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.

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.

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.

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.

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.

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.

Evolutionary trade-offs between testes size and parenting in Neotropical glassfrogs.

In males, large testes size signifies high sperm production and is commonly linked to heightened sperm competition levels. It may also evolve as a response to an elevated risk of sperm depletion due to multiple mating or large clutch sizes. Conversely, weapons, mate or clutch guarding may allow individuals to monopolize mating events and preclude sperm competition, thereby reducing the selection of large testes. Herein, we examined how paternal care, sexual size dimorphism (SSD), weaponry and female fecundity are linked to testes size in glassfrogs. We found that paternal care was associated with a reduction in relative testes size, suggesting an evolutionary trade-off between testes size and parenting. Although females were slightly larger than males and species with paternal care tended to have larger clutches, there was no significant relationship between SSD, clutch size and relative testes size. These findings suggest that the evolution of testes size in glassfrogs is influenced by sperm competition risk, rather than sperm depletion risk. We infer that clutch guarding precludes the risk of fertilization by other males and consequently diminishes selective pressure for larger testes. Our study highlights the prominent role of paternal care in the evolution of testes size in species with external fertilization.

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.

Exposure to female olfactory cues hastens reproductive ageing and increases mortality when mating in male mice.

Theories of ageing predict that investment in reproduction will trade-off against survival and later-life reproduction. Recent evidence from invertebrates suggests that just perceiving cues of a potential mate's presence can reduce lifespan, particularly in males, and that activation of neuroendocrine reward pathways associated with mating can alleviate these effects. Whether similar effects occur in vertebrates remains untested. We tested whether exposure to olfactory cues from the opposite sex would influence mortality and reproductive senescence in male mice. We observed that males exposed to female olfactory cues from middle- to old age (from 10 to 24 months of age) showed reduced late-life fertility, irrespective of whether they had also been allowed to mate with females earlier in life. Males that were exposed to female odours in conjunction with mating also showed an increased mortality rate across the exposure period, indicating that olfactory cues from females can increase male mortality in some environments. Our results show that exposure to female odours can influence reproductive ageing and mortality in male mice, highlighting that sensory perception of mates may be an important driver of life-history trade-offs in mammals.

Long-term neuropeptide modulation of female sexual drive via the TRP channel in Drosophila melanogaster.

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 pyx expression and pC1 excitability. Dh44 is orthologous to the conserved corticotrophin-releasing hormone family, suggesting similar roles in other species.

The evolution of sexual dimorphism in gene expression in response to a manipulation of mate competition.

Many genes are differentially expressed between males and females and patterns of sex-biased gene expression (SBGE) vary among species. Some of this variation is thought to have evolved in response to differences in mate competition among species that cause varying patterns of sex-specific selection. We used experimental evolution to test this by quantifying SBGE and sex-specific splicing in 15 Drosophila melanogaster populations that evolved for 104 generations in mating treatments that removed mate competition via enforced monogamy, or allowed mate competition in either small, simple, or larger, structurally more complex mating environments. Consistent with sex-specific selection affecting SBGE, initially sex-biased genes diverged in expression more among treatments than unbiased genes, and there was greater expression divergence for male- than female-biased genes. It has been suggested the transcriptome should be "feminized" under monogamy because of the removal of sexual selection on males; we did not observe this, likely because selection differs in additional ways between monogamy vs. polygamy. Significant divergence in average expression dimorphism between treatments was observed and, in some treatment comparisons, the direction of the divergence differed across different sex-bias categories. There was not a generalized reduction in expression dimorphism under enforced monogamy.

Sexual cannibalism as a female resistance trait: a new hypothesis.

Female spiders and praying mantises are renowned for their cannibalism of male partners before, during, or after mating. While several hypotheses have been proposed to explain species-specific examples of sexual cannibalism, much variation remains unexplained, including why the timing of cannibalism varies across taxa. Here, I outline how sexually cannibalistic behavior could evolve via sexually antagonistic selection as a type of behavioral resistance to male-imposed mating costs, and how such a generalizable interpretation provides a framework for understanding the evolution of both sexual cannibalism in females and anti-cannibalistic traits in males. I discuss how differences between mating systems that physiologically constrain males to mate only once (monogyny) or twice (bigyny) and systems where the sexes can potentially mate multiply (polygyny and polyandry) are likely to influence how sexual conflict shapes cannibalistic behavior. I review key examples from the literature that suggest how sexually cannibalistic behavior might function as a female resistance trait and provide comprehensive predictions for testing this hypothesis empirically.

Nested neural circuits generate distinct acoustic signals during Drosophila courtship.

Many motor control systems generate multiple movements using a common set of muscles. How are premotor circuits able to flexibly generate diverse movement patterns? Here, we characterize the neuronal circuits that drive the distinct courtship songs of Drosophila melanogaster. Male flies vibrate their wings toward females to produce two different song modes-pulse and sine song-which signal species identity and male quality. Using cell-type-specific genetic reagents and the connectome, we provide a cellular and synaptic map of the circuits in the male ventral nerve cord that generate these songs and examine how activating or inhibiting each cell type within these circuits affects the song. Our data reveal that the song circuit is organized into two nested feedforward pathways with extensive reciprocal and feedback connections. The larger network produces pulse song, the more complex and ancestral song form. A subset of this network produces sine song, the simpler and more recent form. Such nested organization may be a common feature of motor control circuits in which evolution has layered increasing flexibility onto a basic movement pattern.

Neural control of reproduction in reptiles.

Reptiles display considerable diversity in reproductive behavior, making them great models to study the neuroendocrine control of reproductive behavior. Many reptile species are seasonally breeding, such that they become reproductively active during their breeding season and regress to a nonreproductive state during their nonbreeding season, with this transition often prompted by environmental cues. In this review, we will focus on summarizing the neural and neuroendocrine mechanisms controlling reproductive behavior. Three major areas of the brain are involved in reproductive behavior: the preoptic area (POA), amygdala, and ventromedial hypothalamus (VMH). The POA and VMH are sexually dimorphic areas, regulating behaviors in males and females respectively, and all three areas display seasonal plasticity. Lesions to these areas disrupt the onset and maintenance of reproductive behaviors, but the exact roles of these regions vary between sexes and species. Different hormones influence these regions to elicit seasonal transitions. Circulating testosterone (T) and estradiol (E2) peak during the breeding season and their influence on reproduction is well-documented across vertebrates. The conversion of T into E2 and 5α-dihydrotestosterone can also affect behavior. Melatonin and corticosterone have generally inhibitory effects on reproductive behavior, while serotonin and other neurohormones seem to stimulate it. In general, there is relatively little information on the neuroendocrine control of reproduction in reptiles compared to other vertebrate groups. This review highlights areas that should be considered for future areas of research.

Female Preferences for More Elaborate Signals Are an Emergent Outcome of Male Chorusing Interactions in Túngara Frogs.

AbstractIn chorusing species, conspecific interference exerts strong selection on signal form and timing to maximize conspicuousness and attractiveness within the signaling milieu. We investigated how túngara frog calling strategies were influenced by varied social environments and male phenotypes and how calling interactions influenced female preferences. When chorusing, túngara frog calls consist of a whine typically followed by one to three chucks. In experimental choruses we saw that as chorus size increased, calls increasingly had their chucks overlapped by the high-amplitude beginning section of other callers' whines. Playback experiments revealed that such overlap reduced the attractiveness of calls to females but that appending additional chucks mitigated this effect. Thus, more elaborate calls were preferred when calls suffered overlap, although they were not preferred when overlap was absent. In response to increasing risk of overlap in larger choruses, males increased call elaboration. However, males overwhelmingly produced two-chuck calls in even the largest choruses, despite our results suggesting that additional chucks would more effectively safeguard calls. Furthermore, aspects of male phenotypes predicted to limit call elaboration had negligible or uncertain effects, suggesting that other constraints are operating. These results highlight how complex interrelations among signal form, signaling interactions, and the social environment shape the evolution of communication in social species.

Sexual behaviour of young rams is improved and less stressful after intranasal administration of oxytocin.

The aim of this study was to determine if intranasal administration of oxytocin modifies sexual behaviour and the stress response in young rams during sexual tests with ewes in oestrus. Ten rams were used in a cross-over design. At Day 0, the control group (CG, n = 5) received isotonic saline spray intranasally, and the treated group (OTG, n = 5) received oxytocin (24 IU) intranasally, 40 min before the sexual test. At Day 15, the groups were reversed. In each sexual test (20 min) with an oestrous-induced ewe, the sexual behaviour of the young rams was recorded. Serum cortisol concentrations were determined before and after the test. Less flehmen was observed in the OTG, but mounts with ejaculation were increased. The OTG presented lower serum cortisol concentration than the CG. In conclusion, intranasal administration of oxytocin modified the sexual behaviour of rams, evidenced by a decrease in flehmen behaviour and an increase in mounts with ejaculation, making sexual activity more efficacious. In addition, the treatment decreased the stress response of the rams in the sexual tests. Therefore, intranasal administration of oxytocin could be used to increase sexual activity in rams, and with less stress, providing better welfare conditions.

Failure to mate enhances investment in behaviors that may promote mating reward and impairs the ability to cope with stressors via a subpopulation of Neuropeptide F receptor neurons.

Living in dynamic environments such as the social domain, where interaction with others determines the reproductive success of individuals, requires the ability to recognize opportunities to obtain natural rewards and cope with challenges that are associated with achieving them. As such, actions that promote survival and reproduction are reinforced by the brain reward system, whereas coping with the challenges associated with obtaining these rewards is mediated by stress-response pathways, the activation of which can impair health and shorten lifespan. While much research has been devoted to understanding mechanisms underlying the way by which natural rewards are processed by the reward system, less attention has been given to the consequences of failure to obtain a desirable reward. As a model system to study the impact of failure to obtain a natural reward, we used the well-established courtship suppression paradigm in Drosophila melanogaster as means to induce repeated failures to obtain sexual reward in male flies. We discovered that beyond the known reduction in courtship actions caused by interaction with non-receptive females, repeated failures to mate induce a stress response characterized by persistent motivation to obtain the sexual reward, reduced male-male social interaction, and enhanced aggression. This frustrative-like state caused by the conflict between high motivation to obtain sexual reward and the inability to fulfill their mating drive impairs the capacity of rejected males to tolerate stressors such as starvation and oxidative stress. We further show that sensitivity to starvation and enhanced social arousal is mediated by the disinhibition of a small population of neurons that express receptors for the fly homologue of neuropeptide Y. Our findings demonstrate for the first time the existence of social stress in flies and offers a framework to study mechanisms underlying the crosstalk between reward, stress, and reproduction in a simple nervous system that is highly amenable to genetic manipulation.

Hair from sexually active bucks strongly activates olfactory sensory inputs but fails to trigger early first ovulation in prepubescent does.

Early exposure of does to sexually active bucks triggers early puberty onset correlating with neuroendocrine changes. However, the sensory pathways that are stimulated by the male are still unknown. Here, we assessed whether responses to olfactory stimuli are modulated by social experience (exposure to males or not) and/or endocrine status (prepubescent or pubescent). We used a calcium imaging approach on goat sensory cells from the main olfactory epithelium (MOE) and the vomeronasal organ (VNO). For both cell types, we observed robust responses to active male hair in females under three physiological conditions: prepubescent females isolated from males (ISOL PrePub), pubescent females exposed to males (INT Pub) and isolated females (ISOL Pub). Response analysis showed overall greater proportion of responses to buck hair in ISOL PrePub. We hypothesized that females would be more responsive to active buck hair during the prepubertal period, with numerous responses perhaps originating from immature neurons. We also observed a greater proportion of mature olfactory neurons in the MOE and VNO of INT Pub females suggesting that male exposure can induce plastic changes on olfactory cell function and organization. To determine whether stimulation by male odor can advance puberty, we exposed prepubescent does to active buck hair (ODOR). In both ODOR and females isolated from males (ISOL) groups, puberty was reached one month after females exposed to intact bucks (INT), suggesting that olfactory stimulation is not sufficient to trigger puberty.

On the function of a female-like signal type in the vibrational repertoire of Enchenopa male treehoppers (Hemiptera: Membracidae).

Animals often mimic the behaviours or signals of conspecifics of the opposite sex while courting. We explored the potential functions of a novel female-like signal type in the courtship displays of male Enchenopa treehoppers. In these plant-feeding insects, males produce plant-borne vibrational advertisement signals, to which females respond with their own duetting signals. Males also produce a signal type that resembles the female duetting responses. We experimentally tested whether this signal modifies the behaviour of receivers. First, we tested whether the female-like signal would increase the likelihood of a female response. However, females were as likely to respond to playbacks with or without them. Second, we tested whether the female-like signal would inhibit competing males, but males were as likely to produce displays after playbacks with or without them. Hence, we found no evidence that this signal has an adaptive function, despite its presence in the courtship display, where sexual selection affects signal features. Given these findings, we also explored whether the behavioural and morphological factors of the males were associated with the production of the female-like signal. Males that produced this signal had higher signalling effort (longer and more frequent signals) than males that did not produce it, despite being in worse body condition. Lastly, most males were consistent over time in producing the female-like signal or not. These findings suggest that condition-dependent or motivational factors explain the presence of the female-like signal. Alternatively, this signal might not bear an adaptive function, and it could be a way for males to warm up or practice signalling, or even be a by-product of how signals are transmitted through the plant. We suggest further work that might explain our puzzling finding that a signal in the reproductive context might not have an adaptive function.