Cited by 173Neuroendocrine regulation and behaviorAnimal Behavior and ReproductionEvolutionary Game Theory and Cooperation

Hormonal mechanisms of cooperative behaviour

Open access
Soares, Marta C., Bshary, Redouan, Fusani, Leonida, Goymann, Wolfgang, Hau, Michaela, Hirschenhauser, Katharina, Oliveira, Rui F.·2010·Philosophical Transactions of the Royal Society B: Biological Sciences

Abstract

Research on the diversity, evolution and stability of cooperative behaviour has generated a considerable body of work. As concepts simplify the real world, theoretical solutions are typically also simple. Real behaviour, in contrast, is often much more diverse. Such diversity, which is increasingly acknowledged to help in stabilizing cooperative outcomes, warrants detailed research about the proximate mechanisms underlying decision-making. Our aim here is to focus on the potential role of neuroendocrine mechanisms on the regulation of the expression of cooperative behaviour in vertebrates. We first provide a brief introduction into the neuroendocrine basis of social behaviour. We then evaluate how hormones may influence known cognitive modules that are involved in decision-making processes that may lead to cooperative behaviour. Based on this evaluation, we will discuss specific examples of how hormones may contribute to the variability of cooperative behaviour at three different levels: (i) within an individual; (ii) between individuals and (iii) between species. We hope that these ideas spur increased research on the behavioural endocrinology of cooperation.

AI snapshot

Written from the paper’s full text.

TL;DR

This review proposes that neuroendocrine mechanisms—especially sex steroids, stress hormones, and AVP/OT-family neuropeptides—may modulate cooperative behaviour by acting on cognitive building blocks and by generating variation within individuals, between individuals, and between species. It remains largely speculative because few studies directly link hormones to cooperation.

Key findings

  • Hormones are framed as modulators, not causes, of cooperative behaviour; they may affect prosociality, social recognition, bonding, assessment of social environment, social memory/learning, temporal discounting, and partner choice.
  • AVP/OT-family neuropeptides are repeatedly implicated: OT-knockout mice fail to recognize familiar individuals, and a single OT treatment before social interaction restores later recognition; intranasal OT increased money transfer in a trust game but had no effect on non-social risk-taking; AVP increased subjective threat perception to emotionally neutral faces.
  • Organizational and activational hormonal effects may shape cooperation: male Mongolian gerbils gestated between two female siblings show up to a 50% increase in alloparental care and lower aggression than males gestated between two male siblings; maternal care in rats alters stress responsiveness, brain organization, and social behaviour via glucocorticoid receptor demethylation.
  • Comparative data link AVP/OT systems to social variation: vole species differ in AVP V1a and OT receptor distributions by mating system, and estrildid finches differ in socially driven AVT neuron activation in the BNST between gregarious and territorial species.

Methods

  • Narrative review, not a primary empirical study; it synthesizes existing literature on neuroendocrine regulation of social behaviour in vertebrates.
  • Draws on examples from rodents, voles, birds, fish, and humans, with no systematic search or meta-analysis described.
  • Main analysis is conceptual: it identifies cognitive building blocks of cooperative behaviour and maps potential hormonal influences onto them, while noting that direct studies of hormones and cooperation are scarce.

Limitations

  • Stated: there is very little, if any, research on hormonal mechanisms in a cooperative context, so much of the review remains speculative; the focus on vertebrates reflects the authors’ expertise; neurotransmitter systems and central neuromodulators are excluded.
  • Evident: no systematic review protocol or quantitative synthesis is reported, and many inferences are extrapolated from general social behaviour rather than from cooperative behaviour itself.

Model-written summary. Check it against the paper before relying on it.

Integrity signals

Registry

Crossref · 10.1098/rstb.2010.0151

Cites

125 of 125 references verified0 citation errors · 0 not checkable

Statistics

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Claims the paper makes

0 of 116 cited sources checked · 0 supported · 0 flagged

  • Premisecitation

    Hormones help animals deal with complex real-life problems by acting as coordinators of behavioural, morphological and physiological outputs at both short- and long-term life-history scales.

    “hormones help animals to deal with complex real-life problems by acting as coordinators of behavioural, morphological and physiological outputs at both short-and long-term life-history scales”
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    • cites Adkins-Regan 2005

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  • Premisecitation

    In order to modulate the expression of behaviour, hormones have to modulate one or more of the sensory systems, the central nervous system, or the effector systems.

    “Thus, in order to modulate the expression of behaviour, hormones have to modulate one or more of these components”
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    • cites Nelson 2005

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    • cites Oliveira 2005

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  • Premisecitation

    Hormones should not be seen as deterministic factors but instead as modulators of behaviour that may increase or decrease the probability of the expression of a given behaviour by acting on the neural mechanisms underlying behaviour.

    “Therefore, hormones should not be seen as deterministic factors but instead as modulators of behaviour that may increase or decrease the probability of the expression of a given behaviour by acting on the neural mechanisms underlying behaviour”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Oliveira 2005

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  • Interpretationreasoning

    The influence of hormones is not simply unidirectional, but includes intrinsic feedbacks of social context and social behaviour on hormones.

    “the influence of hormones is not simply unidirectional, but includes intrinsic feedbacks of social context and social behaviour on hormones.”
    Quote in the paperSubstantial claim
  • Premisecitation

    Within a social network, an individual's androgen level modulates perceptive, motivational and cognitive mechanisms, which in turn influence future social behavioural efficiency.

    “within a social network, an individual's androgen level will modulate perceptive, motivational and cognitive mechanisms, that will in turn influence future social behavioural efficiency”
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    • cites Oliveira 2009

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    Premisereasoning

    Of the many different hormones present in vertebrates, three groups have received most attention in terms of their role in the expression of social behaviour: sex hormones, stress hormones and neuropeptides from the vasopressin/oxytocin family.

    “Of the many different hormones present in vertebrates, there are three groups that have received most attention in terms of their role in the expression of social behaviour: sex hormones, stress hormones and neuropeptides from the vasopressin (AVP)/oxytocin (OT) family”
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    Premisereasoning

    Social behaviour is naturally related with reproduction and to responses to emergencies or challenges.

    “social behaviour is naturally related with reproduction and to responses to emergencies or challenges”
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    Premisecitation

    Testosterone plays a pivotal role in the regulation of morphology, physiology and behaviour of male vertebrates.

    “testosterone, the principal steroid secreted by most vertebrate testes, which plays a pivotal role in the regulation of morphology, physiology and behaviour of male vertebrates”
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    • cites Wingfield et al. 2006

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    Premisenone given

    Both sex and stress hormones are organized in specific neuroendocrine axes, the HPG and HPA axes, both of which are organized in a hierarchical fashion.

    “Both sex and stress hormones are organized in specific neuroendocrine axes, the hypothalamicpituitary-gonadal (HPG) and the hypothalamicpituitary-adrenal (HPA) axes, both of which are organized in a hierarchical fashion.”
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    Premisecitation

    Functional effects of hormones are rapid and short-lived; structural effects are slow and long-lasting.

    “Functional effects are rapid and short-lived and can either result from a direct effect of hormones on neural excitability and neurotransmission”
    • Also stated in: § 2. A PRIMER TO THE NEUROENDOCRINE REGULATION OF SOCIAL BEHAVIOUR (a) Hormonal modulation of social behaviour · plain
      “Structural effects are slow and long-lasting”
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    • cites Remage-Healey & Bass 2006a

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    Interpretationnone given

    These behavioural traits are also likely to determine the tendency of an individual to show cooperative behaviour.

    “These behavioural traits are also likely to determine the tendency of an individual to show cooperative behaviour.”
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    Premisereasoning

    At the top of the HPG and HPA hierarchies are hypothalamic peptides that control the synthesis and release of specific tropic hormones in the anterior pituitary, which in turn regulate production of specific steroids in the gonads and adrenals.

    “At the top of the hierarchy are the hypothalamic peptides, i.e. gonadotropin-releasing hormone in the HPG and corticotropin-releasing hormone in the HPA, which control the synthesis and release of specific tropic hormones in the anterior pituitary”
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    Premisenone given

    Organizational effects of hormones are usually only effective at an early stage of life within strict time windows and are expected to last for the entire lifespan of the individual.

    “These latter effects are usually only effective at an early stage of life within strict time windows termed sensitive or critical periods, and are expected to last for the entire lifespan of the individual.”
    Quote in the paperNot a substantial claim
  • Classified as probably not a substantial claim.

    Premisenone given

    Behaviour is influenced by hormones.

    “Countless studies have convincingly demonstrated that behaviour is influenced by hormones.”
    Quote in the paperSubstantial claim
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    Premisenone given

    The posterior pituitary receives neural projections from hypothalamic neurons, which release neurohormones into the bloodstream.

    “the posterior pituitary receives neural projections from the hypothalamic neurons, which end in a capillary network, where the neurohormones produced by these neurons are released into the bloodstream.”
    Quote in the paperNot a substantial claim
  • Probably not a substantial claim: may not pass S4 (based). May combine two claims.

    Premisenone given

    Hormones have both activational and organizational influence on general social behaviour.

    “Hormones are likely to affect levels of helping in various ways as they have both activational and organizational influence on general social behaviour.”
    Quote in the paperNot a substantial claim
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    Premisecitation

    A single hormone may have effects on many different aspects of behaviour, which may depend on social context and the life-history stage.

    “A single hormone may have effects on many different aspects of behaviour, which may depend on social context and the life-history stage”
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    • cites Wingfield 2008

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    Premisecitation

    A hormone may have pleiotropic effects by affecting many different traits at the same time, thereby acting as the proximate mediator of functional trade-offs.

    “a hormone may also have pleiotropic effects by affecting many different traits at the same time, thereby acting as the proximate mediator of functional trade-offs”
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    • cites Lessells 2008

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    Premisenone given

    The modulatory action of hormones on the nervous system can occur at a functional level, by changing the activity of a given neural circuit, or at a structural level, by changing the architecture and/or connectivity of different nodes of the neural circuit.

    “The modulatory action of hormones on the nervous system can occur at a functional level, by changing the activity of a given neural circuit, or at a structural level, by changing the architecture and/or connectivity of different nodes of the neural circuit.”
    Quote in the paperNot a substantial claim
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    Premisecitation

    Hormones may modulate the expression of behaviour, but are not causes of behaviour.

    “Hormones may modulate the expression of behaviour, but are not causes of behaviour.”
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    • cites Nelson 2005

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    • cites Oliveira 2005

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    Premisecitation

    Androgens are behavioural facilitators by acting as modulators of neural pathways of social behaviour, while their concentrations may respond to social circumstances.

    “androgens are behavioural facilitators by acting as modulators of neural pathways of social behaviour, while in turn their concentrations may respond to social circumstances”
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    • cites Wingfield et al. 1990

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    • cites Oliveira 2004

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    • cites Goymann et al. 2007

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    Premisereasoning

    To ensure successful operation within the group, individual recognition and cooperation between individuals (e.g. pair partners or similar social alliances) may be essential.

    “To ensure successful operation within the group, individual recognition and cooperation between individuals (e.g.pair partners or similar social alliances) may be essential.”
    Quote in the paperNot a substantial claim
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    Premisecitation

    Steroid and neuropeptide receptors are present in different nodes of the social behaviour neural network, suggesting that plasticity in social behaviour is likely to be modulated by these hormones.

    “Steroid and neuropeptide (AVP, OT and their nonmammalian homologues) receptors are present in different nodes of this network, suggesting that plasticity in social behaviour is likely to be modulated by these hormones”
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    • cites Goodson 2005

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    Premisecitation

    Cleaner fish (Labroides dimidiatus) are able to distinguish between familiar and unfamiliar clients from the same client species, and prefer to interact with familiar ones.

    “cleaner fish (Labroides dimidiatus) are able to distinguish between familiar and unfamiliar clients from the same client species, and prefer to interact with familiar ones”
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    • cites Tebbich et al. 2002

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    Premisecitation

    According to this hypothesis, OT acting on hindbrain parasympathetic systems should stimulate prosocial behaviour, whereas AVP acting on sympathetic pathways should be associated with social withdrawal and/or aggression.

    “According to this hypothesis, OT acting on hindbrain parasympathetic systems should stimulate prosocial behaviour, whereas AVP acting on sympathetic pathways should be associated with social withdrawal and/or aggression.”
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    • cites Porges 2001

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    Premisenone given

    Proximate mechanisms are required that make an individual tolerate the presence of conspecifics, coordinate its actions to produce behaviour that reduces immediate pay-offs, recognize partners and assess their behaviour, and choose appropriate responses from the available behavioural repertoire.

    “proximate mechanisms are required that make an individual tolerate the presence of conspecifics, coordinate its actions to produce behaviour that reduces immediate pay-offs, recognize partners and assess their behaviour, and choose the appropriate responses from the available behavioural repertoire.”
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    Premisereasoning

    A first condition for the occurrence of cooperative behaviour is that individuals show a predisposition to approach conspecifics or other potential partners, and tolerate their presence.

    “A first condition for the occurrence of cooperative behaviour is that individuals show a predisposition to approach conspecifics or other potential partners, and tolerate their presence.”
    Quote in the paperNot a substantial claim
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    Premisereasoning

    This social behaviour neural network is seen as the core of the social brain but it is not its whole, since other brain areas are relevant for social behaviour.

    “This network is seen as the core of the social brain but it is certainly not its whole, since there are other brain areas that are quite relevant for social behaviour”
    Quote in the paperNot a substantial claim
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    Premisecitation

    Intranasal administration of OT improves the capacity to recognize faces but has no effect on memorization of non-social stimuli in humans.

    “Intranasal administration of OT improves the capacity to recognize faces, but has no effect on the memorization of non-social stimuli (Rimmele et al. 2009).”
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    • cites Rimmele et al. 2009

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    Premisecitation

    OT-knockout mice fail to show behaviours indicating recognition of familiar individuals despite normal olfaction and no generalized deficits in learning and memory.

    “OT-knockout mice are not olfactory impaired and show no generalized deficits in learning and memory, and yet they fail to show behaviours which would indicate that they recognize familiar individuals, even after repeated encounters (Ferguson et al. 2000).”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Ferguson et al. 2000

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    Premisenone given

    Social animals may take advantage of living in groups which are organized in complex social networks of related and unrelated individuals.

    “Social animals may take advantage of living in groups which are organized in complex social networks of related and unrelated individuals.”
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    Premisenone given

    Bonding mechanisms may be necessary to avoid aggression against partners.

    “Bonding mechanisms may be necessary to avoid aggression against partners.”
    Quote in the paperNot a substantial claim
  • Classified as probably not a substantial claim.

    Interpretationreasoning

    The tendency to approach a partner in a cooperative context must overcome the tendency for social withdrawal.

    “Therefore, the tendency to approach a partner in a cooperative context overcome the tendency for social withdrawal.”
    Quote in the paperSubstantial claim
  • Probably not a substantial claim: may not pass S4 (based). May combine two claims.

    Premisereasoning

    Bonding may be crucial for any individual's willingness to invest: by creating affection towards another individual, bonding may help to overcome the problem of objective reduction in immediate gains through cooperative behaviour.

    “Bonding may also be crucial for any individual's willingness to invest: by creating affection towards another individual, bonding may help to overcome the problem of objective reduction in immediate gains through cooperative behaviour.”
    Quote in the paperNot a substantial claim
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    Premisecitation

    In the goldfish (Carassius auratus), central infusions of AVT inhibit social approach, whereas the administration of an AVT antagonist or of IT stimulated social approach.

    “in the goldfish (Carassius auratus), central infusions of AVT inhibit social approach, whereas the administration of an AVT antagonist or of IT stimulated social approach”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Thompson & Walton 2004

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    Premisenone given

    Social recognition is necessary to distinguish between cooperators and cheaters or between partners and opponents.

    “Social recognition is necessary to distinguish between cooperators and cheaters or between partners and opponents.”
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    Premisecitation

    Simple (i.e. genetically coded) solutions may exist, for example if partners are sessile.

    “Simple (i.e.genetically coded) solutions may exist, for example if partners are sessile”
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    • cites Brosnan et al. 2010

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    Premisecitation

    The two cell types have different projections associated with differential function: magnocellular cells project to the posterior pituitary for peripheral effects, whereas parvocellular cells project to limbic areas for central effects on the brain.

    “the OT and AVP hypothalamic magnocellular cells project to the posterior pituitary and these pathways are responsible for peripheral systemic effects of these neuropeptides (e.g.AVP: anti-diuretic; OT: parturition and lactation); whereas the AVP and OT parvocellular cells project to limbic areas, including several of the nodes of the social behaviour neural network described above, and this system”
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    • cites De Vries & Panzica 2006

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    • cites Caldwell 2008b

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    Premisenone given

    In many vertebrate animals, the brain mechanisms described above allow individuals to more flexibly respond to environmental stimuli.

    “However, in many vertebrate animals, the brain mechanisms described above allow individuals to more flexibly respond to environmental stimuli.”
    Quote in the paperNot a substantial claim
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    Premisecitation

    AVP is involved in the formation of social memories, as shown by AVP-deficient Brattelboro rats having totally disrupted social recognition.

    “The involvement of AVP in the formation of social memories was originally illustrated by the finding of the AVP-deficient Brattelboro rat, which has a totally disrupted social recognition (Feifel et al. 2009).”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Feifel et al. 2009

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    Premisenone given

    Individual recognition or recognition of different classes of social partners is both the basis and the consequence of interactions with others, and requires consolidation of memory of past interactions and outcomes.

    “Individual recognition or recognition of different classes of social partners (e.g.cooperators versus noncooperators) is both the basis and the consequence of interactions with others, and requires consolidation of memory of past interactions and outcomes.”
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    Interpretationreasoning

    There is a continuum from neurocrine to endocrine communication, and hormonal and neural mechanisms are interconnected with multiple reciprocal effects.

    “In short, there is a continuum from neurocrine to endocrine communication, and hormonal and neural mechanisms are interconnected with multiple reciprocal effects.”
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    Interpretationnone given

    Both the perception of the partner's effort and the critical threshold that may cause a switch in behavioural responses can be affected by hormones.

    “Both the perception of the partner's effort and the critical threshold that may cause a switch in behavioural responses can be affected by hormones.”
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  • Probably not a substantial claim: may not pass S2 (checkable), S3 (load-bearing), S4 (based).

    Interpretationreasoning

    Considering the vast diversity of examples for cooperation, there likely exists an equal diversity of mechanisms that regulate cooperation.

    “Considering the vast diversity of examples for cooperation, there likely exists an equal diversity of mechanisms that regulate cooperation.”
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    Premisenone given

    Individuals may adjust their behaviour depending on how a partner has behaved in the past, especially if these previous interactions were risky or involved cheating.

    “Individuals may adjust their behaviour depending on how a partner has behaved in the past, especially if these previous interactions were risky or involved cheating.”
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    Premisecitation

    The biological market paradigm is linked to communication and negotiation.

    “This biological market paradigm (Noe ¨2001) is linked to communication and negotiation.”
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    • cites Noe ¨2001

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    Premisereasoning

    Bystanders may gain information about interacting partners and may adjust their future behaviour with these partners depending on their observations.

    “Bystanders may gain information about interacting partners and may adjust their future behaviour with these partners depending on their observations.”
    Quote in the paperNot a substantial claim
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    Premisecitation

    A set of brain areas in the basal forebrain and midbrain are involved in the regulation of multiple forms of social behaviour and have bidirectional connections between each pair.

    “A set of brain areas in the basal forebrain and midbrain have been identified as being involved in the regulation of multiple forms of social behaviour (aggression, affiliation, bonding, parental behaviour, social stress) and to have bidirectional connections between each pair”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites Newman 1999

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    • cites Goodson 2005

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    Premisenone given

    Neurotransmitters and neuromodulators are also known to modulate behavioural expression.

    “Neurotransmitters and neuromodulators are also known to modulate behavioural expression.”
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    Premisecitation

    It has been hypothesized that AVP and OT may influence basic emotional mechanisms that regulate social approach and social aversion.

    “It has been hypothesized that AVP and OT may influence basic emotional mechanisms that regulate social approach and social aversion”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Porges 2001

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  • Probably not a substantial claim: may not pass S4 (based). May combine two claims.

    Premisenone given

    Hormones are known to affect and be affected by components of cooperative behaviour.

    “Hormones are known to affect and be affected by the following components of cooperative behaviour.”
    Quote in the paperNot a substantial claim
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    Premisecitation

    Newman originally proposed the existence of this social behaviour neural network in mammals, and Goodson confirmed its presence across different vertebrate classes and identified putative homologous areas.

    “Newman (1999) originally proposed the existence of this social behaviour neural network in mammals, and Goodson (2005) confirmed its presence across different vertebrate classes and identified the putative homologous areas for each node in the different classes and/or taxa.”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites Newman 1999

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    • cites Goodson 2005

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    Premisenone given

    Steroid hormones modulate the synthesis of neuropeptides and their receptors and therefore may also exert their effects indirectly through the AVP/OT neuromodulatory system.

    “steroid hormones are also known to modulate the synthesis of neuropeptides and their receptors and therefore may also exert their effects indirectly through the AVP/OT neuromodulatory system.”
    Quote in the paperNot a substantial claim
  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Interpretationreasoning

    All of these hormonal effects may occur in different compartments of the neural circuits underlying behaviour, thereby affecting the perception, the valence and the salience of social interactions.

    “All of these may occur in different compartments of the neural circuits underlying behaviour (input, central processing, output), therefore affecting the perception, the valence and the salience of social interactions.”
    Quote in the paperNot a substantial claim
  • Probably not a substantial claim: may not pass S3 (load-bearing), S4 (based). May combine two claims.

    Premisereasoning

    Flexible behavioural responses require neural plasticity, which can be achieved by the chemical modulation of neural circuits at various levels.

    “flexible behavioural responses require neural plasticity, which can be achieved by the chemical modulation of neural circuits at various levels.”
    Quote in the paperNot a substantial claim
  • May combine two claims.

    Premisecitation

    OT is important for mate recognition and pair bond formation in monogamous voles.

    “In monogamous voles, OT is important for mate recognition and pair bond formation (Young & Wang 2004).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Young & Wang 2004

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    Premisecitation

    The hippocampus is a brain area involved in relational memory processing and episodic memory.

    “a brain area involved in relational memory processing and episodic memory (Squire 1992;Eichenbaum et al. 1999)”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites Squire 1992

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    • cites Eichenbaum et al. 1999

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    Interpretationreasoning

    OT increases trust by reducing amygdala activation and concomitantly anxiety states associated with the possibility of non-reciprocation.

    “Thus, OT seems to increase trust by reducing amygdala activation and concomitantly anxiety states associated with the possibility of non-reciprocation.”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Interpretationreasoning

    The ability to remember specific aspects of past social encounters (episodic memory) would allow individuals to reciprocate cooperative behaviour and to punish non-cooperators.

    “the ability to remember specific aspects of past social encounters, such as a relative place in time and space, associated emotions and other contextual knowledge (i.e.episodic memory) would allow individuals to reciprocate cooperative behaviour and to punish non-cooperators.”
    Quote in the paperNot a substantial claim
  • May combine two claims.

    Interpretationnone given

    Species with different life histories will differ both with respect to organizational and activational effects of hormones, which may also promote or hinder the expression of cooperative behaviour.

    “Third, species with different life histories will differ both with respect to organizational and activational effects of hormones, which may also promote or hinder the expression of cooperative behaviour.”
    Quote in the paperNot a substantial claim
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    Premisecitation

    AVP V1b receptor knockout mice display impaired social memory, despite having normal olfactory ability and other memory functions (e.g. spatial memory).

    “AVP V1b receptor knockout mice also display impaired social memory, despite having normal olfactory ability and other memory functions (e.g.spatial memory; Wersinger et al. 2004).”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Wersinger et al. 2004

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  • Classified as probably not a substantial claim. May combine two claims.

    Interpretationreasoning

    Hormones may affect the basic mood of an individual, which in turn may influence neuronal decisions.

    “Hormones may affect the basic mood of an individual, which in turn may influence neuronal decisions.”
    Quote in the paperSubstantial claim
  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    The existence of episodic memory in animals is still a matter of debate.

    “The existence of episodic memory in animals is still a matter of debate (Clayton et al. 2003;Suddendorf & Busby 2003;Roberts et al. 2008).”
    Quote in the paperNot a substantial claim0 of 3 sources checked
    • cites Clayton et al. 2003

      Not checked in the free run.

    • cites Suddendorf & Busby 2003

      Not checked in the free run.

    • cites Roberts et al. 2008

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Male Mongolian gerbils situated during gestation between two female siblings show up to a 50 per cent increase in alloparental care and lower rates of aggressive behaviour when compared with males situated between two male siblings during gestation.

    “male Mongolian gerbils (Meriones unguiculatus) situated during gestation between two female siblings show up to a 50 per cent increase in alloparental care (to offspring that are not their own) and lower rates of aggressive behaviour when compared with males situated between two male siblings during gestation (Clark & Galef 1998, 2000).”
    Quote in the paperSubstantial claim0 of 2 sources checked
    • cites Clark & Galef 1998

      Not checked in the free run.

    • cites Clark & Galef 2000

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Intranasal OT administration increases money transfer by investors in a trust game but has no effect on risk-taking in a non-social context.

    “intranasal OT administration increased money transfer by investors in a trust game, but had no effect in risk-taking in a non-social context (Kosfeld et al. 2005).”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Kosfeld et al. 2005

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    OT increases trusting behaviour and decreases amygdala activation during a trust game.

    “OT increased trusting behaviour and decreased amygdala activation during a trust game (Baumgartner et al. 2008).”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Baumgartner et al. 2008

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing), S4 (based).

    Premisereasoning

    The formation and maintenance of pairs is a good example of cooperation between two unrelated individuals, as both may benefit from tolerating and supporting each other.

    “The formation and maintenance of pairs is a good example of cooperation between two unrelated individuals, as both may benefit from tolerating and supporting each other.”
    Quote in the paperNot a substantial claim
  • May combine two claims.

    Premisecitation

    OT- and AVP-releasing neurons project into the midbrain and exert an influence on the mesolimbic dopaminergic reward pathway.

    “OT-and AVPreleasing neurons project into the midbrain and exert an influence on the mesolimbic dopaminergic reward pathway (reviewed in Skuse & Gallagher 2009).”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Skuse & Gallagher 2009

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Hormones may work through organizational effects during ontogeny, which may cause differentiation between individuals with respect to growth, strength and personality, and which in turn may lead to consistent differences between individuals with respect to behaviour, including levels of cooperation.

    “First, hormones may work through organizational effects during ontogeny, which may cause differentiation between individuals with respect to growth, strength and personality, and which in turn may lead to consistent differences between individuals with respect to behaviour; including levels of cooperation (see Bergmuller et al. 2010).”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Bergmuller et al. 2010

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Premisecitation

    The amygdala is a danger detection centre activated when a potential threat is detected.

    “The amygdala has been viewed as a danger detection centre in the brain, which is activated when a potential threat is detected in the environment (LeDoux 2007).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites LeDoux 2007

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    In prairie voles, a single injection of OT on the day of birth affects aggressive behaviour and male alloparenting rates.

    “In prairie voles, a single injection of OT on the day of birth affects aggressive behaviour (Carter 2003) and male alloparenting rates (Bales et al. 2004).”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites Carter 2003

      Not checked in the free run.

    • cites Bales et al. 2004

      Not checked in the free run.

  • May combine two claims.

    Premisereasoning

    Both sex steroids (in particular oestrogens) and glucocorticoids modulate learning and memory processes.

    “both sex steroids (in particular oestrogens) and glucocorticoids modulate learning and memory processes.”
    Quote in the paperNot a substantial claim
  • Probably not a substantial claim: may not pass S4 (based).

    Premisenone given

    Hormones can influence learning processes.

    “Hormones can influence learning processes.”
    Quote in the paperNot a substantial claim
  • May combine two claims.

    Premisenone given

    These effects are mediated by stress hormones, the secretion of which is increased after the separation of the mother from her offspring and decreased again when she is allowed to lick and groom her offspring intensively after the separation.

    “These effects are mediated by stress hormones, the secretion of which is increased after the separation of the mother from her offspring and decreased again when she is allowed to lick and groom her offspring intensively after the separation.”
    Quote in the paperSubstantial claim
  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Interpretationreasoning

    Hormones may be involved in other learning and memory tasks relevant for the expression of cooperative behaviour.

    “Hormones may also be involved in other learning and memory tasks relevant for the expression of cooperative behaviour.”
    Quote in the paperNot a substantial claim
  • May combine two claims.

    Premisecitation

    Patients with lesions of the amygdala fail to recognize fearful faces and display behavioural disinhibition.

    “patients with lesions of the amygdala fail to recognize fearful faces and display behavioural disinhibition (Adolphs et al. 2005).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Adolphs et al. 2005

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S4 (based). May combine two claims.

    Premisenone given

    Unlike neuronal signals, hormones target areas of the brain rather than specific post-synaptic cells, or may reach the entire body, thus influencing systemic adjustments.

    “Unlike neuronal signals, hormones target areas of the brain rather than specific post-synaptic cells, or may reach the entire body, thus influencing systemic adjustments.”
    Quote in the paperNot a substantial claim
  • May combine two claims.

    Premisecitation

    Administration of AVP soon after birth increases aggressive behaviour in adult male prairie voles and changes risk-taking and social behaviour in rats.

    “administration of AVP soon after birth increases aggressive behaviour in adult male prairie voles (Stribley & Carter 1999) and changes risk-taking and social behaviour in rats (Boer et al. 1994).”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites Stribley & Carter 1999

      Not checked in the free run.

    • cites Boer et al. 1994

      Not checked in the free run.

  • Classified as probably not a substantial claim.

    Premisecitation

    In the 'finite state machine theory', Jacobs & Wingfield (2000) explain why different hormones may be linked to the same behaviour during different life-history stages.

    “In the 'finite state machine theory', Jacobs & Wingfield (2000) explain why different hormones may be linked to the same behaviour during different life-history stages.”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Jacobs & Wingfield 2000

      Not checked in the free run.

  • May combine two claims.

    Interpretationreasoning

    Year-round cooperative behaviours may be hard-wired by neuronal pathways instead or influenced by hormones only during ontogeny (i.e. organizational effects).

    “Year-round cooperative behaviours may be hard-wired by neuronal pathways instead or influenced by hormones only during ontogeny (i.e.organizational effects).”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Premisecitation

    In cooperatively breeding meerkats, glucocorticoids have a positive effect on pup feeding by helpers; helpers with higher glucocorticoid levels provided more food to pups than helpers with low glucocorticoid levels.

    “Glucocorticoids also have a positive effect on pup feeding by helpers in cooperatively breeding meerkats (Carlson et al. 2006a).”
    • Also stated in: § (a) Organizational effects of hormones and levels of cooperation · plain
      “Helpers with higher glucocorticoid levels provided more food to pups than helpers with low glucocorticoid levels.”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Carlson et al. 2006a

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Changes in baseline corticosteroid levels affect social behaviour in various ways, including enhancing foraging, food intake, attention, alertness, and affectionate interactions with infants.

    “These changes in baseline levels are known to affect social behaviour in various ways, i.e. by enhancing foraging, food intake (Koch et al. 2002), attention levels and alertness (Chapotot et al. 1998), and also affectionate interactions with infants (Fleming et al. 1997).”
    Quote in the paperSubstantial claim0 of 3 sources checked
    • cites Koch et al. 2002

      Not checked in the free run.

    • cites Chapotot et al. 1998

      Not checked in the free run.

    • cites Fleming et al. 1997

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Premisecitation

    Major hormones acting on social behaviour in vertebrates include sex steroids, stress steroids, and neurohormones.

    “Major hormones acting on social behaviour in vertebrates (adapted from Adkins-Regan 2005).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Adkins-Regan 2005

      Not checked in the free run.

  • May combine two claims.

    Interpretationreasoning

    Males can be expected to be particularly self-centred during this life-history stage and hence less cooperative.

    “males can be expected to be particularly self-centred during this life-history stage and hence less cooperative.”
    Quote in the paperSubstantial claim
    • Rests on an assumption: In males, an increase in testosterone prepares the individual for breeding: the size of the gonads increases and sperm production starts, and secondary sexual traits may develop.
    • Rests on an assumption: At the behavioural level, the increase in testosterone levels prepares males to display territorial behaviour, courtship and mating.
  • May combine two claims.

    Premisecitation

    Both AVP and OT are involved in pair-bond formation in both sexes, with males being more sensitive to AVP, and females to OT.

    “Although it was initially thought that AVP and OT would have sex-specific roles in pair-bonding, recent evidence demonstrates that both neuropeptides are involved in pair-bond formation in both sexes, with males being more sensitive to AVP, and females to OT (Young et al. 2008a,b).”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Young et al. 2008a,b

      Not checked in the free run.

  • May combine two claims.

    Interpretationreasoning

    These results reveal a mechanism that allows gregarious species to accentuate the positive valence of social stimuli during social interactions, therefore promoting prosocial behaviour.

    “These results reveal a mechanism that allows gregarious species to accentuate the positive valence of social stimuli during social interactions, therefore promoting prosocial behaviour.”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Premisecitation

    Brain administration of a V1a receptor or an OT receptor antagonist prevented mating, but induced partner preference formation, whereas the administration of AVP induced partner preference even without mating.

    “Brain administration of a V1a receptor or an OT receptor antagonist prevented mating, but induced partner preference formation, whereas the administration of AVP induced partner preference even without mating (e.g.Winslow et al. 1993;Williams et al. 1994;Lim et al. 2004).”
    Quote in the paperSubstantial claim0 of 3 sources checked
    • cites Winslow et al. 1993

      Not checked in the free run.

    • cites Williams et al. 1994

      Not checked in the free run.

    • cites Lim et al. 2004

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S4 (based).

    Interpretationnone given

    Changes in the weight of each node and in the strength of the connection between each pair of nodes in the brain social behaviour network correlate with behavioural changes within and between species.

    “Changes in the weight of each node and in the strength of the connection between each pair of them correlate with behavioural changes within and between species.”
    Quote in the paperNot a substantial claim
  • May combine two claims.

    Premisecitation

    Comparative studies of central AVP and OT systems in the vole brain have revealed a conserved pattern of distribution for AVP and OT, but an otherwise divergent pattern between monogamous and promiscuous vole species in terms of distribution of their receptors.

    “Comparative studies of central AVP and OT systems in the vole brain have revealed a conserved pattern of distribution for AVP and OT, but an otherwise divergent pattern between monogamous and promiscuous vole species in terms of distribution of their receptors (see Young et al. (2008a,b) for a recent review).”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Young et al. 2008a,b

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    These differences are associated with the type of social organization and are not necessarily species-specific, since both monogamous prairie and pine voles share a similar pattern of AVP V1a receptor and OT receptor labelling in the brain, whereas promiscuous montane and meadow voles show a different pattern.

    “These differences are associated with the type of social organization and are not necessarily species-specific, since both monogamous prairie and pine voles share a similar pattern of AVP V1a receptor and OT receptor labelling in the brain, whereas promiscuous montane and meadow voles show a different pattern (Young et al. 2008a,b).”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Young et al. 2008a,b

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    In male meerkat helpers, prolactin has an effect on helping behaviour; elevated prolactin levels immediately preceded decisions to babysit.

    “In male meerkat helpers, Carlson et al. (2006b) also found an effect of prolactin on helping behaviour.”
    • Also stated in: § (a) Organizational effects of hormones and levels of cooperation · plain
      “Elevated prolactin levels immediately preceded decisions to babysit.”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Carlson et al. 2006b

      Not checked in the free run.

86 of 86
  • The paper relies on this without support.

    Only a few studies have tried to specifically establish a link between hormones and cooperative behaviour.

    “However, only a few studies have tried to specifically establish a link between hormones and cooperative behaviour.”
  • The paper relies on this without support.

    Social and/or individual recognition allows animals to establish preferential relationships with chosen individuals within their social groups.

    “Social and/or individual recognition allows animals to establish preferential relationships with chosen individuals within their social groups.”
  • The paper relies on this without support.

    The emergence of social bonds depends on the expression of preferences associated with specific individuals (and not others).

    “The emergence of social bonds depends on the expression of preferences associated with specific individuals (and not others), which underlies the emergence of different types of social behaviour, such as parental care and pairbonding”
  • The paper relies on this without support.

    Different vole species show marked interspecific differences in social attachment despite close phylogenetic relationship.

    “Different vole species have been used in comparative studies of pair-bonding mechanisms which show marked interspecific differences in terms of social attachment (which is reflected in their mating system) despite their close phylogenetic relationship.”
  • The paper relies on this without support.

    Cooperation between pair partners is particularly relevant for maintaining the pairbond, at least in long-term monogamous species.

    “Cooperation between pair partners is particularly relevant for maintaining the pairbond, at least in long-term monogamous species.”
  • The paper relies on this without support.

    The maintenance of a pairbond is the result of bilateral interactions between pair partners and multilateral interactions between the pair and its social environment.

    “The maintenance of a pairbond is the result of 'bilateral' interactions between pair partners and of 'multilateral' interactions between the pair and its social environment.”
  • The paper relies on this without support.

    In birds and mammals, female testosterone is related to sexual motivation and fecundity.

    “In birds and mammals, female testosterone is related to sexual motivation and fecundity.”
  • The paper relies on this without support.

    In males of all vertebrate taxa, testosterone regulates and responds to sexual and/or agonistic interactions.

    “In males of all vertebrate taxa, testosterone regulates and responds to sexual and/or agonistic interactions.”
  • The paper relies on this without support.

    Animals must assess the valence and salience of social stimuli in their environment.

    “Animals must assess the valence (positive versus negative) and salience (high versus low) of social stimuli in their environment.”
  • The paper relies on this without support.

    Two brain systems are critical for the attribution of valence to social stimuli: the amygdaloid complex and the basal forebrain rewarding system.

    “Two brain systems are critical for the attribution of valence to social stimuli: the amygdaloid complex and the basal forebrain rewarding system.”
  • The paper relies on this without support.

    Social interactions can be rewarding and lead to further interactions with the same partner.

    “Social interactions can be rewarding and lead to further interactions with the same partner.”
  • The paper relies on this without support.

    OT is involved in social recognition in ewes.

    “Besides laboratory rodents, the involvement of OT in social recognition has been shown in ewes and in monogamous prairie voles.”
  • The paper relies on this without support.

    Cooperation and conflict are often based on individual recognition and memory of the partner or opponent.

    “cooperation and conflict are often based on individual recognition and memory of the partner or opponent”
  • The paper relies on this without support.

    The decrease in circulating oestrogen in the menopause brings about cognitive deficits, which include reduced capacity for spatial learning.

    “the decrease in circulating oestrogen in the menopause brings about cognitive deficits, which include reduced capacity for spatial learning”
  • The paper relies on this without support.

    Environmental conditions change in a predictable fashion across the seasons in long-lived species and in particular those inhabiting arctic and temperate climates.

    “environmental conditions change in a predictable fashion across the seasons”
  • The paper relies on this without support.

    Species have adapted to these changes by adjusting their life history: specific times of the year are used for specific activities.

    “Species have adapted to these changes by adjusting their life history: specific times of the year are used for specific activities.”
  • The paper relies on this without support.

    Spring and summer are typically used for reproduction.

    “spring and summer are typically used for reproduction”
  • The paper relies on this without support.

    In males, an increase in testosterone prepares the individual for breeding: the size of the gonads increases and sperm production starts, and secondary sexual traits may develop.

    “In males, an increase in testosterone prepares the individual for breeding: the size of the gonads increases and sperm production starts, and secondary sexual traits may develop.”
  • The paper relies on this without support.

    At the behavioural level, the increase in testosterone levels prepares males to display territorial behaviour, courtship and mating.

    “At the behavioural level, the increase in testosterone levels prepares males to display territorial behaviour, courtship and mating.”
  • The paper relies on this without support.

    Corticosteroids prepare animals for energy-demanding periods.

    “Corticosteroids prepare animals for energydemanding periods.”
  • The paper relies on this without support.

    In many vertebrates, baseline levels of corticosteroids are higher during the breeding season than during the rest of the year.

    “In many vertebrates, baseline levels of corticosteroids are higher during the breeding season than during the rest of the year.”
  • The paper relies on this without support.

    The effects of glucocorticoid concentrations are usually nonlinear.

    “However, it is important to emphasize that the effects of glucocorticoid concentrations are usually nonlinear.”
  • The paper relies on this without support.

    There is very little, if any, research on hormonal mechanisms in a cooperative context.

    “Because there is very little, if any, research on these hormonal mechanisms in a cooperative context, most of what we have developed was based on knowledge about the role of hormones in general social behaviour.”
  • The paper relies on this without support.

    Most hormones act within minutes.

    “Furthermore, the time-course of cooperative behaviour may be important: most hormones act within minutes.”
24 of 24

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • Sharers may experience a mutual increase in positive attitude, resulting in the promotion of stronger social bonds and longer-term benefits of more frequent cooperation.

    “Also, as oxytocin is thought to act on positive feedback circuits [16,17,21], sharers may experience a mutual increase in positive attitude [15,79,80], resulting in the promotion of stronger social bonds and longer-term benefits of more frequent cooperation [23,26,80].”
  • An additional major source of variation in oxytocin reactivity to certain social contexts and across individuals is likely related to interactions between the oxytocinergic system and other hormonal and neurotransmitter systems.

    “An additional major source of variation in oxytocin reactivity to certain social contexts and across individuals is likely related to interactions between the oxytocinergic system and other hormonal and neurotransmitter systems (for reviews see Heinrichs et al., 2009; Soares et al., 2010; Neumann and Landgraf, 2012), such as with cortisol (see Szczepanska-Sadowska, 2008; Heinrichs et al., 2009),”

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

Each contradiction between two passages listed here was confirmed by an independent check.

  • Vole review citation includes a meerkat paper

    Minor

    The text cites Young et al. (2008a,b) as a review of vole AVP and OT systems, but the listed 2008a paper concerns physiological suppression in female meerkats, not voles.

1 of 1

Cites

Flagged first, then by citations

Research works printed but not linked: 3

  1. Adkins-Regan E., 2005, Hormones and social behavior
  2. Bshary R., Short term stress increases the level of cooperation in the cleaner wrasse Labroides dimidiatus, Behav. Ecol. Sociobiol.
  3. Wingfield J. C., 2006, Biology of aggression, 179

Cited by

Sorted by citations

Authors
Soares, M. C., Bshary, R., Fusani, L., Goymann, W., Hau, M., Hirschenhauser, K., & Oliveira, R. F.
Affiliations
  • University of Neuchâtel (CH)
  • University of Ferrara (IT)
  • Max Planck Society (DE)
  • Instituto Gulbenkian de Ciência (PT)
Corresponding author
Soares, Marta C.
Venue
Philosophical Transactions of the Royal Society B: Biological Sciences
Published
2010-09-12
Volume
365
Issue
1553
Pages
2737-2750
ISSN
  • 0962-8436 (ISSN-L)
  • 1471-2970
OpenAlex
W2158110613
Cited by
173
References
125
Citations by year
2026: 2 · 2025: 4 · 2024: 10 · 2023: 7 · 2022: 8 · 2021: 10 · 2020: 14 · 2019: 18 · 2018: 12 · 2017: 20 · 2016: 10 · 2015: 16 · 2014: 10 · 2013: 8 · 2012: 11
FWCI
1.28
Type
journal article
Language
en
Open access
Locations
  • Philosophical Transactions of the Royal Society B Biological Sciences (publishedVersion)
  • Europe PMC (PubMed Central) (publishedVersion)
  • PubMed Central (publishedVersion)
  • PubMed (publishedVersion)
  • MPG.PuRe (Max Planck Society) (submittedVersion)
  • Portuguese National Funding Agency for Science, Research and Technology (RCAAP Project by FCT) (submittedVersion, other-oa)
  • Institutional Research Information System University of Ferrara (University of Ferrara) (submittedVersion)
Funders
  • National Science Foundation
  • Alexander von Humboldt-Stiftung
  • Max-Planck-Gesellschaft
  • Fundação para a Ciência e a Tecnologia
Topics
  • Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
  • Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Animal Behavior and Reproduction
  • Social Sciences › Sociology and Political Science › Evolutionary Game Theory and Cooperation
Keywords
cooperative behavior, neuroendocrine regulation, social behavior, decision-making, behavioral diversity, evolution of cooperation, vertebrates
MeSH terms
Altruism, Animals, Behavior, Animal, Cooperative Behavior, Neurosecretory Systems

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Claims read by deepseek-v4.1-flash under definition version 3 (extract-v3) on 2026-10-09.

Classified by jev-1.13-20260917 (gold-guideline-v0.2) on 2026-10-09.

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