Sociosexual Interactions Research Articles

Sociosexual interactions: A clock synchronized by smell

While the daily rhythmicity of organisms is entrained by several cues, light is thought to be the strongest signal. Surprisingly, a new study in a moth shows that olfactory communication can be even more powerful for synchronization, and, at least to some extent, works across related species.

Pheromone-mediated command from the female to male clock induces and synchronizes circadian rhythms of the moth Spodoptera littoralis

To extract any adaptive benefit, the circadian clock needs to be synchronized to the 24-h day-night cycles. We have investigated if it is a general property of the brain's circadian clock to recognize social interactions as external time givers. Sociosexual interactions with the opposite sex are universal, prevalent even in the lives of solitary animals. The solitary adult life of the Spodoptera littoralis moth is singularly dedicated to sex, offering an ideal context for exploring the impact of sociosexual cues on circadian timekeeping. We have identified specific olfactory cues responsible for social entrainment, revealing a surprisingly strong influence of pheromone-mediated remote sociosexual interactions on circadian rhythms. Males' free-running rhythms are induced and synchronized by the sex pheromone that the female releases in a rhythmic fashion, highlighting a hierarchical relation between the female and male circadian oscillators. Even a single pulse of the sex pheromone altered clock gene expression in the male brain, surpassing the effect of light on the clock. Our finding of a daytime-dependent, lasting impact of pheromone on male's courtship efficacy indicates that circadian timing in moths is a trait under sexual selection. We have identified specific components of the sex-pheromone blend that lack mate-attractive property but have powerful circadian effects, providing rationale for their continued retention by the female. We show that such volatiles, when shared across sympatric moth species, can trigger communal synchronization. Our results suggest that the sex pheromone released by female moths entrains males' behavioral activity rhythm to ensure synchronized timing of mating.

Understanding the impact of sociosexual interactions on sleep using Drosophila melanogaster as a model organism.

Sleep is conserved across species, and it is believed that a fixed amount of sleep is needed for normal neurobiological functions. Sleep rebound follows sleep deprivation; however, continuous sleep deprivation for longer durations is believed to be detrimental to the animal's wellbeing. Under some physiologically demanding situations, such as migration in birds, the birth of new offspring in cetaceans, and sexual interactions in pectoral sandpipers, animals are known to forgo sleep. The mechanisms by which animals forgo sleep without having any obvious negative impact on the proper functioning of their neurobiological processes are yet unknown. Therefore, a simple assay is needed to study how animals forgo sleep. The assay should be ecologically relevant so it can offer insights into the physiology of the organisms. Equally important is that the organism should be genetically amenable, which helps in understanding the cellular and molecular processes that govern such behaviors. This paper presents a simple method of sociosexual interaction to understand the process by which animals forgo sleep. In the case of Drosophila melanogaster, when males and females are in proximity, they are highly active and lose a significant amount of sleep. In addition, there is no sleep rebound afterward, and instead, males engaged in sexual interactions continue to show normal sleep. Thus, sexual drive in the fruit flies is a robust assay to understand the underlying mechanism by which animals forgo sleep.

Modulating chronic outcomes after pediatric traumatic brain injury: Distinct effects of social and environmental enrichment

Impairments in social and cognitive function are a common consequence of pediatric traumatic brain injury (TBI). Rehabilitation has the potential to promote optimal behavioral recovery. Here, we evaluated whether an enhanced social and/or cognitive environment could improve long-term outcomes in a preclinical model of pediatric TBI. Male C57Bl/6 J mice received a moderately-severe TBI or sham procedure at postnatal day 21. After one week, mice were randomized to different social conditions (minimal socialization, n = 2/cage; or social grouping, n = 6/cage), and housing conditions (standard cage, or environmental enrichment (EE), incorporating sensory, motor, and cognitive stimuli). After 8 weeks, neurobehavioral outcomes were assessed, followed by post-mortem neuropathology. We found that TBI mice exhibited hyperactivity, spatial memory deficits, reduced anxiety-like behavior, and reduced sensorimotor performance compared to age-matched sham controls. Pro-social and sociosexual behaviors were also reduced in TBI mice. EE increased sensorimotor performance, and the duration of sociosexual interactions. Conversely, social housing reduced hyperactivity and altered anxiety-like behavior in TBI mice, and reduced same-sex social investigation. TBI mice showed impaired spatial memory retention, except for TBI mice exposed to both EE and group housing. In the brain, while TBI led to significant regional tissue atrophy, social housing had modest neuroprotective effects on hippocampal volumes, neurogenesis, and oligodendrocyte progenitor numbers. In conclusion, manipulation of the post-injury environment has benefit for chronic behavioral outcomes, but the benefits are specific to the type of enrichment available. This study improves understanding of modifiable factors that may be harnessed to optimize long-term outcomes for survivors of early-life TBI.

Increased male investment in sperm competition results in reduced maintenance of gametes.

Male animals often show higher mutation rates than their female conspecifics. A hypothesis for this male bias is that competition over fertilization of female gametes leads to increased male investment into reproduction at the expense of maintenance and repair, resulting in a trade-off between male success in sperm competition and offspring quality. Here, we provide evidence for this hypothesis by harnessing the power of experimental evolution to study effects of sexual selection on the male germline in the seed beetle Callosobruchus maculatus. We first show that 50 generations of evolution under strong sexual selection, coupled with experimental removal of natural selection, resulted in males that are more successful in sperm competition. We then show that these males produce progeny of lower quality if engaging in sociosexual interactions prior to being challenged to surveil and repair experimentally induced damage in their germline and that the presence of male competitors alone can be enough to elicit this response. We identify 18 candidate genes that showed differential expression in response to the induced germline damage, with several of these previously implicated in processes associated with DNA repair and cellular maintenance. These genes also showed significant expression changes across sociosexual treatments of fathers and predicted the reduction in quality of their offspring, with expression of one gene also being strongly correlated to male sperm competition success. Sex differences in expression of the same 18 genes indicate a substantially higher female investment in germline maintenance. While more work is needed to detail the exact molecular underpinnings of our results, our findings provide rare experimental evidence for a trade-off between male success in sperm competition and germline maintenance. This suggests that sex differences in the relative strengths of sexual and natural selection are causally linked to male mutation bias. The tenet advocated here, that the allocation decisions of an individual can affect plasticity of its germline and the resulting genetic quality of subsequent generations, has several interesting implications for mate choice processes.

More Than Just Kibbles: Keeper Familiarity and Food Can Affect Bonobo Behavior.

The welfare of captive animals relies on numerous factors. Keepers can affect animals' welfare and this could especially apply to emotionally and cognitively complex species, such as great apes. We collected video data over three months on 17 bonobos (La Vallée des Singes, France) and extracted five behaviours (play, aggression, anxiety, gestures, sociosexual interactions) -during two-minute slots-under three conditions: keeper-present/food-unavailable; keeper-present/food-available; keeper-absent/food-unavailable. We ran generalized linear models to investigate whether behavioral frequencies were affected by food presence/quality and keeper familiarity. Anxiety-related behaviors increased when the keeper was present and in absence of food, due to food expectation. Sociosexual interactions increased in presence of more familiar keepers and in absence of food, maybe to decrease the tension around food. Gestures increased in presence of more familiar keepers and with low-quality food, which was provided in large 'catchable' pieces. Aggression levels increased with high-quality food with no effect of keeper. Play behavior was not affected by any variable. Hence, bonobos were affected not just by food but also by keeper features. Considering multiple variables in the 'welfare equation' can improve captive management and increase the well-being of bonobos, a species that is much closer to humans than to other non-human animals.

Rams sexually activated in spring by light treatment stimulate social and sexual activities in non-activated rams

Twelve rams were used to confirm whether rams sexually activated in spring by light treatment increase social and sexual activities of non-treated rams in the presence of ewes. Males were divided into 2 groups: light-treated rams (group L, n = 6), which were exposed to artificial long days (16 h light) for 2 months (1 Nov-31 Dec), or non-exposed, control rams (group C, n = 6), exposed to the natural photoperiod. At the end of the long-day period, light-treated rams were returned to the natural photoperiod, groups isolated from each other. In mid-Feb, 3 rams from each group were put together such that 4 experimental groups were created: the remaining light-treated rams (L, n = 3), the remaining control rams (C, n = 3), and the other treated (L-mixed n = 3) and non-treated (C-mixed, n = 3) rams, exposed to 30, 30, and 60 ewes, respectively, in 3 separate paddocks. To identify each ram, large (30-cm-high) numbers were painted on the sides and rump of the males with washable sheep spray paint. Behaviors were documented by 4 video cameras using 6 30-minute segments from 1600 to 1800 h the following day (27 hours). C rams presented the lowest proportion of activities (P < 0.01), and C-mixed rams exhibited proportions similar to L and L-mixed rams. C rams exhibited the fewest fight attempts (P < 0.001), fighting (P < 0.05), pushing (P < 0.001), and sniffing another ram. The groups differed significantly (P < 0.001) in pushing, pawing, flehmen, and attempt mounting, and C rams had the fewest interactions. In conclusion, rams exposed to 2 months of long days at late-autumn early-winter increased social and sexual activities of unexposed rams. These observations can be explained by a “ram-to-ram effect”, which can enhance the endocrine activity of rams in sexual rest if they are joined with rams who have been made sexually active by a photoperiodic treatment. These findings suggest that socio-sexual interactions could be used to restrict out-of-season reproduction in this species.

Partner choice in genito-genital rubbing among female bonobos (Pan paniscus) is highly dependent on physical proximity.

Sociosexual interactions of non-human primates have multiple functions, and information on partner choice could help us to determine the major purpose of these behaviors. Female bonobos (Pan paniscus) frequently engage in genito-genital (GG) rubbing, which is categorized as a sociosexual behavior. The functions of GG rubbing may vary across allopatric bonobo populations, especially in relation to its use in social bonding. Thus, we aimed to examine the use of GG rubbing in the formation and maintenance of social bonds by examining partner choice in this context in the habituated bonobo population at Wamba, Democratic Republic of the Congo. We examined the effect of female age (and correlated dominance rank) on the proportion of solicited GG rubbing, and the effects of age difference, proximity index, and grooming index on the successful GG rubbing occurrences. Our results showed that female age significantly affected the proportion of solicited GG rubbing, indicating that older and higher-ranking females solicited this activity more frequently. Individuals of female-female dyads who were close in age and dominance rank frequently engaged in GG rubbing. The more the females in a dyad were in physical proximity, the more they engaged in GG rubbing. No correlation was observed between grooming and GG rubbing. These results indicate that partner choice in GG rubbing is highly dependent on physical proximity, and suggest that characteristics of female gregariousness might be important with respect to this choice among bonobos.

Reliability of caretakers’ ratings of captive bottlenose dolphins (Tursiops truncatus) and finless porpoises’ (Neophocaena asiaeorientalis sp.) behavioral style for welfare monitoring

ABSTRACT Qualitative ratings are increasingly used to assess animal welfare. We investigated the associations between daily caretakers’ ratings of individuals’ behavioral style, behavior during free time, participation during training sessions, and environmental variables in captive Yangtze finless porpoises, East-Asian finless porpoises, and bottlenose dolphins. Associations between caretakers’ ratings and behavior were found, including social swimming, fast swimming, play, interaction with humans, and agonistic and socio-sexual interactions. Ratings were also associated with participation during training sessions and food intake. Social separation, transport to a new pool, high visitors’ density, and holding of a sick conspecific were associated with ratings indicating a deteriorated human–animal relationship, a lower interest/fear of the environment, and/or a higher social cohesion depending on the group. Through principal component analyses, new variables that represented both caretakers’ ratings and behavior and that could be used for an easier interpretation of the data for welfare monitoring within each group were extracted. Caretaker ratings and behavior should be used as a complement to previously validated indicators to detect changes in welfare state and understand the potential causes of these changes.

To fight or not to fight: activation of the mPFC during decision to engage in aggressive behavior after ethanol consumption in a novel murine model.

Alcohol consumption is a common antecedent of aggressive behavior. The effects of alcohol on the decision to engage in aggression in preference over pro-social interaction are hypothesized to arise from augmented function within the medial prefrontal cortex (mPFC). In a newly developed procedure, we studied social decision-making in male C57BL/6J mice based on preferentially seeking access to either sociosexual interactions with a female partner or the opportunity to attack an intruder male. While deciding to engage in aggressive vs. sociosexual behavior, corresponding neural activation was assessed via c-Fos immunoreactivity in cortical, amygdaloid and tegmental regions of interest. A further objective was to investigate how self-administered alcohol impacted social choice. During repeated confrontations with an intruder male in their home cage, experimental mice engaged in species-specific sequence of pursuit, threat, and attack behavior within < 2min. Mice were then conditioned to respond at one of two separate illuminated operanda in an experimental chamber (octagon) attached to their home cage; completion of 10 responses (fixed ratio 10; FR10) was reinforced by access to either a female or a male intruder which were presented in the resident's home cage. Brains were harvested following choice between the concurrently available aggressive and sociosexual options and processed for c-Fos immunoreactivity across 10 brain regions. In two separate groups, mice were trained to rapidly self-administer ethanol prior to a social choice trial in order to examine the effects of alcohol on social choice, sociosexual, aggressive acts and postures, and concurrent c-Fos activity in the mPFC and limbic regions. Eight out of 65 mice consistently chose to engage in aggressive behavior in preference to sociosexual contact with a female when each outcome was concurrently available. Self-administered alcohol (experiment 1: 1.2 ± 0.02g/kg; experiment 2: 0, 1.0, 1.5, and 1.8g/kg) increased responding for the aggressive option in mice that previously opted predominantly for access to sociosexual interactions with the female. When choosing the aggressive, but not the sociosexual option, the prelimbic area of the mPFC revealed increased c-Fos activity, guiding future detailed inquiry into the neural mechanisms for aggressive choice.

Bared-teeth displays in bonobos (Pan paniscus): An assessment of the power asymmetry hypothesis.

Facial expressions are key to navigating social group life. The Power Asymmetry Hypothesis of Motivational Emancipation predicts that the type of social organization shapes the meaning of communicative displays in relation to an individual's dominance rank. The bared-teeth (BT) display represents one of the most widely observed communicative signals across primate species. Studies in macaques indicate that the BT display in despotic species is often performed unidirectionally, from low- to high-ranking individuals (signaling submission), whereas the BT display in egalitarian species is usually produced irrespective of dominance (mainly signaling affiliation and appeasement). Despite its widespread presence, research connecting BT displays to the power asymmetry hypothesis outside the Macaca genus remains scarce. To extend this knowledge, we investigated the production of BT in relation to social dominance in dyadic interactions (N = 11,377 events) of 11 captive bonobos (Pan paniscus). Although adult bonobos were more despotic than previously suggested in the literature, BT displays were produced irrespective of dominance rank. Moreover, while adults produced the BT exclusively during socio-sexual interactions, especially during periods of social tension, immature bonobos produced the BT in a wider number of contexts. As such, the results indicate that the communicative meaning of the BT display is consistent with signaling appeasement, especially in periods of social tension. Moreover, the BT display does not seem to signal social status, supporting the prediction for species with a high degree of social tolerance. These results advance our understanding of the origins of communicative signals and their relation to species' social systems.

Chemical cues of identity and reproductive status in Japanese macaques.

Olfactory communication plays an important role in the regulation of socio-sexual interactions in mammals. There is growing evidence that both human and nonhuman primates rely on odors to inform their mating decisions. Nevertheless, studies of primate chemical ecology remain scarce due to the difficulty of obtaining and analyzing samples. We analyzed 67 urine samples from five captive female Japanese macaques (Macaca fuscata) and 30 vaginal swabs from three of these females using gas chromatography-mass spectrometry and examined the relationship between odor (compounds identified, richness, intensity, and diversity) and female identity as well as cycle phase. We found a total of 36 urine compounds of which we identified 31, and 68 vaginal compounds of which we identified 37. Our results suggest that urine and vaginal odor varied more between individuals than within cycle phases. However, we found that within a female cycle, urine samples from similar phases may cluster more than samples from different phases. Our results suggest that female odor may encode information about identity (vaginal and urine odor) and reproductive status (urine odor). The question of how conspecifics use female urine and vaginal odor remains open and could be tested using bioassays. Our results and their interpretation are constrained by our limited sample size and our study design. Nonetheless, our study provides insight into the potential signaling role of female odor in sexual communication in Japanese macaques and contributes to our understanding of how odors may influence mating strategies in primates.

A Protocol for the Non-invasive Method of Ultrasound Separation During the Sociosexual Vocal-Non-contact Model in Rats.

Ultrasonic vocalization (USV) is one of the measurable behavioral parameters of sociosexual interactions in rats. To precisely and accurately describe the neurobehavioral properties of USV and the potentially related specific emotional responsiveness of animals, we need to know which animals vocalize and what is their exact behavioral and physiological response. To this end, we modified the non-contact cage [non-contact erection model (NCE)] by adding a modification [vocalization-non-contact erection (VOC-NCE)] that makes it possible to assign emitted ultrasonic signals to a particular animal. Typically, the NCE cage consists of two compartments separated by perforated baffles. A male is placed in one section, and a receptive female is placed in the other section. This makes possible the accurate description of sexual parameters related to the cues controlled by the experimenter. In VOC-NCE, we completely separated the male USV from the female USV by three appropriately perforated baffles and located microphones combined with ultrasonic screening. We recorded emission in both typical bands, the so-called 22- and 50-kHz bands, with various subtypes, thus highlighting the utility of our protocol to investigate the sexual dimorphism of vocalization. Similar to the anticipatory model, we showed that emission can occur without acoustic feedback from concomitants during the VOC-NCE test. Therefore, we propose a relatively simple method for assigning individual vocalization. We discuss its usefulness and limitations in assessing vocal differentiation related to sexual parameters, adaptive changes during conditioning procedures, and further applications.

Socio‐sexual interactions in captive finless porpoises and bottlenose dolphins

FIGURE S1 Photograph of the dorsal ridge of a Yangtze finless porpoise. TABLE S1 Marginal means and standard errors (SE) of (a) the frequency of socio-sexual interactions, and (b) the time spent engaged in socio-sexual interactions, depending on season and sex in captive Yangtze finless porpoises, East-Asian finless porpoises, and bottlenose dolphins. Please note: The publisher is not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing content) should be directed to the corresponding author for the article.

Experimental evidence for effects of sexual selection on condition-dependent mutation rates.

Sexual selection depletes genetic variation but depleted genetic variation limits the efficacy of sexual selection-a long-standing enigma known as the lek paradox. Here we offer a twist to this paradox by showing that sexual selection and the generation of new genetic variation via mutation may be entangled in an evolutionary feedback loop. We induced DNA damage in the germline of male seed beetles evolved under regimes manipulating the opportunity for natural and sexual selection, and quantified de novo mutations in F2-F7 generations by measuring mutation load. Sexually selected males passed on smaller loads, suggesting that selection for male quality not only purges segregating deleterious alleles, but can also reduce the rate at which such alleles originate de novo. However, when engaging in socio-sexual interactions, males evolved exclusively under sexual selection transferred greater loads, suggesting that trade-offs between naturally and sexually selected fitness components can increase mutation rate. These results offer causality to the widely observed male mutation bias and have implications for the maintenance of genetic variation in fitness.

Sociosexual behavioral patterns involving nulliparous female orangutans (Pongo sp.) reflect unique challenges during the adolescent period.

The primate adolescent period is characterized by a series of changes in physiology, behavior, and social relationships. Orangutans have the slowest life history and the longest period of dependency of all primates. As members of a semisolitary species with high levels of sexual coercion, adolescent female orangutans face a unique combination of challenges when achieving independence from their mother. This study examined the mating behavior of adolescent female orangutans and compared it with that of adult females to assess whether mating behavior reflects distinct strategies at these different points in the life cycle. Data were collected in Gunung Palung National Park on the island of Borneo over 20 years. Mating events from adolescent (n = 19) and adult females (n = 26) were scored and compared. Adolescent female mating events had significantly higher mating scores (indicating more proceptivity) than those of adult females (β = 1.948, p = .001). Adolescent females also engaged in elaborate sociosexual interactions with different flanged males, behaviors that were never observed during mating events of adult females. These interactions involved characteristic behavior on the part of both the adolescent females and the flanged males. Given these findings and the documentation of similar accounts of adolescent female-flanged male mating from the island of Sumatra, we propose that adolescent female orangutans display distinctive behavioral repertoires throughout the genus Pongo which serves to overcome male ambivalence toward nulliparous females, establish familiarity, and evaluate coercive tendencies in flanged males. We suggest that these behavioral patterns are an integral part of female social development in a female philopatric, but highly dispersed species where consistent social support is absent after ranging independence is achieved.

Sexual selection, environmental robustness, and evolutionary demography of maladapted populations: A test using experimental evolution in seed beetles.

Whether sexual selection impedes or aids adaptation has become an outstanding question in times of rapid environmental change and parallels the debate about how the evolution of individual traits impacts on population dynamics. The net effect of sexual selection on population viability results from a balance between genetic benefits of “good‐genes” effects and costs of sexual conflict. Depending on how these facets of sexual selection are affected under environmental change, extinction of maladapted populations could be either avoided or accelerated. Here, we evolved seed beetles under three alternative mating regimes to disentangle the contributions of sexual selection, fecundity selection, and male–female coevolution to individual reproductive success and population fitness. We compared these contributions between the ancestral environment and two stressful environments (elevated temperature and a host plant shift). We found evidence that sexual selection on males had positive genetic effects on female fitness components across environments, supporting good‐genes sexual selection. Interestingly, however, when males evolved under sexual selection with fecundity selection removed, they became more robust to both temperature and host plant stress compared to their conspecific females and males from the other evolution regimes that applied fecundity selection. We quantified the population‐level consequences of this sex‐specific adaptation and found evidence that the cost of sociosexual interactions in terms of reduced offspring production was higher in the regime applying only sexual selection to males. Moreover, the cost tended to be more pronounced at the elevated temperature to which males from the regime were more robust compared to their conspecific females. These results illustrate the tension between individual‐level adaptation and population‐level viability in sexually reproducing species and suggest that the relative efficacies of sexual selection and fecundity selection can cause inherent sex differences in environmental robustness that may impact demography of maladapted populations.

Reproductive and productive seasonality of goats is modified with use of photoperiod and socio-sexual interactions

Reproductive and productive seasonality of goats is modified with use of photoperiod and socio-sexual interactions

Mice modulate ultrasonic calling bouts according to sociosexual context.

Mice produce various sounds within the ultrasonic range in social contexts. Although these sounds are often used as an index of sociability in biomedical research, their biological significance remains poorly understood. We previously showed that mice repeatedly produced calls in a sequence (i.e. calling bout), which can vary in their structure, such as Simple, Complex or Harmonics. In this study, we investigated the use of the three types of calling bouts in different sociosexual interactions, including both same- and opposite-sex contexts. In same-sex contexts, males typically produced a Simple calling bout, whereas females mostly produced a Complex one. By contrast, in the opposite-sex context, they produced all the three types of calling bouts, but the use of each calling type varied according to the progress and mode of sociosexual interaction (e.g. Harmonic calling bout was specifically produced during reproductive behaviour). These results indicate that mice change the structure of calling bout according to sociosexual contexts, suggesting the presence of multiple functional signals in their ultrasonic communication.

Dynamic corticostriatal activity biases social bonding in monogamous female prairie voles.

Summary paragraphAdult pair bonding involves dramatic changes in the perception and valuation of another individual1. One key change is that partners come to reliably activate the brain's reward system2-6, though the precise neural mechanisms by which partners become rewarding during sociosexual interactions leading to a bond remain unclear. Using a prairie vole model of social bonding7, we show how a functional circuit from medial prefrontal cortex (mPFC) to nucleus accumbens (NAcc) is dynamically modulated to enhance females' affiliative behavior towards a partner. Individual variation in the strength of this functional connectivity, particularly after the first mating encounter, predicts how quickly animals begin affiliative huddling with their partner. Rhythmically activating this circuit in a social context without mating biases later preference towards a partner, indicating that this circuit's activity is not just correlated with how quickly animals become affiliative but causally accelerates it. These results provide the first dynamic view of corticostriatal activity during bond formation, revealing how social interactions can recruit brain reward systems to drive changes in affiliative behavior.