The cooperative sex: Sexual interactions among female bonobos are linked to increases in oxytocin, proximity and coalitions.

In some species habitual same-sex sexual behavior co-occurs with high levels of intra-sexual alliance formation, suggesting that these behaviors may be linked. We tested for such a link by comparing behavioral and physiological outcomes of sex with unrelated same- and opposite-sex partners in female bonobos (Pan paniscus). We analyzed behavioral outcomes following 971 sexual events involving n = 19 female and n = 8 male adult and sub-adult members of a wild, habituated bonobo community. We additionally collected n = 143 urine samples before and after sexual interactions to non-invasively measure oxytocin (OT), which modulates female sexual behavior and facilitates cooperation in other species. The majority of sexual events (65%) consisted of female same-sex genito-genital rubbing (or GG-rubbing). Female dyads engaged in significantly more sexual interactions than did inter-sexual dyads, and females were more likely to remain within close proximity to their partners following GG-rubbing. Females also exhibited greater increases in urinary OT following GG-rubbing compared with copulations, indicating a physiological basis for increased motivation to cooperate among females. The frequency of coalitionary support among non-kin was positively predicted by the frequency of sexual interactions for female as well opposite-sex dyads, although coalitionary support tended to be more frequent among females. The emergence of habitual same-sex sexual behavior may have been an important step in the evolution of cooperation outside of kinship and pair-bonds in one of our closest phylogenetic relatives.

• Publication year

  2019

• Venue

  Hormones and Behavior

• Publication date

  2019-09-10

• Fields of study

  Biology, Medicine, Psychology

• Identifiers
  DOI 10.1016/j.yhbeh.2019.104581PMID 31449811
• External record

  Open on Semantic Scholar

• Source metadata

  Semantic Scholar, PubMed

• No claims are published for this paper.

• No concepts are published for this paper.

• The “tolerant chimpanzee”—towards the costs and benefits of sociality in female bonobos

  2018influential reference
• Homosexuality, Biosocial Theories of

  2018cited by this paper
• Sex-specific association patterns in bonobos and chimpanzees reflect species differences in cooperation

  2017cited by this paper
• Stable and fluctuating social preferences and implications for cooperation among female bonobos at LuiKotale, Salonga National Park, DRC.

  2017influential reference
• Male reproductive skew is higher in bonobos than chimpanzees.

  2017cited by this paper
• Hormonal systems, human social bonding, and affiliation

  2017cited by this paper
• Mixed messages: wild female bonobos show high variability in the timing of ovulation in relation to sexual swelling patterns

  2016cited by this paper
• A Comparison Between Bonobos and Chimpanzees: A Review and Update

  2016cited by this paper
• Do friends help each other? Patterns of female coalition formation in wild bonobos at Wamba

  2016influential reference
• Oxytocin reactivity during intergroup conflict in wild chimpanzees

  2016cited by this paper
• Food begging and sharing in wild bonobos (Pan paniscus): assessing relationship quality?

  2016cited by this paper
• Male dolphin alliances in Shark Bay: changing perspectives in a 30-year study

  2015cited by this paper
• Dispersing Primate Females

  2015cited by this paper
• Welcome Back: Responses of Female Bonobos (Pan paniscus) to Fusions

  2015cited by this paper
• Evolving the neuroendocrine physiology of human and primate cooperation and collective action

  2015cited by this paper
• Pointing and pantomime in wild apes? Female bonobos use referential and iconic gestures to request genito-genital rubbing

  2015cited by this paper
• Intergroup Transfer of Females and Social Relationships Between Immigrants and Residents in Bonobo (Pan paniscus) Societies

  2015cited by this paper
• Prolonged maximal sexual swelling in wild bonobos facilitates affiliative interactions between females

  2015cited by this paper
• Non-reciprocal but peaceful fruit sharing in wild bonobos in Wamba

  2015influential reference
• Fitting Linear Mixed-Effects Models Using lme4

  2014cited by this paper
• Food sharing is linked to urinary oxytocin levels and bonding in related and unrelated wild chimpanzees

  2014cited by this paper
• Primates and Cetaceans

  2014cited by this paper
• Endogenous peripheral oxytocin measures can give insight into the dynamics of social relationships: a review

  2014cited by this paper
• R: A language and environment for statistical computing.

  2014cited by this paper
• Non-conceptive Sexual Interactions in Monkeys, Apes, and Dolphins

  2014cited by this paper
• Homosexual behaviour increases male attractiveness to females

  2013cited by this paper
• Urinary oxytocin and social bonding in related and unrelated wild chimpanzees

  2013cited by this paper
• Monogamy, strongly bonded groups, and the evolution of human social structure

  2013cited by this paper
• Intersexual dominance relationships and the influence of leverage on the outcome of conflicts in wild bonobos (Pan paniscus)

  2013cited by this paper
• Oxytocin during the initial stages of romantic attachment: relations to couples' interactive reciprocity.

  2012cited by this paper
• Oxytocin modulates cooperation within and competition between groups: an integrative review and research agenda.

  2012cited by this paper
• The role of oxytocin in mating and pregnancy.

  2012cited by this paper
• Oxytocin, Feeding, and Satiety

  2012cited by this paper
• AD Model Builder: using automatic differentiation for statistical inference of highly parameterized complex nonlinear models

  2012cited by this paper
• Social tolerance in a despotic primate: co-feeding between consortship partners in rhesus macaques.

  2012cited by this paper
• Oxytocin and social affiliation in humans.

  2012influential reference
• A RFID-enabled leisure system for computer-illiterate elderly

  2011cited by this paper
• Post-Conflict Affiliation by Chimpanzees with Aggressors: Other-Oriented versus Selfish Political Strategy

  2011cited by this paper
• Mothers matter! Maternal support, dominance status and mating success in male bonobos (Pan paniscus)

  2011cited by this paper
• Yes, I Am Ready Now: Differential Effects of Paced versus Unpaced Mating on Anxiety and Central Oxytocin Release in Female Rats

  2011cited by this paper
• Female contributions to the peaceful nature of bonobo society

  2011cited by this paper
• Variation in oxytocin is related to variation in affiliative behavior in monogamous, pairbonded tamarins.

  2010cited by this paper
• An R Companion to Applied Regression

  2010cited by this paper
• Causes and consequences of maleemale courtship in fruit flies

  2010cited by this paper
• Characterization of the oxytocin system regulating affiliative behavior in female prairie voles.

  2009cited by this paper
• Dog's gaze at its owner increases owner's urinary oxytocin during social interaction.

  2009cited by this paper
• The relationship between socio‐sexual behavior and salivary cortisol in bonobos: tests of the tension regulation hypothesis

  2009cited by this paper
• Same-sex sexual behavior and evolution.

  2009cited by this paper
• Cooperation and competition in chimpanzees: Current understanding and future challenges

  2009cited by this paper
• Female feeding priority in bonobos, Pan paniscus, and the question of female dominance

  2007cited by this paper
• Sexual Reward via Vulvar, Perineal, and Anal Stimulation: A Proximate Mechanism for Female Homosexual Mounting in Japanese Macaques

  2006cited by this paper
• Social grease for females? Same sex genital contacts in wild bonobos

  2006cited by this paper
• Effects of Partner Support on Resting Oxytocin, Cortisol, Norepinephrine, and Blood Pressure Before and After Warm Partner Contact

  2005cited by this paper
• Hormones and history: The evolution and development of primate female sexuality

  2004cited by this paper
• Intra- and inter-sexual aggression by bonobos in the context of mating

  2003cited by this paper
• Lui Kotal - A new site for field research on bonobos in the Salonga National Park

  2003influential reference
• How bonobos handle hunts and harvests : Why share food?

  2002cited by this paper
• Same-Sex Sexual Partner Preference in Hormonally and Neurologically Unmanipulated Animals

  2002cited by this paper
• The Evolution of Human Homosexual Behavior1

  2000influential reference
• The Evolution of Homoerotic Behavior in Humans

  2000cited by this paper
• Use and function of genital contacts among female bonobos.

  2000cited by this paper
• The evolution of exaggerated sexual swellings in primates and the graded-signal hypothesis.

  1999cited by this paper
• Interventions and alliance formation between female Japanese macaques, Macaca fuscata, during homosexual consortships

  1996influential reference
• Relationships among cardiovascular, muscular, and oxytocin responses during human sexual activity

  1994cited by this paper
• The evolution of sexuality in chimpanzees and bonobos

  1993cited by this paper
• Social relationships between immigrant and resident bonobo (Pan paniscus) females at Wamba.

  1991influential reference
• Issues in Bonobo (Pan paniscus) Sexual Behavior

  1990cited by this paper
• Sociosexual Behavior Used for Tension Regulation in All Age and Sex Combinations Among Bonobos

  1990cited by this paper
• Sexual swelling, receptivity, and grouping of wild pygmy chimpanzee females at Wamba, Zaïre

  1987cited by this paper
• Clearance studies of oxytocin in humans using radioimmunoassay measurements of the hormone in plasma and urine.

  1987cited by this paper
• Tension regulation and nonreproductive functions of sex in captive bonobos pan paniscus

  1987influential reference
• Oxytocin release during coitus in male and female rabbits: effect of opiate receptor blockade with naloxone.

  1986cited by this paper
• The external genitalia of female pygmy chimpanzees

  1985cited by this paper
• Sexual Behavior of Pan paniscus under Natural Conditions in the Lomako Forest, Equateur, Zaire

  1984cited by this paper
• Social behavior of wild pygmy chimpanzees (Pan paniscus) of Wamba: A preliminary report☆

  1980cited by this paper

• SEX in bonobos: The intensity of sexual stimulation sharply drops after facial mimicry

  2026cites this paper
• Emotions mediate nonlinear phenomena production in the vocalizations of two ape species.

  2025cites this paper
• Investigating Changes in Social Networks Following Conflict in Zoo‐Housed Bonobos (Pan paniscus)

  2025cites this paper
• Collective Acoustics in Pan: Conserved Roots in the Evolution of Human Musicality

  2025cites this paper
• Oxytocin activity is not linked to out-group prosociality in wild bonobos

  2025influential citation
• Gender and its constellation of constructs: A theory of gender identity and how to reduce gender-ignorance and -phobias via gender-inclusive spaces

  2025cites this paper
• The Role of Oxytocin and Sex in Analgesic Placebo-Response: Exploratory Analysis from a Sham Randomized Clinical Trial in Chronic Back-Pain Patients

  2025cites this paper
• Self-Medication in Humans (Homo sapiens) and Bonobos (Pan paniscus) in the Democratic Republic of the Congo

  2025cites this paper
• Bonobos and chimpanzees overlap in sexual behaviour patterns during social tension

  2025cites this paper
• Same-sex sexual behavior in brown-headed spider monkeys (Ateles fusciceps fusciceps) during grappling between two subadult males

  2024cites this paper
• New perspectives on fighting violence against women

  2024cites this paper
• Conserved and differing functions of the endocrine system across different social systems – oxytocin as a case study

  2024cites this paper
• Hominin musical sound production: palaeoecological contexts and self domestication

  2024cites this paper
• Intense Body Contact Increases Homosexual Pair Bond Stability in Female Japanese Macaques (Macaca fuscata)

  2024cites this paper
• Peptides and primate personality: Central and peripheral oxytocin and vasopressin levels and social behavior in two baboon species (Papio hamadryas and Papio anubis).

  2024cites this paper
• Structural and Cognitive Mechanisms of Group Cohesion in Primates

  2024cites this paper
• Fertility of Czech Gay and Straight Men, Women, and Their Relatives: Testing the Sexually Antagonistic Gene Hypothesis

  2024cites this paper
• Primate Behavior and the Importance of Comparative Studies in Biological Anthropology.

  2024cites this paper
• From pathology to pleasure: Reframing mechanistic studies on same-sex sexual behavior in primates.

  2024cites this paper
• The evolution of same-sex sexual behaviour in mammals

  2023cites this paper
• Same-sex sociosexual behaviour is widespread and heritable in male rhesus macaques

  2023cites this paper
• Reproductive inequality among males in the genus Pan

  2023cites this paper
• Female age and reproductive stage influence copulation patterns in mountain gorillas’ variable mating system

  2023cites this paper
• Male–male relationships in chimpanzees and the evolution of human pair bonds

  2023cites this paper
• Cooperation increases bottlenose dolphins’ (Tursiops truncatus) social affiliation

  2023cites this paper
• Oxytocin increases during fur‐rubbing regardless of level of social contact in tufted capuchin monkeys

  2023influential citation
• More Than Just Kibbles: Keeper Familiarity and Food Can Affect Bonobo Behavior

  2023cites this paper
• Linked OXTR Variants Are Associated With Social Behavior Differences in Bonobos (Pan paniscus)

  2023cites this paper
• Maternal conflict intervention is more frequent in chimpanzee compared to bonobo development

  2023cites this paper
• The evolution of group-mindedness: comparative research on top-down and bottom-up group cooperation in bonobos and chimpanzees

  2022cites this paper
• A socio-ecological perspective on the gestural communication of great ape species, individuals, and social units

  2022cites this paper
• Yawn contagion in bonobos: Another group, another story

  2022cites this paper
• Do immigrant female bonobos prefer older resident females as important partners when integrating into a new group?

  2022cites this paper
• What are oxytocin assays measuring? Epitope mapping, metabolites, and comparisons of wildtype & knockout mouse urine

  2022cites this paper
• Is History the Same as Evolution? No. Is it Independent of Evolution? Certainly Not

  2022cites this paper
• Oxytocin promotes social proximity and decreases vigilance in groups of African lions

  2022cites this paper
• Parochial cooperation in wild chimpanzees: a model to explain the evolution of parochial altruism

  2022cites this paper
• Dominance or Tolerance? Causes and consequences of a period of increased intercommunity encounters among bonobos (Pan paniscus) at LuiKotale

  2022cites this paper
• Oxytocin promotes species-relevant outgroup attention in bonobos and chimpanzees.

  2022cites this paper
• The eco-evolutionary landscape of power relationships between males and females.

  2022cites this paper
• Human Females as a Dispersal-Egalitarian Species: A Hypothesis about Women and Status

  2022cites this paper
• Bared‐teeth displays in bonobos (Pan paniscus): An assessment of the power asymmetry hypothesis

  2022cites this paper
• Flexible signalling strategies by victims mediate post-conflict interactions in bonobos

  2022cites this paper
• Self-interest precludes prosocial juice provisioning in a free choice group experiment in bonobos

  2022cites this paper
• Female bonobos show social swelling by synchronizing their maximum swelling and increasing bonding

  2022cites this paper
• Partner choice in genito-genital rubbing among female bonobos (Pan paniscus) is highly dependent on physical proximity

  2022cites this paper
• Behavioral and physiological response to inequity in bonobos (Pan paniscus)

  2022cites this paper
• Testing the effect of oxytocin on social grooming in bonobos

  2021cites this paper
• Validation of a commercial enzyme immunoassay to assess urinary oxytocin in humans

  2021cites this paper
• Playful interactions and facial mimicry in infant bonobos (Pan paniscus)

  2021cites this paper
• The effects of female-male friendships on male postcopulatory levels of oxytocin and vasopressin, and sperm parameters in Macacaarctoides.

  2021cites this paper
• Sex and grooming as exchange commodities in female bonobos’ daily biological market

  2021cites this paper
• Attractiveness of female sexual signaling predicts differences in female grouping patterns between bonobos and chimpanzees

  2021cites this paper
• Assessing joint commitment as a process in great apes

  2021cites this paper
• Analytical and physiological validation of an enzyme immunoassay to measure oxytocin in dog, wolf, and human urine samples

  2021cites this paper
• Two wild female bonobos adopted infants from a different social group at Wamba

  2021cites this paper
• Prosociality and a Sociosexual Hypothesis for the Evolution of Same-Sex Attraction in Humans

  2020cites this paper
• Gregariousness, foraging effort, and affiliative interactions in lactating bonobos and chimpanzees.

  2020cites this paper
• Fellatio among male sanctuary-living chimpanzees during a period of social tension

  2020influential citation
• Divergent effects of oxytocin on eye contact in bonobos and chimpanzees.

  2020cites this paper
• Comparative analyses of the Pan lineage reveal selection on gene pathways associated with diet and sociality in bonobos

  2020cites this paper
• Mirror replication of sexual facial expressions increases the success of sexual contacts in bonobos

  2020cites this paper
• Look at me while having sex! Eye-to-eye contact affects homosexual behaviour in bonobo females

  2020cites this paper
• Foraging postures are a potential communicative signal in female bonobos

  2020cites this paper
• Oxytocin and Human Sexuality: Recent Developments

  2020cites this paper
• Oxytocin increases after affiliative interactions in male Barbary macaques

  2019cites this paper