusion, a courtship rejection behavior performed by mated females. We show that these two neurons are present in the nerve cord of larvae as mature, sexually monomorphic interneurons. During pupal development, they acquire the expression of the sexual differentiation gene, doublesex; undergo doublesex-dependent programmed cell death in males; and are remodeled in females for functions in female mating behavior. Our results demonstrate that the neural circuits for courtship in Drosophila are built in part using neurons that are sexually reprogrammed from former sex-shared activities in larval life.