No full-text available
To read the full-text of this research,
you can request a copy directly from the authors.
Primate Reciprocity and Its Cognitive Requirements
Abstract
Humans can engage in relatively indiscriminate altruistic behaviors such as donating money to charities, giving blood, and volunteering to review scientific papers. They also live in societies characterized by examples of cooperation of unmatched complexity, such as organized armies, the cooperative building of infrastructures such as roads and railways, and tax-paying, among others. (We exclude, of course, the “anonymous” societies of some social insects in which the animals themselves are not aware of the cooperative roles they play.) The emphasis on these unique aspects of our behavior1 has sometimes distracted scientists from paying attention to the more common aspects of our daily lives, which share characteristics with those of our fellow primates. We invite friends for dinner, console others after a loss, intervene in ongoing fights, and even groom others.2–4 These small acts of altruism, which constitute a large part of our daily social life, tend to resemble those of nonhuman primates.
... This type of 'titfor-tat' reciprocity is recorded in highly social animals who can be altruistic to close peers, including coyotes (Canis latrans) (Romero and Aureli 2008), rats (Dolivo, Rutte, and Taborsky 2016) and vampire bats (member of the subfamily Desmodontinae) (Carter and Wilkinson 2015), and is particularly common in primates, as in 'tit-for-tat' grooming, for example. Favours can be remembered for several months in chimpanzees (Schino and Aureli 2010), for whom such helping, whilst limited to 'low-cost' effort, includes not only sharing food or helping instrumentally (to achieve a goal) but also in taking risks to help out others in conflicts (Engelmann, Herrmann, and Tomasello 2015). Favours need not be explicitly remembered as discrete events but rather as a pervasive influence reflecting how each partner feels about (and feels sympathy towards and wishes to help) the other. ...
... We do share a certain sensitivity to others' motivations with many highly social animals. Chimpanzees, for example, can remember favours that have been done to them for at least six months (Schino and Aureli 2010). Domestic dogs make judgements about people who have either helped or refused to help their owners, and will not accept food from the latter (Chijiiwa et al. 2015). ...
... iewing the Face of Their Female Partner. ' Proceedings of the National Academy of Sciences of the United States of America 110 (50): 20308-13.Schino, Gabriele, and Filippo Aureli. 2010. 'Primate Reciprocity and Its Cognitive Requirements. ' Evolutionary Anthropology 19 (4): 130-35. Smaldino, Paul E., Lesley Newson, Jeffrey C. Schank, and Peter J. Richerson. 2013. 'Simulating the Evolution of the Human Family: Cooperative Breeding Increases in Harsh Environments. ' PLoS One 8 (11): e80753. Smith, Adam S., Anders Agmo, ...
In Hidden Depths, Professor Penny Spikins explores how our emotional connections have shaped human ancestry. Focusing on three key transitions in human origins, Professor Spikins explains how the emotional capacities of our early ancestors evolved in response to ecological changes, much like similar changes in other social mammals. For each transition, dedicated chapters examine evolutionary pressures, responses in changes in human emotional capacities and the archaeological evidence for human social behaviours. Starting from our earliest origins, in Part One, Professor Spikins explores how after two million years ago, movement of human ancestors into a new ecological niche drove new types of collaboration, including care for vulnerable members of the group. Emotional adaptations lead to cognitive changes, as new connections based on compassion, generosity, trust and inclusion also changed our relationship to material things. Part Two explores a later key transition in human emotional capacities occurring after 300,000 years ago. At this time changes in social tolerance allowed ancestors of our own species to further reach out beyond their local group and care about distant allies, making human communities resilient to environmental changes. An increasingly close relationship to animals, and even to cherished possessions, appeared at this time, and can be explained through new human vulnerabilities and ways of seeking comfort and belonging. Lastly, Part Three focuses on the contrasts in emotional dispositions arising between ourselves and our close cousins, the Neanderthals. Neanderthals are revealed as equally caring yet emotionally different humans, who might, if things had been different, have been in our place today. This new narrative breaks away from traditional views of human evolution as exceptional or as a linear progression towards a more perfect form. Instead, our evolutionary history is situated within similar processes occurring in other mammals, and explained as one in which emotions, rather than ‘intellect’, were key to our evolutionary journey. Moreover, changes in emotional capacities and dispositions are seen as part of differing pathways each bringing strengths, weaknesses and compromises. These hidden depths provide an explanation for many of the emotional sensitivities and vulnerabilities which continue to influence our world today.
... Researchers, who assume reciprocity to be highly cognitively demanding, came to the conclusion that reciprocity is virtually absent in non-human animals (Amici et al., 2014;Clements & Stephens, 1995;Hauser, McAuliffe, & Blake, 2009;Pelé, Thierry, Call, & Dufour, 2010;Sánchez-Amaro & Amici, 2015;Stephens, McLinn, & Stevens, 2002;Stevens & Hauser, 2004). In contrast, researchers who assume that reciprocity varies in its cognitive load came to the opposite conclusion that reciprocity is widespread (Brosnan & de Waal, 2002;Brosnan, Salwiczek, & Bshary, 2010;Carter, 2014;Freidin, Carballo, & Bentosela, 2017;Melis & Semmann, 2010;Raihani & Bshary, 2011;Schino & Aureli, 2009, 2010bTaborsky, Frommen, & Riehl, 2016). Here, we argue that the debate can be enriched and potentially resolved by identifying and discussing the concrete psychological processes of all different forms of reciprocity by using and incorporating findings from different lines of research. ...
... Although several authors have discussed the various mechanisms that may underlie reciprocal exchanges between individuals (e.g. Brosnan & de Waal, 2002;Schino & Aureli, 2010b), as far as we know, no attempt has been made to systematically relate those mechanisms to the psychological processes underlying them. Our aim in this article is to bring attention to this issue as a necessary step towards the ultimate goal of elucidating the psychological processes underlying different forms of reciprocity. ...
... Another line of research has focussed mostly on mechanisms that may enable reciprocity (e.g. Brosnan & de Waal, 2002;Schino & Aureli, 2010b). A mechanism describes the basal cause of a behaviour or a strategy, which can be cognitive in the case of reciprocity (Bateson & Laland, 2013;Tinbergen, 1963). ...
Reciprocity is probably one of the most debated theories in evolutionary research. After more than 40 years of research, some scientists conclude that reciprocity is an almost uniquely human trait mainly because it is cognitively demanding. Others, however, conclude that reciprocity is widespread and of great importance to many species. Yet, it is unclear how these species reciprocate, given its apparent cognitive complexity. Therefore, our aim was to unravel the psychological processes underlying reciprocity. By bringing together findings from studies investigating different aspects of reciprocity, we show that reciprocity is a rich concept with different behavioural strategies and cognitive mechanisms that require very different psychological processes. We reviewed evidence from three textbook examples, i.e. the Norway rat, common vampire bat and brown capuchin monkey, and show that the species use different strategies and mechanisms to reciprocate. We continue by examining the psychological processes of reciprocity. We show that the cognitive load varies between different forms of reciprocity. Several factors can lower the memory demands of reciprocity such as distinctiveness of encounters, memory of details and network size. Furthermore, there are different information operation systems in place, which also vary in their cognitive load due to assessing the number of encounters and the quality and quantity of help. We conclude that many species possess the psychological processes to show some form of reciprocity. Hence, reciprocity might be a widespread phenomenon that varies in terms of strategies and mechanisms.
... Second, reputation-building can occur when actors have repeated interactions: both direct knowledge of a partner's past actions and indirect third-party knowledge, or 'reputation', can facilitate more trusting behaviour [11,18,19]. This propensity to trust others appears to be either unique to or especially exaggerated in humans, as other animals do not show such robust tendencies for trust when facing a risk of betrayal [20][21][22] and exhibit limits on their reciprocal behaviour more generally [23,24]. Therefore, engaging in acts of trust and identifying trustworthy exchange partners based on their social history can help overcome the moral hazard problem posed by economic exchange and allow humans to engage in new forms of cooperation. ...
... The only evidence for non-human trust in reciprocity comes from low-cost interactions where the partner's temptation to engage in betrayal is reduced [20][21][22]. More broadly, there is surprisingly little empirical evidence for any sort of reciprocal interactions in non-human animals, despite theoretical proposals suggesting that reciprocity should be common in nature [23,24]. For example, while humans routinely use reciprocation in the context of food sharing, most other primates do not [22]. ...
... R. Soc. B 286: 20190822 natural interactions like grooming, but do not exhibit robust contingent reciprocity involving reasoning about costs and benefits [23,24,58,59]. This stands in contrast to chimpanzees' sophistication when it comes to mutualistic forms of cooperation [45]. ...
Mutually beneficial interactions often require trust that others will reciprocate. Such interpersonal trust is foundational to evolutionarily unique aspects of human social behaviour, such as economic exchange. In adults, interpersonal trust is often assessed using the 'trust game', in which a lender invests resources in a trustee who may or may not repay the loan. This game captures two crucial elements of economic exchange: the potential for greater mutual benefits by trusting in others, and the moral hazard that others may betray that trust. While adults across cultures can trust others, little is known about the developmental origins of this crucial cooperative ability. We developed the first version of the trust game for use with young children that addresses these two components of trust. Across three experiments, we demonstrate that 4- and 6-year-olds recognize opportunities to invest in others, sharing more when reciprocation is possible than in a context measuring pure generosity. Yet, children become better with age at investing in trustworthy over untrustworthy partners, indicating that this cooperative skill emerges later in ontogeny. Together, our results indicate that young children can engage in complex economic exchanges involving judgements about interpersonal trust and show increasing sensitivity to appropriate partners over development.
... Choosing good social partners is one key to successful human cooperation (Henrich, 2017), but accurately evaluating a potential partner requires acquiring, integrating and processing information across a variety of situations (Brosnan and De Waal, 2002;Schino and Aureli, 2009). Information processing trade-offs create pressure to learn and apply cheap heuristics in partner choice (Schino and Aureli, 2010). These heuristics, however, can produce undesired biases. ...
... This is especially likely where social evaluations are rapid; humans make more mistakes when making decisions under time pressure (Rubinstein, 2013), and these results transfer to social interactions (Evans et al., 2015) including in responses to discrimination (FitzGerald and Hurst, 2017;Greenwald and Banaji, 1995). In primates, there is evidence that reciprocity is driven by relatively simple cognitive processes (Brosnan and De Waal, 2002;Schino and Aureli, 2010). In humans, implicit bias is a measurable and unconscious process that biases perception of social partners based on their perceived group membership (Greenwald and Banaji, 1995). ...
Undesired bias afflicts both human and algorithmic decision making, and may be especially prevalent when information processing trade-offs incentivize the use of heuristics. One primary example is \textit{statistical discrimination} -- selecting social partners based not on their underlying attributes, but on readily perceptible characteristics that covary with their suitability for the task at hand. We present a theoretical model to examine how information processing influences statistical discrimination and test its predictions using multi-agent reinforcement learning with various agent architectures in a partner choice-based social dilemma. As predicted, statistical discrimination emerges in agent policies as a function of both the bias in the training population and of agent architecture. All agents showed substantial statistical discrimination, defaulting to using the readily available correlates instead of the outcome relevant features. We show that less discrimination emerges with agents that use recurrent neural networks, and when their training environment has less bias. However, all agent algorithms we tried still exhibited substantial bias after learning in biased training populations.
... Numerous authors claim that prosociality in animals, including primates, is usually restricted to mutualism, or else a form of attitudinal reciprocity based on emotional dyadic tie strength generated by past interactions (Schino & Aureli, 2010). For example, subordinate bonobos begging a dominant for abundant fruit are considered to be testing or reinforcing tie strength (Yamamoto, 2015). ...
... Once calculated reciprocity is ubiquitous in a species, it becomes adaptive to not only predict which conspecifics will best reciprocate, but also recalling who owes favours, which selects for memory and cognition (Schino & Aureli, 2010). Privileging calculated reciprocity as a divisor between hominin and Pan, Mazzolini and Celani (2020) claim that calculated reciprocity for non-human animals is rare, while Clutton-Brock (2009) conceive that Pan reciprocity is instead explained by mutualism or manipulation (dominant enforcement). ...
A perennial challenge of evolutionary psychology is explaining prosocial traits such as a preference for fairness rather than inequality, compassion towards suffering, and an instinctive ability to coordinate within small teams. Considering recent fossil evidence and a novel logical test, we deem present explanations insufficiently explanatory of the divergence of hominins. In answering this question, we focus on the divergence of hominins from the last common ancestor (LCA) shared with Pan. We consider recent fossil discoveries that indicate the LCA was bipedal, which reduces the cogency of this explanation for hominin development. We also review evolutionary theory that claims to explain how hominins developed into modern humans, however it is found that no mechanism differentiates hominins from other primates. Either the mechanism was available to the last common ancestor (LCA) (with P. troglodytes as its proxy), or because early hominins had insufficient cognition to utilise the mechanism. A novel mechanism, sub-group level selection (sGLS) is hypothesised by triangulating two pieces of data rarely considered by evolutionary biologists. These are behavioural dimorphism of Pan (chimpanzees and bonobos) that remain identifiable in modern humans, and the social behaviour of primate troops in a savannah ecology. We then contend that sGLS supplied an exponential effect which was available to LCA who left the forest, but was not sufficiently available to any other primates. In conclusion, while only indirectly supported by various evidence, sGLS is found to be singularly and persuasively explanatory of human's unique evolutionary story.
... Numerous authors claim that prosociality in animals, including primates, is usually restricted to mutualism, or else a form of attitudinal reciprocity based on emotional dyadic tie strength generated by past interactions (Schino & Aureli, 2010). For example, subordinate bonobos begging a dominant for abundant fruit are considered to be testing or reinforcing tie strength (Yamamoto, 2015). ...
... Once calculated reciprocity is ubiquitous in a species, it becomes adaptive to not only predict which conspecifics will best reciprocate, but also recalling who owes favours, which selects for memory and cognition (Schino & Aureli, 2010 to not be a convincing differentiator between hominin and Pan. ...
As a thesis by publication, the candidate presents his published or submitted first-author research papers that develop a model to explain the innate capacity of humans to collaborate in egalitarian teams. Group dynamics are comprised of the minutiae of member perceptions and reactions that cohere a group. This research addresses the lack of a compelling (comprehensive, accurate and detailed) model of group dynamics.
The word model describes a simplified representation of reality, that may encapsulate multiple theories. By contrast, theory is singular and suggests only partial representation of reality. A model may therefore offer a more complete representation and may achieve the consilience of numerous theories.
This thesis formulates the PILAR model and evaluates each of its five Pillars (Prospects, Involved, Liked, Agency, Respect) and 20 interconnecting forces for their collective capacity to characterise a small group. Various empirical and conceptual evaluations allow the candidate to recommend PILAR as a consilience model that credibly integrates numerous theories while representing an extensive assortment of group dynamics.
Chapter one
Reviews current group dynamics literature; including concepts, models, perspectives, and methodologies. Reasons are proposed for why social and organisational psychology has (arguably) failed to converge upon a compelling baseline model that is consistent with anthropological hominin groups. To demonstrate a potential application of such a model, I examine a practitioner method of organisational devolution, Appreciative Inquiry (AI). The chapter then presents a novel, iterative, method for developing a baseline model of group dynamics that has been adopted by the candidate.
Chapter two (published)
Proposes PILAR as a baseline model of group dynamics encapsulating a significant proportion of social and group psychology (SGP) theory. PILAR postulates five ostensive constructs (Pillars) that each member is unconsciously influenced by, when moderating their level of effort, or engagement. These five Pillars then prompt various participant behaviours, including both visible actions such as expressing an opinion or aiding another member, and hidden actions such as thought processes, which may only be evident in body language (if at all).
Chapters three, four and five (all published)
These three chapters examine whether group members use the five Pillars to assess one another’s contribution to a team. A member observing a colleague’s low Pillars may deduce their poor engagement, while higher Pillars suggest significant effort. A member might also collectively evaluate colleagues’ Pillars to assess a group’s overall engagement, either to match this level, or strategically vary from it, for instance to demonstrate leadership (discussed further in §8.3.3).
Chapter three considers whether peer assessment data is indicative of a student team’s collective engagement, and therefore team grade. However only a weak correlation between team grade and team engagement is found. Empirical investigation reveals that half of the respondents answered the survey insincerely, as demonstrated by a lack of variance between responses. Recommendations are made for an improved, and shorter, peer assessment instrument to encourage sincere responses.
Using an Exploratory Factor Analysis, Chapter four tests whether respondents aligned their item responses in accordance with the five Pillars. Results were as hypothesised, which prompts the candidate to assess whether the five Pillars were present in a popular online peer assessment tool, the Comprehensive Assessment of Team Member Effectiveness (CATME). It is found that CATME’s originating methodology had excluded two Pillars from consideration. High inter-correlations between CATME’s dimensions may have been the result of redundancy as three Pillars were extended over five dimensions.
Chapter five reports the design of a brief peer assessment instrument informed by the Pillars, called Pillar-PP, that assesses a respondent’s peer’s perceptions. The chapter concludes with a recommendation to validate Pillar-PP, while also attempting to identify inter-rater bias between respondents.
Chapter six (published)
To investigate the universality of PILAR, Chapter six attempts unification of two divergent literatures, one positivist and one constructivist. Regarding the positivist literature, it was postulated that should PILAR accurately represent the small group, its Pillars may be able to categorise industrial and organisational psychology (IOP) constructs, since organisations are constituted by (albeit, hierarchical) teams. Regarding the constructivist literature, AI is action research that facilitates the formation of egalitarian team to undertake ad hoc projects.
Chapters seven (published) and eight (submitted)
These two chapters develop an evolutionary story behind a postulated baseline model. Chapter seven contends that sub-group level selection (sGLS) selected for pre-verbal anthropological prosociality. Chapter eight extends sGLS by considering how hominins and modern humans moderate their engagement as hierarchy steepness varies.
Chapter nine (submitted)
Assesses to extent to which Pillars are represented within a systematically selected set of constructs used for group research. It is found that approximately 80% of constructs conceptually align with one Pillar, which suggests that PILAR constitutes a baseline model.
Chapter ten (published)
Applies PILAR to two growing societal problems, mental health and precarious employment. I develop a model that connects the five Pillars with wellbeing via constructs associated with positive psychology. Each Pillar is postulated as only being reliably achievable when a member possesses the respective dimension of psychological capital (PsyCap). Furthermore, that participation in the team delivers the member each of five basic psychological needs (BPN). When examined in the context of low-status, precarious, employment, a novel public policy for increasing population wellbeing is presented.
Chapter eleven
The conclusion summarises the sequence of postulates developed through the course of the thesis. Policy and theory implications were then explored, followed by chapter-specific limitations that are potentially significant in aggregation. The thesis ends with a contention that a unique methodology allows deeper insights than ordinarily possible in a dynamically complex problem space.
... Nowak & Sigmund (1998) and Ferrière (1998) propose that this may be the mechanism which operates on establishing cooperation when the "recipients" of altruism do not have the 1 In this regard, even when the debate is still in force, it seems that it has opted to assume that there are different types of reciprocity and that only the reciprocity calculated is the one that demands all these requirements. For further insight into this topic it is recommended Brosnan & de Waal, 2002;Carter, 2014;de Waal & Brosnan, 2006;de Waal & Suchak, 2010, Freidin, Carballo & Bentosela, 2015Schino & Aureli, 2009, 2010a, 2010b, 2010cSchweinfurth & Call, 2019. opportunity to reciprocate the "giver". ...
... Does this mean that the first hominins or even hominids weren't cooperative and did not establish reciprocal relationships? How can the current presence of this behavior be explained in non-human primates and other gregarious non-human animals (Brosnan & De Waal, 2002;Carter, 2014;Carter & Wilkinson, 2013a, b;de Moura, da Silva Rodrigues, & Siciliano, 2009;de Waal & Suchak, 2010;Freidin et al., 2015;Kuczaj et al., 2015;Kunz, Allgaier, Seyjagat, & Caligiuri, 1994;Schino & Aureli, 2010a, 2010bWilkinson, 1988)? Did the evolution of social behavior also occur during the Late Pleistocene? ...
The question about the origin of social behavior from the evolutionary perspective can be traced back to Darwin. However, the advance of research and discoveries made especially in the first half of the past century, as well as the theoretical positions disseminated by some of the representatives of the so-called «Neo-Darwinist» epistemological position, led to the inquiry about reciprocity and cooperation towards the complex necessity to validate the existence of cooperation and reciprocity. This document offers a critical review of the main assumptions that demonstrate how it is that one of its basic assumptions, that of the existence of an asocial state prior to cooperation and reciprocity can be the cause of the difficulties involved in the explanation of the evolutionary origin of the social behavior.
... They note that emotional mediation makes long-term reciprocity possible (Brosnan & de Waal 2002) and that it allows for the conversion of the value of different behavioral episodes (services like grooming or food sharing) into a common currency. At least for primates this emotional bookkeeping approach seems relevant (see also: van Hooff, 2001;Aureli & Schaffner, 2002;Schino & Aureli, 2010;Evers, de Vries, Spruijt, & Sterck, 2015, and shows clear parallels with the affective tie formation part of the iATM model. ...
... Direct reciprocity involves the exchange of benefits and favors between two people or groups (Axelrod & Hamilton, 1981;Trivers, 1971). Most instances of reciprocal exchange in humans and nonhuman animals involve established relationships within which the exact values of exchanged goods or services are not tracked explicitly and there is no conscious expectation of reciprocation; rather, a history of past interactions serves to establish trust and a statistical expectation of reciprocation (Brosnan & de Waal, 2002;Jaeggi & Gurven, 2013;Schino & Aureli, 2010;Xue & Silk, 2012). This trust may be underwritten by knowledge that the partner has a non-zero welfare tradeoff ratio for the self, which could be established through repeated interactions with increasing stakes (Roberts & Sherratt, 1998). ...
... Another paper documented in detail how partner choice options must be combined with other variables such parasite load, mucus quality and manoeuvrability to predict realised service quality [43]. Furthermore, while many review/perspective papers consider potential links between cooperation and cognition [44][45][46][47][48][49][50][51][52][53], the cognitive machinery necessary to exert partner prioritisation in a cleaning market has now been studied in unprecedented detail [40,[54][55][56]. As another motivation for the current paper, the co-authorship of RN, the main founder of BMT, offers alternative views on this cleaning mutualism. ...
Most mutually beneficial social interactions (cooperation within species, mutualism between species) involve some degree of partner choice. In an analogy to economic theory as applied to human trading practices, biological market theory (BMT) focusses on how partner choice affects payoff distributions among non-human traders. BMT has inspired a great diversity of research, including research on the mutualism between cleaner fish Labroides dimidiatus and other marine fish, their ‘clients’. In this mutualism, clients have ectoparasites removed and cleaners obtain food in return. We use the available data on L. dimidiatus cleaner–client interactions to identify avenues for future expansion of BMT. We focus on three main topics, namely how partner quality interacts with supply-to-demand ratios to affect service quality, the role of threats and forms of forceful intervention, and the potential role of cognition. We consider it essential to identify the specifics of each biological market as a basis for the development of more sophisticated BMT models.
... This type of 'titfor-tat' reciprocity is recorded in highly social animals who can be altruistic to close peers, including coyotes (Canis latrans) (Romero and Aureli 2008), rats (Dolivo, Rutte, and Taborsky 2016) and vampire bats (member of the subfamily Desmodontinae) (Carter and Wilkinson 2015), and is particularly common in primates, as in 'tit-for-tat' grooming, for example. Favours can be remembered for several months in chimpanzees (Schino and Aureli 2010), for whom such helping, whilst limited to 'low-cost' effort, includes not only sharing food or helping instrumentally (to achieve a goal) but also in taking risks to help out others in conflicts (Engelmann, Herrmann, and Tomasello 2015). Favours need not be explicitly remembered as discrete events but rather as a pervasive influence reflecting how each partner feels about (and feels sympathy towards and wishes to help) the other. ...
In Hidden Depths, Professor Penny Spikins explores how our emotional connections have shaped human ancestry. Focusing on three key transitions in human origins, Professor Spikins explains how the emotional capacities of our early ancestors evolved in response to ecological changes, much like similar changes in other social mammals. For each transition, dedicated chapters examine evolutionary pressures, responses in changes in human emotional capacities and the archaeological evidence for human social behaviours. Starting from our earliest origins, in Part One, Professor Spikins explores how after two million years ago, movement of human ancestors into a new ecological niche drove new types of collaboration, including care for vulnerable members of the group. Emotional adaptations lead to cognitive changes, as new connections based on compassion, generosity, trust and inclusion also changed our relationship to material things. Part Two explores a later key transition in human emotional capacities occurring after 300,000 years ago. At this time changes in social tolerance allowed ancestors of our own species to further reach out beyond their local group and care about distant allies, making human communities resilient to environmental changes. An increasingly close relationship to animals, and even to cherished possessions, appeared at this time, and can be explained through new human vulnerabilities and ways of seeking comfort and belonging. Lastly, Part Three focuses on the contrasts in emotional dispositions arising between ourselves and our close cousins, the Neanderthals. Neanderthals are revealed as equally caring yet emotionally different humans, who might, if things had been different, have been in our place today. This new narrative breaks away from traditional views of human evolution as exceptional or as a linear progression towards a more perfect form. Instead, our evolutionary history is situated within similar processes occurring in other mammals, and explained as one in which emotions, rather than ‘intellect’, were key to our evolutionary journey. Moreover, changes in emotional capacities and dispositions are seen as part of differing pathways each bringing strengths, weaknesses and compromises. These hidden depths provide an explanation for many of the emotional sensitivities and vulnerabilities which continue to influence our world today.
... We do share a certain sensitivity to others' motivations with many highly social animals. Chimpanzees, for example, can remember favours that have been done to them for at least six months (Schino and Aureli 2010). Domestic dogs make judgements about people who have either helped or refused to help their owners, and will not accept food from the latter (Chijiiwa et al. 2015). ...
In Hidden Depths, Professor Penny Spikins explores how our emotional connections have shaped human ancestry. Focusing on three key transitions in human origins, Professor Spikins explains how the emotional capacities of our early ancestors evolved in response to ecological changes, much like similar changes in other social mammals. For each transition, dedicated chapters examine evolutionary pressures, responses in changes in human emotional capacities and the archaeological evidence for human social behaviours. Starting from our earliest origins, in Part One, Professor Spikins explores how after two million years ago, movement of human ancestors into a new ecological niche drove new types of collaboration, including care for vulnerable members of the group. Emotional adaptations lead to cognitive changes, as new connections based on compassion, generosity, trust and inclusion also changed our relationship to material things. Part Two explores a later key transition in human emotional capacities occurring after 300,000 years ago. At this time changes in social tolerance allowed ancestors of our own species to further reach out beyond their local group and care about distant allies, making human communities resilient to environmental changes. An increasingly close relationship to animals, and even to cherished possessions, appeared at this time, and can be explained through new human vulnerabilities and ways of seeking comfort and belonging. Lastly, Part Three focuses on the contrasts in emotional dispositions arising between ourselves and our close cousins, the Neanderthals. Neanderthals are revealed as equally caring yet emotionally different humans, who might, if things had been different, have been in our place today. This new narrative breaks away from traditional views of human evolution as exceptional or as a linear progression towards a more perfect form. Instead, our evolutionary history is situated within similar processes occurring in other mammals, and explained as one in which emotions, rather than ‘intellect’, were key to our evolutionary journey. Moreover, changes in emotional capacities and dispositions are seen as part of differing pathways each bringing strengths, weaknesses and compromises. These hidden depths provide an explanation for many of the emotional sensitivities and vulnerabilities which continue to influence our world today.
... Primates continuously and closely monitor their social environment [17]. Affective responses play a crucial role in fostering social relationships (e.g. for emotional book-keeping: [18]; for the neuropeptide theory of social bonding: [19]), and in navigating social challenges, such as aggression or the threat thereof [8]. However, these important affective responses can be challenging to investigate, as they do not always include direct, easily observable, behavioural correlates. ...
Understanding the affective lives of animals has been a long-standing challenge in science. Recent technological progress in infrared thermal imaging has enabled researchers to monitor animals' physiological states in real-time when exposed to ecologically relevant situations, such as feeding in the company of others. During social feeding, an individual's physiological states are likely to vary with the nature of the resource and perceptions of competition. Previous findings in chimpanzees have indicated that events perceived as competitive cause decreases in nasal temperatures, whereas the opposite was observed for cooperative interactions. Here, we tested how food resources and audience structure impacted on how social feeding events were perceived by wild chimpanzees. Overall, we found that nasal temperatures were lower when meat was consumed as compared to figs, consistent with the idea that social feeding on more contested resources is perceived as more dangerous and stressful. Nasal temperatures were significant affected by interactions between food type and audience composition, in particular the number of males, their dominance status, and their social bond status relative to the subject, while no effects for the presence of females were observed. Our findings suggest that male chimpanzees closely monitor and assess their social environment during competitive situations, and that infrared imaging provides an important complement to access psychological processes beyond observable social behaviours.
This article is part of the theme issue ‘Cognition, communication and social bonds in primates’.
... Precisamente por lo anterior es que se desató una controversia en torno a la posibilidad de que la reciprocidad no fuera un fenómeno exclusivamente humano, sino que se presenta también entre todas aquellas especies gregarias y que además, en su definición, no se contemplaran sólo las acciones de ayuda o cooperación (Brandts & Solà, 2001;Clutton-Brock et al., 2000;Clutton-Brock & Parker, 1995;de Waal, 2000;de Waal & Brosnan, 2006;Fher & Henrich, 2003;Hauser, McAuliffe, & Blake, 2009;Jensen, Hare, Call, & Tomasello, 2006;Nowak, 2006;Zahavi, 1995). Esta controversia parece haberse decantado hacia la afirmación de la existencia de interacciones recíprocas en otras especies animales, además de la humana, y en el reconocimiento de lo profundamente entrelazada que se encuentra ésta con otros procesos y fenómenos propios de la existencia en grupo (Carter, 2014;Freidin et al., 2015;Schino & Aureli, 2009, 2010b, 2010a, 2017Suchak & de Waal, 2012;Yamamoto & Takimoto, 2012). ...
Se realizaron dos estudios para evaluar sistemáticamente el establecimiento de interacciones recíprocas, variando el tipo de acción involucrada en la interacción. La serie experimental se realizó con estudiantes universitarios de entre 18 y 28 años, 9 hombres y 7 mujeres. En el primer experimento, las acciones involucradas podían ser vistas como de ayuda para quienes recibían su efecto, en el segundo experimento las acciones involucradas podían ser consideradas como aversivas o molestas para quienes recibían el efecto. De manera general se observó que en ambos casos se estableció la reciprocidad aunque, se estableció en mayor medida, con las acciones que involucraban la ayuda. De manera inversa, el efecto de la historia de interacción creada mediante el experimento adquiere mayor relevancia con las acciones aversivas o molestas que con las de ayuda.
... The variables surplus grooming received and the duration of grooming received by the dominant allowed us to address different reciprocity mechanisms: the terms 'scorekeeping' or 'calculated reciprocity' are typically used to describe strategies investigated by game theoreticians, like tit-fortat (Boyd, 2006;Lehmann, Foster, Borenstein, & Feldman, 2008;Schweinfurth & Taborsky, 2020;Wubs, Bshary, & Lehmann, 2016), although the term 'calculated' may be misleading as it implies a rather precise counting mechanism while animals may rather use rules of thumb. The term 'attitudinal reciprocity' refers to shortterm changes in emotional states that consequently affect behaviour in the short term (Brosnan & de Waal, 2002;Schino & Aureli, 2010). As random factors, we included the identity of the dominant and subordinate individual in 29 possible dyads as well as the hour of the day (with no effect on the outcome) in which the tolerance was tested at the box set-up. ...
Keywords: attitudinal reciprocity Chlorocebus pygerythrus cooperative behaviour experiment grooming tolerance vervet monkey Grooming is the most common cooperative behaviour in primates. It has helped advance our understanding of how animals achieve reciprocal cooperation without using precise counting strategies. For example, attitudinal reciprocity refers to recipients making short-term adjustments like reciprocated grooming or tolerance at food sources based on a change in emotional states. Here, we used an experimental setup to investigate in unprecedented detail the building blocks of attitudinal reciprocity that govern wild dominant females' tolerance around food after a grooming interaction with a subordinate female partner in vervet monkeys. We measured the tolerance of dominant females towards the previous grooming partner within 4 h after a grooming interaction. Tolerance levels remained elevated compared to baseline for the entire period, decreasing with time and predicted to fall to baseline levels after approximately 6 h. The decline in tolerance was not affected by the relationship quality between females, further grooming received from other group members or the surplus grooming that the dominant received relative to what she gave. However, the duration of grooming by the subordinate influenced the dominant's tolerance positively. These results suggest that the temporal dynamics of tolerance are best described as grooming triggering the start of a partner-specific 'hourglass', where the amount of remaining 'sand' equates to the dominant's current tolerance level above baseline. The results challenge the notion that dominants use scorekeeping regarding their grooming debts towards subordinates to make decisions about reciprocating with tolerance.
... Primates often engage in vocal turn taking (Pika, Wilkinson, Kendrick, & Vernes, 2018) or in the care of infants (Snowdon & Ziegler, 2007). Note, however, that turn-taking strategies to divide rewards equally are notoriously difficult and cognitively demanding for nonhuman primates (Schino & Aureli, 2010;Stevens, Cushman, & Hauser, 2005). The establishment of such strategy presupposes that marmosets understand that both individuals have a joint goal and that each individual should be equally rewarded to sustain cooperation over prolonged periods (Melis et al., 2016). ...
Social primates constantly face situations in which their preferences collide and they need to engineer strategies to overcome conflicts of interest. Studies with chimpanzees, Pan troglodytes, have found that they use competitive strategies to overcome social dilemmas, maximizing their own benefits while minimizing the loss of rewards. However, little is known about how other primates that rely more on cooperation would overcome similar dilemmas. We therefore presented male–female pairs of common marmosets, Callithrix jacchus (cooperative breeders) with two experiments of an action-based paradigm that creates a conflict of interest over access to an unequal reward distribution. Rather than engaging in mutual defection, marmosets were able to overcome this social dilemma over time, by developing a mix of strategic behaviours (predominantly by females) and tolerance to disadvantageous reward distributions (predominantly by males). This mix of behavioural strategies yielded more and better rewards for the females. Importantly, such a net outcome is consistent with the natural history of this species where females, who carry a high energetic burden of reproduction, tend to be less prosocial and are receivers, rather than donors, in food-sharing events among adults.
... Traditionally, food-sharing was of interest due to its possible reciprocal nature (e.g. 22,26,30,36,37 ) and the cognitive capacities this may or may not require [38][39][40][41][42] . Lately, food-sharing from parents to offspring has been considered important in facilitating learning about what is edible and how to process food, and might under certain circumstances even be regarded as teaching (for a review see 35 ). ...
Abstract Helping others is a key feature of human behavior. However, recent studies render this feature not uniquely human, and describe discoveries of prosocial behavior in non-human primates, other social mammals, and most recently in some bird species. Nevertheless, the cognitive underpinnings of this prosociality; i.e., whether animals take others’ need for help into account, often remain obscured. In this study, we take a first step in investigating prosociality in azure-winged magpies by presenting them with the opportunity to share highly desired food with their conspecifics i) in a situation in which these conspecifics had no such food, ii) in a situation in which they too had access to that highly desired food, and iii) in an open, base-line, situation where all had equal access to the same food and could move around freely. We find that azure-winged magpies regularly share high-value food items, preferably with, but not restricted to, members of the opposite sex. Most notably, we find that these birds, and specifically the females, seem to differentiate between whether others have food or do not have food, and subsequently cater to that lack. Begging calls by those without food seem to function as cues that elicit the food-sharing, but the response to that begging is condition-dependent. Moreover, analyses on a restricted dataset that excluded those events in which there was begging showed exactly the same patterns, raising the possibility that the azure-winged magpies might truly notice when others have access to fewer resources (even in the absence of vocal cues). This sharing behavior could indicate a high level of social awareness and prosociality that should be further investigated. Further studies are needed to establish the order of intentionality at play in this system, and whether azure-winged magpies might be able to attribute desire states to their conspecifics.
... Mutual grooming between two primates strengthens affiliative relationships as they must both actively maintain interaction symmetry [1,4,5,56]. Thus, reciprocal altruism is characteristic of primate grooming. ...
Although herd size, structure, stability, and social rank among Misaki feral horses have been reported, no studies have been conducted on the affiliative relationships and interactions among members in a Misaki horse herd. The validity of three hypotheses regarding the function of social grooming, the affiliative relationship strengthening hypothesis, the worsened relationship restoring hypothesis, and the grooming parasite removal hypothesis, were tested in a Misaki feral horse (Equus caballus) herd in Cape Toi, Japan. All the nine horses in the "6m" herd were investigated in terms of kinship, grooming, aggression, proximity, social rank, and social network. Mutual grooming occurred only in pairs and was almost perfectly symmetrical. For each member, there was a significant negative correlation between total grooming received from other individuals and self-grooming. Controlling for kinship, there were significant positive partial correlations between mutual grooming and proximity and between aggression and proximity. No correlation was observed between aggression and mutual grooming. The results suggest that mutual grooming symmetry may contribute that both participants simultaneously benefit from parasite removal and strengthen affiliative relationships between seasonally changing herd members; however, mutual grooming did not foster restoring the worsened relationship following aggression promoted by physical proximity. The findings of this study may elucidate the mechanisms by which interactions between herd members are maintained or strengthened.
... The fact that natural instances of reciprocal altruism among genetically unrelated individuals is rare in nonhuman species might be explained by two major constraints. One is the cognitive demands to maintain reciprocity in a large group of individuals (Schino and Aureli 2010). Another constraint is that asymmetries in terms of dominance, resource-gathering abilities, or mate values are so common that the standard prisoner's dilemma underlying many models of reciprocity is problematic (Dawkins 2010). ...
... Grooming represents one of the most common commodities traded among primates and has long been considered a reliable indicator of both long-term and short-term social tolerance (Dunbar 2010;Schino and Aureli 2010). Seyfarth (1977) has proposed that there exists a balance between a group member's preference for particular grooming partners and competition among females for access to the most valuable grooming partners. ...
In this chapter, our goal is to review the evidence for multiple behavioral exchange and interchange in Tibetan macaque groups at Mt. Huangshan, China, and to analyze these dyadic behavioral interactions within the context of behavioral exchange or interchange. We focus on grooming exchanges (grooming vs. grooming), the interchange of grooming for tolerance among female or male intrasexual dyads (grooming vs. tolerance), the interchange of grooming for infant-handling opportunities among females (grooming vs. infant handling), and the interchange of male-to-female agonistic support for mating opportunities among intersexual dyads (agonistic support vs. copulation). These results showed that both males and females may establish diverse forms of behavioral exchange for the same behavioral benefit or interchange for the different behavioral benefit with multiple group members. Future studies need to pay closer attention to how behavioral exchange and interchange are related to the maintenance in the stability of social bonds and the cohesiveness of group networks.
... Such reactions are not necessarily self-conscious; all that seems to be required is the recognition of another individual as a potentially rewarding social partner, which seems to be very widespread within the animal kingdom, including invertebrates (Steiger et al. 2008). Current feelings for partners known as attitudinal reciprocity may also play a role here (Schino and Aureli 2010). ...
Martha Nussbaum’s Anger and Forgiveness makes explicit claims about the moral valence and irrationality of the desire for payback. This article explores the roots of that desire through an analysis of research on inequity aversion in primates, and the sociocultural developmental context for expressions of anger. It explores the content of different expressions of anger and their relationship to rationality by engaging in the work of Thomas Aquinas. I argue that the desire for payback has biosocial roots in cooperation, and that these habits are prerequisites for the development of human moral sensibilities. However, the explicit desire for payback, like anger in general, is morally ambiguous. Anger may be laudable insofar as it is tied to constructive efforts, but the desire to see another person suffer is in itself morally repugnant. Christian religious interpretations of payback further complicate the narrative, since unappealing instances of this desire are thought by some Christians to be nonetheless justified under the banner of God’s wrath.
... These forms of reciprocity have been explained by fairly basic and affectivebased proximate mechanisms such as long-term affiliations and emotional bookkeeping (Brosnan & de Waal, 2002;Schino & Aureli, 2009). By contrast, forms of calculated reciprocity and reputation management that require more cognitive sophistication and planning have rarely been observed in nonhuman animals, if at all (Hammerstein, 2003;Schino & Aureli, 2010. Therefore, one aspect of cooperation that may set us apart from other animals is that we learn how to bribe others. ...
Adults will offer favors to advance their standing and solicit a favor in return, using ostensibly prosocial acts strategically for selfish ends. Here we assessed the developmental emergence of such strategic behaviors in which individuals are generous to elicit future reciprocation from others. In a novel experimental paradigm with children aged 3 to 7 years, we tested whether children are willing to share more valuable resources when this act could prompt subsequent reciprocation. In an Experimental condition, children could share a more attractive or less attractive resource with a person who they knew would subsequently choose to play a game with either the children or another individual. In the Control condition, children knew the person would play alone. Across two studies, we found that over repeated trials, 5- and 7-year-olds, but not 3-year-olds, learned to share more valuable resources in the Experimental condition than in the Control condition. This shows that older age groups were able to quickly learn how to influence the subsequent partner choice in a novel situation. We address theoretical questions about the various types of reciprocity as being supported by different psychological mechanisms and discuss whether the current results could be explained by children's emerging ability for future-directed thinking.
... In the case of a cooperative relationship, the rates of helping measured by an observer are actually a proxy for the strength of the underlying causal social relationship; i.e. the observed helping events are not the immediate cause of the observed reciprocal help. In other words, helping events from A to B should predict helping events from B to A, not because the first event directly caused the second event, but because A and B have a cooperative relationship with a longer-term history of reciprocal help (Schino & Aureli, 2010a. To distinguish between causation and correlation, we use the term 'reciprocity' for the 'causal mechanism' and the term 'symmetry' for the observed 'correlation' between rates of help given and received. ...
Nepotism and reciprocity are not mutually exclusive explanations for cooperation, because helping decisions can depend on both kinship cues and past reciprocal help. The importance of these two factors can therefore be difficult to disentangle using observational data. We developed a resampling procedure for inferring the statistical power to detect observational evidence of nepotism and reciprocity. We first applied this procedure to simulated data sets resulting from perfect reciprocity, where the probability and duration of helping events from individual A to B equalled that from B to A. We then assessed how the probability of detecting correlational evidence of reciprocity was influenced by (1) an increasing number of helping observations and (2) an increasing degree of simultaneous nepotism. Last, we applied the same analyses to empirical data on food sharing in common vampire bats, Desmodus rotundus, and allogrooming in mandrills, Mandrillus sphinx, and Japanese macaques, Macaca fuscata. We show that at smaller sample sizes, the effect of kinship was easier to detect and overestimated relative to the effect of reciprocal help. This bias in power was true in both empirical and simulated data, including when simulating perfect reciprocity and imperfect nepotism. We explain the causes and consequences of this difference in power for detecting the roles of kinship versus reciprocal help. When comparing the relative evidence for kin-biased help and reciprocal help, we suggest that researchers measure the relative reliability of both kinship bias and symmetry in the model by plotting the coefficients and their detection probability as a function of sampling effort. We provide R scripts to allow others to do this power analysis with their own data sets.
... Precisamente por lo anterior es que se desató una controversia en torno a la posibilidad de que la reciprocidad no fuera un fenómeno exclusivamente humano, sino que se presenta también entre todas aquellas especies gregarias y que además, en su definición, no se contemplaran sólo las acciones de ayuda o cooperación (Brandts & Solà, 2001;Clutton-Brock et al., 2000;Clutton-Brock & Parker, 1995;de Waal, 2000;de Waal & Brosnan, 2006;Fher & Henrich, 2003;Hauser, McAuliffe, & Blake, 2009;Jensen, Hare, Call, & Tomasello, 2006;Nowak, 2006;Zahavi, 1995). Esta controversia parece haberse decantado hacia la afirmación de la existencia de interacciones recíprocas en otras especies animales, además de la humana, y en el reconocimiento de lo profundamente entrelazada que se encuentra ésta con otros procesos y fenómenos propios de la existencia en grupo (Carter, 2014;Freidin et al., 2015;Schino & Aureli, 2009, 2010b, 2010a, 2017Suchak & de Waal, 2012;Yamamoto & Takimoto, 2012). ...
Two studies were conducted to systematically assess the establishment of reciprocal interactions by varying the type of action involved in the interaction. The experimental series was carried out with university students between 18 and 28 years old, 9 men and 7 women. In the first experiment, the actions involved could be seen as helpful for those who received their effect, in the second experiment the actions involved could be considered as aversive or annoying for those who received the effect. In general, it was observed that in both cases reciprocity was established, although it was established to a greater extent, with the actions that involved the aid. Conversely, the effect of the interactive history created by the experiment acquires greater relevance with the aversive or annoying actions than with the help ones.
... In social groups with tens of individuals, or complex social dynamics (e.g., Aureli et al., 2008), however, this may easily overload the cognitive abilities of the individuals. Future studies should therefore assess whether these mechanisms are really cognitive, as suggested by the authors, and to what extent they may instead be subserved by more simple mechanisms, like emotionally based bookkeeping (see, e.g., Schino & Aureli, 2010). ...
Proops, Grounds, Smith, and McComb (2018) suggest that horses remember previous emotional expressions of specific humans, and use these memories to adjust their behavior in future social interactions. Despite some methodological shortcomings, this study raises important questions on the complexity of social interactions in nonhuman animals, which surely deserve further attention.
... The majority of rock transfers (7 of 10) were also tolerated thefts (i.e. symmetry-based reciprocity; [49,50]). Interestingly, we only documented two trials in which a nut-owner acquired any pieces of cracked nuts from the rock-owner after transferring uncracked nuts to her. ...
A key feature of human prosociality is direct transfers, the most active form of sharing in which donors voluntarily hand over resources in their possession. Direct transfers buffer hunter-gatherers against foraging shortfalls. The emergence and elaboration of this behaviour thus likely played a key role in human evolution by promoting cooperative interdependence and ensuring that humans' growing energetic needs (e.g. for increasing brain size) were more reliably met. According to the strong prosociality hypothesis, among great apes only humans exhibit sufficiently strong prosocial motivations to directly transfer food. The versatile prosociality hypothesis suggests instead that while other apes may make transfers in constrained settings, only humans share flexibly across food and non-food contexts. In controlled experiments, chimpanzees typically transfer objects but not food, supporting both hypotheses. In this paper, we show in two experiments that bonobos directly transfer food but not non-food items. These findings show that, in some contexts, bonobos exhibit a human-like motivation for direct food transfer. However, humans share across a far wider range of contexts, lending support to the versatile prosociality hypothesis. Our species' unusual prosocial flexibility is likely built on a prosocial foundation we share through common descent with the other apes.
... When discussing the cognitive requirements facing cooperating animals, researchers have focused on the challenge of representing previous interactions of the cooperators [17,101]. Here, we show the high behavioural flexibility and possibly cognition needed to optimize partner choice [13,102]. ...
Living in permanent social groups forces animals to make decisions about when, how and with whom to interact, requiring decisions to be made that integrate multiple sources of information. Changing social environments can influence this decision-making process by constraining choice or altering the likelihood of a positive outcome. Here, we conceptualized
grooming as a choice situation where an individual chooses one of a number of potential partners. Studying two wild populations of sympatric primate species, sooty mangabeys
(Cercocebus atys atys) and western chimpanzees (Pan troglodytes verus), we tested what properties of potential partners influenced grooming decisions, including their relative value
based on available alternatives and the social relationships of potential partners with bystanders who could observe the outcome of the decision. Across 1529 decision events, multiple partner attributes (e.g. dominance ranks, social relationship quality, reproductive state, partner sex) influenced choice. Individuals preferred to initiate grooming with partners of similar global rank, but this effect was driven by a bias towards partners with a high rank compared to other locally available options. Individuals also avoided grooming partners who had strong social relationships with at least one bystander. Results indicated flexible decision-making in grooming interactions in both species, based on a partner’s value given the local social environment. Viewing partner choice as a value-based decision-making process allows researchers to compare how different species solve similar social problems.
... In order to engage in a reciprocal exchange, and individual must, first and foremost, be able to override selfish impulses to take a personal cost in the short term in favor of a long[er] term benefit, an ability often referred to as delay of gratification. Indeed, the notion that the ability to delay gratification is related to reciprocity not a new one, and interspecies differences in this ability are often cited as a reason we see contingent reciprocity in humans but few other animals [42]. Importantly, the ability to delay gratification has been shown to improve between the ages of three and five years of age [43,44] and more recent work by Sebastian-Enesco & Warneken [35] found a positive relationship between children's ability to delay gratification and their tendency to share resources. ...
Humans are a remarkably cooperative species, and one behavior thought to play an important role is that of reciprocal altruism. By ensuring that the immediate costs associated with performing a prosocial action will be recouped in the long-run, reciprocal interactions support the emergence and maintenance of group-level cooperation. Existing developmental research suggests that a tendency toward selective prosocial behavior and an understanding of direct reciprocal interactions emerge in early childhood, but much less is known about the interplay between these two behaviors. In this paper, I review the existing literature supporting the notion that reciprocity mediates early prosocial tendencies and suggest that a greater understanding of the psychological mechanisms underlying reciprocity is needed. Finally, I propose two social cognitive capacities related to prospection that I believe may help to shed light on the psychology of strategic reciprocal interactions and their role in prosocial behavior more broadly.
... There is evidence that chimpanzees form reciprocal relationships with others in their natural behaviors, preferentially cooperating with individuals with whom they uphold a long-term friendship (Gomes et al. 2009). However, these patterns can be regarded as forms of partner choice that operate over longer timescales and are supported by positive feelings toward the other [also called attitudinal reciprocity (Schino & Aureli 2010)] rather than as contingent reciprocity, as seen in human children. Whether chimpanzees can engage in contingent reciprocity based on a conspecific's prior behavior is less clear. ...
In this review, I propose a new framework for the psychological origins of human cooperation that harnesses evolutionary theories about the two major problems posed by cooperation: generating and distributing benefits. Children develop skills foundational for identifying and creating opportunities for cooperation with others early: Infants and toddlers already possess basic skills to help others and share resources. Yet mechanisms that solve the free-rider problem-critical for sustaining cooperation as a viable strategy-emerge later in development and are more sensitive to the influence of social norms. I review empirical studies with children showing a dissociation in the origins of and developmental change seen in these two sets of processes. In addition, comparative studies of nonhuman apes also highlight important differences between these skills: The ability to generate benefits has evolutionary roots that are shared between humans and nonhuman apes, whereas there is little evidence that other apes exhibit comparable capacities for distributing benefits. I conclude by proposing ways in which this framework can motivate new developmental, comparative, and cross-cultural research about human cooperation. Expected final online publication date for the Annual Review of Psychology Volume 69 is January 4, 2018. Please see http://www.annualreviews.org/page/journal/pubdates for revised estimates.
... altruism, grooming, primate, reciprocity 1 | INTRODUCTION Behaviors reducing the immediate payoff of the actor while benefitting the recipient are usually referred to as altruistic [e.g., Brosnan & Bshary, 2010;Schino & Aureli, 2010]. Reciprocity is one of the mechanisms that have been proposed to explain the occurrence of altruistic behaviors [e.g., Alexander, 1974;Trivers, 1971]. ...
... Calculated reciprocity, as an example, has been considered cognitively too demanding for nonhuman species (Schino & Aureli, 2010;Stevens & Hauser, 2004; but see Dufour et al., 2009). However, little attention has been given to those cognitive skills that nonhuman animals purportedly lack for the different forms of reciprocity. ...
Keywords: animal memory common ravens cooperation exchange paradigm indirect reciprocity reciprocity To explain reciprocity, direct or indirect, several proximate mechanisms have been proposed, yet little attention has been given to the specific underlying cognitive mechanisms. Regardless of what proximate rules underlie reciprocity, some kind of memory would be paramount. Corvids in general, and ravens, Corvus corax, specifically, have been shown to possess an array of sophisticated cognitive mechanisms involved in memory. In this study, we tested the memory of nine ravens in an exchange paradigm where they could exchange a low-quality for a high-quality food item. Specifically, we tested whether they remembered who was a reliable 'fair' experimenter and who would not reliably exchange (the 'unfair' experimenter), and whether they would subsequently choose to interact with the former when given the choice. In addition, we tested whether ravens that observed the initial seeding of information about who was 'fair' or 'unfair' could transform bystander information into first-person interactions, i.e. also preferring to interact with the 'fair' experimenter when given the choice. The results show that ravens with first-hand experience were more likely to interact with experimenters with whom they had had a positive previous experience, and that this memory lasted at least 1 month. In contrast, observers did not distinguish between the experimenters when given the choice to interact with them. Previous first-hand experience with the paradigm, however, seemed to help observers to be more successful in solving the task, albeit not significantly above chance. In sum, this study shows memory for direct reciprocity in ravens, and tentatively suggests memory for indirect reciprocity. Accordingly, these results provide hints for the underlying mechanism of memory in raven social interactions.
The origins of evolutionary games are rooted in both economics and animal behaviour, but economics has, until recently, focused primarily on humans. Although historically, specific games were used in targeted circumstances with non-human species (i.e. the Prisoner's Dilemma), experimental economics has been increasingly recognized as a valuable method for directly comparing both the outcomes of economic decisions and their underlying mechanisms across species, particularly in comparison with humans, thanks to the structured procedures that allow for them to be instantiated across a variety of animals. So far, results in non-human primates suggest that even when outcomes are shared, underlying proximate mechanisms can vary substantially. Intriguingly, in some contexts non-human primates more easily find a Nash equilibrium than do humans, possibly owing to their greater willingness to explore the parameter space, but humans excel at more complex outcomes, such as alternating between two Nash equilibria, even when deprived of language or instruction, suggesting potential mechanisms that humans have evolved to allow us to solve complex social problems. We consider what these results suggest about the evolution of economic decision-making and suggest future directions, in particular the need to expand taxonomic diversity, to expand this promising approach.
This article is part of the theme issue ‘Half a century of evolutionary games: a synthesis of theory, application and future directions'.
Most mutually beneficial social interactions (cooperation within species, mutualism between species) involve some degree of partner choice. In an analogy to economic theory as applied to human trading practices, biological market theory (BMT) focuses on how partner choice affects payoff distributions among non-human traders. BMT has inspired a great diversity of research, including research on the mutualism between cleaner fish Labroides dimidiatus and other marine fish, their ‘clients’. In this mutualism, clients have ectoparasites removed and cleaners obtain food in return. We use the available data on L. dimidiatus cleaner–client interactions to identify avenues for future expansion of BMT. We focus on three main topics, namely how partner quality interacts with supply-to-demand ratios to affect service quality, the role of threats and forms of forceful intervention, and the potential role of cognition. We consider it essential to identify the specifics of each biological market as a basis for the development of more sophisticated BMT models.
This article is part of the theme issue ‘Half a century of evolutionary games: a synthesis of theory, application and future directions’.
Humans frequently benefit others strategically to elicit future cooperation. While such forms of calculated reciprocity are powerful in eliciting cooperative behaviors even among self-interested agents, they depend on advanced cognitive and behavioral capacities such as prospection (representing and planning for future events) and extended delay of gratification. In fact, it has been proposed that these constraints help explain why calculated reciprocity exists in humans and is rare or even absent in other animals. The current study investigated the cognitive foundation of calculated reciprocity by examining its ontogenetic emergence in relation to key aspects of children's cognitive development. Three-to-five-year-old children from the US (N = 72, mostly White, from mixed socioeconomic backgrounds) first completed a cognitive test battery assessing the cognitive capacities hypothesized to be foundational for calculated reciprocity. In a second session, children participated in a calculated reciprocity task in which they could decide how many resources to share with a partner who later had the opportunity to reciprocate (reciprocity condition) and with a partner who could not reciprocate (control condition). Results indicated a steep developmental emergence of calculated reciprocity between 3 and 5 years of age. Further analyses showed that measures of delay of gratification and prospection were important predictors of children's rate of calculated reciprocity, even when controlling for age and after including a measure of verbal ability. By contrast, theory of mind abilities were unrelated to children's reciprocal behavior. This is the first systematic investigation of essential cognitive capacities for calculated reciprocity. We discuss prospection and delay of gratification as two domain-general capacities that are utilized for calculated reciprocity and which could explain developmental as well as species-differences in cooperation.
Extortion occurs when one person uses some combination of threats and promises to extract an unfair share of benefits from another. Although extortion is a pervasive feature of human interaction, it has received relatively little attention in psychological research. But, we argue, extortion is structured quite similarly to far better-studied “reciprocal” social behaviors, such as conditional cooperation and retributive punishment. All of these strategies function to elicit some desirable behavior from a social partner and do so by constructing conditional incentives. The main difference is that the desired behavioral response is an unfair or unjust allocation of resources during extortion, whereas it is typically assumed to be a fair or just distribution of resources in studies of reciprocal cooperation and punishment. Thus, we propose that a common set of psychological mechanisms may render these strategies successful. We know from prior work that prosocial forms of reciprocity often work best when implemented inflexibly and intuitively, rather than deliberatively. This both affords long-term commitment to the reciprocal strategy, and also signals this commitment to social partners. We argue that, for the same reasons, extortion is likely to depend largely upon inflexible, intuitive psychological processes. Several existing lines of circumstantial evidence support this conjecture.
Most research on reciprocal cooperation aims to either investigate the conditions that allow its evolution or to document actual cases of reciprocity, while the study of its proximate mechanisms is often neglected. Here, we report on an experiment aimed at testing one of the proximate mechanisms that have been proposed to underlie reciprocal cooperation. We tested 'calculated reciprocity', according to which animals behave cooperatively towards conspecifics driven by the expectation of a return of the favour. We examined food sharing in pairs of tufted capuchin monkeys, Sapajus spp., tested in three different experimental conditions. In the first condition (Reciprocity), we gave the subject some less preferred food that could be shared with the partner and, in a following phase, we gave the partner some preferred food that could be shared with the subject. In the second condition (Control), we gave the subject some less preferred food that could be shared with the partner, but the partner did not have the opportunity to reciprocate. In the third condition (Rewarded Cooperation), we gave the subject some less preferred food that could be shared with the partner, and then we gave the subject a quantity of preferred food proportional to the amount shared with the partner during the test. There was no difference between the three experimental conditions in the amount of food transferred from the subject to the partner. However, in the Rewarded Cooperation condition, capuchin monkeys increased the amount of food shared over successive test sessions. Although it remains undemonstrated whether the subjects understood the differences between the three experimental conditions, our results suggest that the expectation of reciprocation did not motivate capuchin monkeys to share their food. Capuchin monkeys seemed, however, able to learn that sharing can lead to a reward.
Many animals cooperate even with unrelated individuals in various contexts, like providing food or allogrooming others. One possibility to explain the evolution of such apparently altruistic behaviour is reciprocity. In reciprocal cooperative interactions, individuals help those partners that have been previously cooperative and therefore exchange favours. This conditional help follows rules like “I help you because you helped me”. These rules are often assumed to be so cognitively demanding that they may be limited to humans. In this chapter, I will shed light on the cognitive underpinnings of reciprocal cooperation by reviewing work on one of the yet best-studied animal in this research area, the Norway rat (Rattus norvegicus). Various studies have demonstrated that Norway rats reciprocally exchange different goods and services. They most likely form attitudes towards social partners that are based on the cooperation level of the last encounter, which they remember over long time spans. Cooperation decisions based on attitudes appear cognitively less complex than calculations of received and given favours. Thus, reciprocal cooperation based on this cognitive mechanism might be in fact more widespread among non-human animals than commonly believed.
Most evolutionary biologists consider selfishness an intrinsic feature of our genes and as the best choice in social situations. During the last years, prolific research has been conducted on the mechanisms that can allow cooperation to emerge “in a world of defectors” to become an evolutionarily stable strategy. A big debate started with the proposal by W.D. Hamilton of “kin selection” in terms of cost sustained by the cooperators and benefits received by related conspecifics. After this, four other main rules for the evolution of cooperation have been suggested. However, one of the main problems of these five rules is the assumption that the payoffs obtained by either cooperating or defeating are quite well known by the parties before they interact and do not change during the time or after repeated encounters. This is not always the case in real life. Following each rule blindly, there is a risk for individuals to get stuck in an unfavorable situation. Axelrod (1984) highlighted that the main problem is how to obtain benefits from cooperation without passing through several trials and errors, which are slow and painful. With a better understanding of this process, individuals can use their foresight to speed up the evolution of cooperation. Here I show that a multi-armed bandit (MAB) model, a classic problem in decision sciences, is naturally employed by individuals to opt for the best choice most of the time, accelerating the evolution of the altruistic behavior and solving the abovementioned problems. A common MAB model that applies extremely well to the evolution of cooperation is the epsilon-greedy (ε-greedy) algorithm. This algorithm, after an initial period of exploration (which can be considered as biological history), greedily exploits the best option ε% of the time and explores other options the remaining percentage of times (1-ε%). Through the epsilon-greedy decision-making algorithm, cooperation evolves as a multilevel process nested in the hierarchical levels that exist among the five rules for the evolution of cooperation. This reinforcement learning, a subtype of artificial intelligence, with trials and errors, provides a powerful tool to better understand and even probabilistically quantify the chances cooperation has to evolve in a specific situation.
Social bonds have been construed as differentiated and enduring affiliative relationships. Strong bonds will improve fitness through interchanging with coalition formation or tolerance over resources. Social bonds have been found in a variety of taxa and predict the formation of coalitions even amongst males. However, in species exhibiting steeply linear dominance hierarchies, coalitions are hypothesized to be suppressed due to severe competition amongst males, and thus strong bonds may manifest in other forms of behavior, notably social tolerance. The aim of this study was to examine the effects of male–male social bonds and dominance on agonistic supports and aggressive interaction in one of the most despotic primate species, Japanese macaques. I conducted focal samples on male individuals, recording their grooming, proximity to other members, agonistic supports and membership, and aggressive interactions over a 2-year observation period. Male macaques formed differentiated affiliative relationships across dyads and those relationships showed positive relations between the non-mating and the mating seasons. Steep dominance hierarchies were found amongst males. The occurrence of agonistic supports was not explained by the strength of social bonds but by the dominance of the participants, whereas strong bonds predicted less frequent aggressive interaction. These results are in line with the hypothesis that dominance is a major mechanism underlying coalition formation amongst males. Unlike more egalitarian species, strong bonds do not predict coalition formation but rather tolerance in despotic species. These results suggest male–male social bonds will bring alternative consequences according to dominance structures.
Biological market theory has in recent years become an important part of the social evolutionist’s toolkit. This article discusses the explanatory potential and pitfalls of biological market theory in the context of big picture accounts of the evolution of human cooperation and morality. I begin by assessing an influential account that presents biological market dynamics as a key driver of the evolution of fairness norms in humans. I argue that this account is problematic for theoretical, empirical, and conceptual reasons. After mapping the evidential and explanatory limits of biological market theory, I suggest that it can nevertheless fill a lacuna in an alternative account of hominin evolution. Trade on a biological marketplace can help explain why norm-based cooperation did not break down when our late-Pleistocene ancestors entered new, challenging social and economic environments.
A large body of evidence suggests that female Old World monkeys maintain selective long-term grooming interactions with fitness benefits. The last two decades have produced evidence that the regulation of social interactions among primates can be, in part, explained by the Biological Markets theory, with grooming behaviour as the focus of these studies. Grooming facilitates bonding between individuals, constituting an essential part of the regulation of social relationships among female cercopithecids. In contrast to the well-studied baboons (Papio spp), knowledge about the nature of grooming interactions and their regulation is generally lacking for the large, terrestrial species of mandrills (Mandrillus sphinx). We used a combination of social network analysis tools and well-established methods for assessing partner diversity and reciprocity to characterise grooming networks, partner choice and patterns of trade (be groomed, give grooming) among females in a captive group of mandrills, both within and across two separate observation periods. Our results suggest that, even though the relatively stable conditions of captivity allowed the studied females to maintain selective grooming interactions across time, small scale demographic changes affected the grooming dynamics of the group in accordance with the expectations of the Biological Markets theory. In particular, the maturation and consequent integration of a high ranking female into the group's grooming network from one period to the next resulted in a more pronounced effect of rank on the regulation of grooming interactions. In addition, the influence of the maturation of a dependent infant on the grooming interactions of his mother were evident between periods. Our results also demonstrate that grooming networks are dynamic and that high ranking individuals are not necessarily the most central in grooming networks. Finally, we discuss the potential of social network analysis to identify cases of social exclusion and its consequences for captive management.
This thesis addresses the question of how a population of modern hunter-gatherers, the Mbendjele BaYaka, utilise social behaviours to exploit high quality but difficult to acquire foods. In contrast to other primates, the human diet contains a high proportion of meat, tubers and honey which have in common not only a very high calorific density but also considerable acquisition costs. The theory that human cognition coevolved with a transition to a diet specialising in these resources is far from novel. However, the underlying proximate mechanisms that allow hunter-gatherers to exploit these foods is poorly understood. It is widely accepted that food sharing by hunter-gatherers acts as a form of reciprocal altruism, reducing the risk inherent to high variability foods such as large game. However, the underlying mechanism which maintain the reciprocity are often ignored, simply assuming humans have the capacity to calculate and act upon inequalities. Similarly, a long-standing theory explaining the extended period of juvenile dependence in humans argues that it provides the opportunity to acquire the skills and knowledge necessary to hunt and gather difficult to acquire foods, yet we still no relatively little about how hunter-gatherer children learn and develop. In this this thesis I address not only the well-worn question of the ultimate explanations for sharing and childhood, but also examine the proximate mechanisms underlying cooperation and social learning. I make use of a range of data on three contemporary Mbendjele camps, which offer varying social structures and levels of market integration, and compare this to previously published data on the Mbendjele as well as data on a contemporary population of fisher-gatherers, the Agta of the Philippines. The Mbendjele in this study live within a logging concession, an area that in recent years has undergone rapid development. This provides an opportunity to study the impact changes in economy have had on foraging and food sharing. In combination with analyses that make use of recent innovations in remote sensing technology and social network analysis to examine how kin and social relations facilitate cooperation, I find evidence that food sharing serves multiple functions in this society, one of which is risk reduction, but also that attitudinal reciprocity rather than calculated reciprocity may be the underlying mechanism. By observing how Mbendjele children spend their time and how this differs with both age and sex I find evidence that learning is a primary motivator of children’s activity. However, I challenge the assumption that direct experiential learning of male specific foraging is the main mode of learning for Mbendjele boys, suggesting that either learning is indirect and reliant on horizontal pathways, or that this type of learning is not the primary cause for the evolution of the extended juvenile period in humans. The key findings of this thesis highlight the important role played, not only by social behaviours, but also social structures in the hunter-gatherer economy. Affiliative relationships stabilise cooperation and facilitate social learning, and a greater understanding of the proximate mechanisms surely offers a pathway to a better understanding of human evolution.
Nepotism and reciprocity are not mutually exclusive explanations for cooperation; helping decisions can depend on both kinship cues and past reciprocal help. The importance of these two factors can therefore be difficult to disentangle with observational data. We developed a resampling procedure for inferring the statistical power to detect observational evidence of nepotism and reciprocity, and applied this procedure to simulated and real datasets. We simulated datasets resulting from perfect reciprocity, where the probability and duration of helping events from individual A to B equaled B to A. We also simulated varying degrees of simultaneous nepotism. We then assessed how nepotism and sampling effort influenced the probability of detecting evidence of reciprocity. We applied the same analysis to empirical data on food sharing in vampire bats and allogrooming in mandrills and Japanese macaques. Nepotism consistently masked evidence for reciprocity. With perfect reciprocity and imperfect nepotism, nepotism was more likely to be detected and overestimated. We explain the causes and consequences. To compare the relative importance of genetic and social ties, researchers should measure the relative reliability of both estimates. We provide R scripts to allow others to assess the reliability of kinship and reciprocal help estimates in their own datasets.
Dissociative identity disorder is characterised by the presence in one individual of two or more alternative personality states (alters). For such individuals, the memory representation of a particular event can have full episodic, autonoetic status for one alter, while having the status of knowledge or even being inaccessible to a second alter. This phenomenon appears to create difficulties for a purely representational theory and is presented to Mahr & Csibra (M&C) for their consideration.
Here we examine the roles of interpersonal valuation and gratitude in the formation of cooperative relationships. Building on prior work, we draw on the concept of a welfare tradeoff ratio (WTR), an internally computed index of the extent to which one person values another person's welfare relative to his or her own. We test several predictions regarding the effects of benefit delivery on changes in WTR, gratitude, and subsequent cooperation. We show that benefit delivery by a stranger: (i) raises the beneficiary's valuation of the stranger's welfare, (ii) predicts downstream cooperative behavior by the beneficiary toward the stranger, and (iii) is coincident with beneficiaries' expressions of gratitude. We find evidence that cooperation and gratitude, while both sparked via benefit delivery and both underpinned by estimates of welfare valuation, are nevertheless produced in parallel via different paths. Specifically, the updated magnitude-not the initial magnitude or degree of change-of a beneficiary's WTR toward a stranger predicts the beneficiary's downstream cooperative behavior. By contrast, the extent to which the beneficiary's WTR positively changes-and not the initial or updated WTR magnitude-predicts gratitude production, a feature proposed to reinforce the benefactor's actions and foreshadow future cooperative intent on the part of the beneficiary. Taken together, our findings point to the possibility that cooperative behavior might operate via internal estimates of welfare valuation, and that gratitude signals benefit reception and the intent to engage in a cooperative relationship.
Reciprocal altruism provides one evolutionary explanation for cooperation, and extensive research has been conducted to discern when reciprocity occurs and the underlying proximate mechanisms. de Waal and colleagues have proposed three levels of reciprocity. Symmetry-based reciprocity is noncontingent and based on symmetries in existing relationships. Attitudinal reciprocity is contingent and based on an increased positive affective state due to recent interactions. Calculated reciprocity requires the cognitive ability to track favors given and received and has thus far only been seen in great apes (including humans). Long-term relationship structure may also play an important role in reciprocity, which may at least partly explain the relative lack of evidence for reciprocity from laboratory-based studies compared with field studies. Future studies need improved methodologies to better assess the roles of partner choice and long-term relationships in order to better discern the role that reciprocity plays in primate interactions.
Social relationship is a concept that links the observable social interactions between group members to the inferred group social system. Social relationships allow animals (as well as the human observers) to predict the actions and responses of their partners and therefore guide their own. Social relationships can also be described as investments that benefit the individuals involved in them. Some benefits simply require stable association and some level of mutual tolerance, whereas others depend on the establishment of more fully developed social relationships. The variation in the quality of social relationships leads to a great flexibility in the frequency and quality of interaction with various group members and with the same individual over time. A key issue is therefore to understand the proximate mechanisms underlying such flexibility since individuals need to be able to assess relationship quality in order to maximise the benefits that social relationships provide. Assessment of social relationships should be based on the information contained in the various interactions that the partners exchange. Assessment should therefore require bookkeeping of the various interactions, computation of their relative frequencies, and conversion of their quality and information associated with them into common currencies. We propose emotional mediation as a possible mechanism that fulfils such requirements and provides the individual with a timely assessment to guide its social decision. Emotions are viewed as intervening variables that result from the integration of the information contained in the various interactions between two partners. Before presenting evidence for relationship assessment through emotional mediation, we define the concept of emotion in animals and provide evidence for measuring relevant emotions in non-human primates. Then, we present four examples obtained by combining findings from multiple studies. The examples provide evidence for emotion resulting from information contained in the interactions exchanged by the partners and for emotional differences being at the basis of the variation in social interactions. Thus, animals may appreciate variation in their social relationships through emotional mediation. This is a promising avenue to disclose the proximate mechanisms of relationship assessment and we suggest new lines of research to gather further evidence for the role of emotional mediation.
McCullough, Kilpatrick, Emmons, and Larson (2001) posited that gratitude prompts individuals to behave prosocially. However, research supporting the prosocial effect of gratitude has relied on scenario and self-report methodology. To address limitations of previous research, this experiment utilised a laboratory induction of gratitude, a method that is potentially more covert than scenarios and that elicits actual grateful emotion. Prosocial responses to gratitude—operationalised as the distribution of resources to another—were paired with a self-report measure of gratitude to test the prosocial effect of gratitude. To investigate positive mood as an alternative explanation, this experiment compared responses of individuals receiving a favour to responses of individuals receiving a positive outcome by chance. A total of 40 participants were randomly assigned to either a Favour or Chance condition. Participants receiving a favour helped more and reported more gratitude compared to participants in the Chance condition.
A model is presented to account for the natural selection of what is termed reciprocally altruistic behavior. The model shows how selection can operate against the cheater (non-reciprocator) in the system. Three instances of altruistic behavior are discussed, the evolution of which the model can explain: (1) behavior involved in cleaning symbioses; (2) warning cries in birds; and (3) human reciprocal altruism. Regarding human reciprocal altruism, it is shown that the details of the psychological system that regulates this altruism can be explained by the model. Specifically, friendship, dislike, moralistic aggression, gratitude, sympathy, trust, suspicion, trustworthiness, aspects of guilt, and some forms of dishonesty and hypocrisy can be explained as important adaptations to regulate the altruistic system. Each individual human is seen as possessing altruistic and cheating tendencies, the expression of which is sensitive to developmental variables that were selected to set the tendencies at a balance ap...
1Animals can derive leverage over others from (a) resource holding power, based for instance on fighting ability or dominance, and (b) the possession of commodities, such as special skills and resources that cannot be taken away by force.2We contend that power based on the possession of commodities strongly depends on the level of supply and demand for that commodity, a phenomenon we call the ‘market effect’.3Several theoretical and empirical examples are given of social systems in which animals belong to two distinct classes that offer two different kinds of commodities.4The relative frequency of occurrence of the two classes is shown to determine the relative power of their members.5We consider the theoretical properties of bargaining processes by which relative power is converted into corresponding pay-off distributions.6We propose coalition games, a class of games with more than two players and in which bargaining is possible, as suitable paradigms for collaboration among members of social units.
The study of reciprocal altruism, or the exchange of goods and services between individuals, requires attention to both evolutionary
explanations and proximate mechanisms. Evolutionary explanations have been debated at length, but far less is known about
the proximate mechanisms of reciprocity. Our own research has focused on the immediate causes and contingencies underlying
services such as food sharing, grooming, and cooperation in brown capuchin monkeys and chimpanzees. Employing both observational
and experimental techniques, we have come to distinguish three types of reciprocity. Symmetry-based reciprocity is cognitively
the least complex form, based on symmetries inherent in dyadic relationships (e.g., mutual association, kinship). Attitudinal
reciprocity, which is more cognitively complex, is based on the mirroring of social attitudes between partners and is exhibited
by both capuchin monkeys and chimpanzees. Finally, calculated reciprocity, the most cognitively advanced form, is based on
mental scorekeeping and is found only in humans and possibly chimpanzees.
Although human behaviour abounds with reciprocal altruism, few examples exist documenting reciprocal altruism in animals.
Recent non-experimental evidence suggests that reciprocal altruism may be more common in nature than previously documented.
Here we present experimental evidence of mobbing behaviour, the joint assault on a predator in an attempt to drive it away,
as reciprocal altruism in the breeding pied flycatcher (Ficedula hypoleuca). Given a choice, pied flycatchers assisted in mobbing initiated by co-operating neighbours and did not join in mobbing when
initiated by conspecific neighbours which had defected from necessary assistance 1h before. The results suggest the birds
followed a ‘tit-for-tat’-like strategy and that mobbing behaviour of breeding birds may be explained in terms of reciprocal
altruism.
We investigated the temporal relationship between grooming given and agonistic support received in a group of chimpanzees at Chester Zoo, U.K. We compared grooming levels the day before a conflict-with-support to those the day before a conflict-without-support and to baseline to investigate whether individuals groom potential supporters in anticipation of the need for support. We also compared grooming and aggression levels the day after conflicts-with-support to levels the day after conflicts-without-support and to baseline levels to determine whether chimpanzees reward individuals that support them or punish those that do not. Finally, we compared grooming and aggression levels the day after conflicts-with-unsuccessful-solicitations-for-support to those the day after conflicts-with-support and to baseline to examine the behavioral consequences of not providing support when an individual had solicited but did not receive it. Future recipients of support groomed future supporters more the day before receiving support, compared to the day before conflicts-without-support, indicating that grooming increased the likelihood of support. The relationship between prior grooming and support held true only for aggressor and not victim support and is consistent with behavior expected if chimpanzees anticipated the need for agonistic support and groomed their supporter the day before to increase the likelihood of support. We found evidence of a system of reward and punishment. Individuals experienced significantly lower rates of aggression after conflicts in which they provided support than at baseline and after conflicts in which they did not provide support. The finding was true only for aggressor support. We found no evidence that chimpanzees punished individuals whom or that they unsuccessfully solicited with aggression or a reduction in grooming. However, solicitors groomed individuals that they solicited for support significantly more after unsuccessful solicitations than after individuals provided support (but with no difference from baseline), indicating that individuals may attempt to recement their relationship after an unsuccessful solicitation. The findings are consistent with a mechanism of calculated interchange in chimpanzees.
The formation of collaborating pairs by individuals belonging to two different classes occurs in the contexts of reproduction and intea-specific cooperation as well as of inter-specific mutualism. There is potential for partner choice and for competition for access to preferred partners in all three contexts. These selective forces have long been recognised as important in sexual selection, but their impact is not yet appreciated in cooperative and mutualistic systems. The formation of partnerships between members of different classes has much in common with the conclusion of trade agreements in human markets with two classes of traders, like producers and consumers, or employers and employees. Similar game-theoretical models can be used to predict the behaviour of rational traders in human markets and the evolutionarily stable strategies used in biological markets. We present a formal model in which the influence of the market mechanism on selection is made explicit. We restrict ourselves to biological markets in which: (1) Individuals do not compete over access to partners in an agonistic manner, but rather by outcompeting each other in those aspects that are preferred by the choosing party. (2) The commodity the partner has to offer cannot be obtained by the use of force, but requires the consent of the partner. These two restrictions ensure a dominant role for partner choice in the formation of partnerships. In a biological market model the decision to cooperate is based on the comparison between the offers of several potential partners, rather than on the behaviour of a single potential partner, as is implicitly assumed in currently accepted models of cooperation. In our example the members of one class A offer a commodity of fixed value in exchange for a commodity of variable value supplied by the other class, B. We show that when the B-class outnumbers the A-class sufficiently and the cost for the A-class to sample the offers of the B-class are low, the choosiness of the A-class will lead to selection for the supply of high value commodities by the B-class (Fig. 3a). Under the same market conditions, but with a high sampling cost this may still be the evolutionariy stable outcome, but another pair of strategies proves to be stable too: relaxed choosiness of class A coupled with low value commodities supplied by class B (Fig. 3b). We give a number of examples of mating, cooperative and mutualistic markets that resemble the low sampling cost situation depicted in Fig. 3a.
Over the last two decades a large number of experiments have been conducted in which two conspecifics, mainly vertebrates, could obtain rewards through cooperation. At least three different motivations to perform such experiments can be distinguished: (1) detecting the mechanistic basis of naturally occurring forms of cooperation; (2) analysing behavioural strategies specific to cooperation; and (3) testing game-theoretical models. Experimenters in the latter two categories, on which this review concentrates, make use of highly artificial devices. The impression of cooperation in the third category is created because two animals are tested simultaneously after having been trained to interact with an apparatus individually before the experiment. These results can be explained most parsimoniously as the product of instrumental (‘trial-and-error’) learning, hence my label ‘instrumental cooperation’. The underlying philosophy of several studies is reminiscent of the strongly disputed ideas of the ‘behaviourist school’. Results from experiments in the second category highlight the importance of communication; therefore I call this ‘communicative cooperation’. The crucial role of communication identified by studies in the second category calls into question the relevance of the most popular paradigm used in the third category, the two-player Iterated Prisoner's Dilemma. Its stringent conditions, which are hardly ever fulfilled in nature, are very difficult to fulfil in experiments too. I propose that future studies concentrate on experiments that emphasize the role of communication and partner choice with the aim of explaining the emergence and maintenance of naturally occurring forms of cooperation.
Seyfarth (1977, Journal of Theoretical Biology,65, 671–698) proposed a model of social grooming among female monkeys that has had an enormous influence in the primatological literature. To test this model, I reviewed published data on primate grooming behaviour, using meta-analytical techniques. An analysis of grooming behaviour in 27 different social groups belonging to 14 different species revealed that a significant role in the distribution of grooming was played by attraction to high-ranking animals, attraction to kin and competition for grooming partners. These results confirm the majority of the predictions of the model. The need for more observational data on grooming (and other affiliative interactions) in New World monkeys, and experimental data on the relations between the exchange of grooming and the formation of agonistic alliances, is emphasized.
According to a widely accepted paradigm, cooperation among animals resembles an iterated, two-player Prisoner's Dilemma game. In this symmetrical game the two players have equivalent strategic options. Decisions are based only on information obtained in similar interactions with the same player in the past. The Prisoner's Dilemma model ignores the social organization within which cooperation occurs. This paper advocates a set of alternative models based on N-player coalition games that apply especially to collaboration (that is, cooperation and reciprocity) within social groups. The model takes into account the effect of competition for the favours of suitable partners. In Coalition games negotiations are possible and the strategic options of the players can be unequal. An example of a Coalition game, the Veto game, is illustrated by patterns of coalition formation among adult males in a group of wild baboons Papio c. cynocephalus.
In biological markets, two classes of traders exchange commodities to their mutual benefit. Characteristics of markets are: competition within trader classes by contest or outbidding; preference for partners offering the highest value; and conflicts over the exchange value of commodities. Biological markets are currently studied under at least three different headings: sexual selection, intraspecific cooperation and interspecific mutualism. The time is ripe for the development of game theoretic models that describe the common core of biological markets and integrate existing knowledge from the separate fields.
Grooming among female Japanese macaques (Macaca fuscata) was studied to test some predictions derived from the application of biological market theory. Contrary to expectations, Japanese macaques did not time match the duration of grooming episodes, their degree of reciprocation was not related to rank distance, and they did not distribute their immediately reciprocated and nonreciprocated grooming in different ways. However, they did reciprocate total amount of grooming received. These results suggest that the use of the temporal patterning of grooming (immediately reciprocated versus nonreciprocated grooming) to distinguish the different classes of traders predicted by the theory (reciprocal versus interchange traders) is unsuccessful. Copyright 2003.
Primate female allogrooming models based on biological markets theory predict that grooming is "time matched" within bouts, that is, the amount of time the first female grooms predicts the amount of time the second one grooms. The models also predict that when female--female contest competition is weak, grooming is traded for grooming, but when female--female contest competition is strong, grooming may be traded for other commodities such as feeding tolerance, and grooming discrepancy between members of dyads is rank related. We tested these predictions using data collected from adult and subadult female gray-cheeked mangabeys (Lophocebus albigena) (N = 26) in 5 groups in Kibale National Park, Uganda. We found that, overall, females reciprocated in 33% of grooming bouts. Among reciprocated bouts, females in all 5 groups showed time matching. In 2 groups, we also found rank-related grooming discrepancies but showing opposite patterns to each other. Consistent with predictions based on biological markets theory, these groups may have been under greater feeding competition, revealed more by adjustments in ranging behavior than increased agonistic rates. Although these results support current allogrooming models, they also suggest that the models may become more robust if the influence of scramble competition is incorporated. In addition, they emphasize the flexibility and dynamic nature of female competitive relationships within the same population of primates. Copyright 2009, Oxford University Press.
People can time travel cognitively because they can remember events having occurred at particular times in the past (episodic memory) and because they can anticipate new events occurring at particular times in the future. The ability to assign points in time to events arises from human development of a sense of time and its accompanying time-keeping technology. The hypothesis is advanced that animals are cognitively stuck in time; that is, they have no sense of time and thus have no episodic memory or ability to anticipate long-range future events. Research on animals' abilities to detect time of day, track short time intervals, remember the order of a sequence of events, and anticipate future events are considered, and it is concluded that the stuck-in-time hypothesis is largely supported by the current evidence.
A central problem in the study of animal behavior concerns why individuals cooperate and exchange altruistic acts (Dugatkin 1997). Considerable theoretical attention has focused on explaining the evolution of cooperation and altruism in taxa as diverse as insects and primates (Hamilton 1964a, 1964b, Trivers 1971, Brown 1983). Empirically, cooperation among males generates substantial interest because the resource over which they primarily compete, females, is not easily divided and shared (Trivers 1972).
Imagine an individual called "hunter" that expends a good deal of energy to capture a gazelle. As the hunter is consuming his small prey, a second individual called "recipient" approaches and begins feeding peacefully alongside the hunter. A few weeks later the roles reverse, such that the previous recipient has now captured a gazelle, and the previous hunter is taking advantage of the recipient's hard work. Could the hunter and recipient be Maasai warriors? Is it equally likely that they are common chimpanzees, African lions, or Nile crocodiles? All of these species hunt gazelle and live in groups, so why would this scenario apply to some species more appropriately than to others? The answer lies in the costs and benefits associated with sharing food with non-kin. Assuming that one individual can consume the entire gazelle, sharing food with the recipient constitutes an altruistic act-the hunter accepts a fitness cost (reduction in food intake) while increasing the fitness of another (increasing the intake of the recipient).
Data on a large sample of interventions that individuals in two mountain gorilla (Gorilla gorilla beringei) groups made in agonistic interactions between others corroborate and extend earlier analyses in several ways. Related females supported each other as often as those in some female-bonded primates and maintained alliances while they resided together. Most unrelated females rarely supported each other, but some developed alliances. Females mostly supported other females with whom they had affinitive relationships against those they often engaged in dyadic aggression. They showed reciprocity in support, and often intervened against individuals who, in turn, often intervened against them. But even female coalitions that outnumbered their opponents by more than two-to-one had limited effectiveness, largely because males intervened in many female contests to control aggression. By rendering coalitions ineffective, males contribute to a combination of factors (e.g. low potential to gain from cooperation in contest feeding competition) that limit the benefits of female philopatry. Male curtailment of female aggression may influence female mate choice. Co-resident mature males in the study groups competed to control female aggression. High-ranking males curtailed aggression to females by subordinates, although two males formed an alliance against two others in their group. Immature animals mostly received defensive support against larger individuals and did not receive support from adults that could lead to a nepotistic dominance system.
Current socioecological models argue that multi-female primate groups engaging in cooperative, between-group resource competition (BGC), should have egalitarian social relations that promote cohesion among group members, while those that experience strong within-group competition (WGC) should exhibit nepotistic and despotic social behaviour (van Schaik, 1989; Sterck et al., 1997). Here we investigate the idea that very slight WGC can have strong effects on social relationships, even in 'egalitarian' populations, and that individual responses to ecological conditions may vary among group members. We estimated the intensity of both BGC and WGC and used the Biological Markets model to examine their effects on female dominance and grooming distributions for a group of samango monkeys (Cercopithecus mitis erythrarchus) in a high-density, territorial population. We found high levels of territorial activity consistent with female resource defence, low levels of within-group aggression and only slight effects of contest competition on diet. Individual grooming bouts were reciprocal, with no effects of rank, demonstrating that grooming was not exchanged for feeding tolerance. However, in contrast to other C. mitis populations, female samangos maintained a consistent, linear dominance hierarchy that was reflected in the overall patterns of association and grooming, with high-ranking females receiving more grooming, and lower-ranking females were less likely to take part in territorial activity. Our results support the prediction of the current socioecological model that WGC effects on female relationships will always be greater than the cohesive effects of BGC (Wrangham, 1980; Cheney, 1992), and show that a simple 'egalitarian' description of C. mitis female relationships is insufficient.
Evidence is presented that the reciprocal exchange of social services among chimpanzees (Pan troglodytes) rests on cognitive abilities that allow current behavior to be contingent upon a history of interaction. Food sharing within a captive colony of chimpanzees was studied by means of 200 food trials, conducted on separate daus over a 3-year period, in which 6,972 approaches occurred among the nine adults in the colony. The success rate of each adult, A, to obtain food from another adult, B, was compared with grooming interactions between A and B in the 2 hours prior to each food trial. The tendency of B to share with A was higher if A had groomed B than if A had not done so. The exchange was partner-specific, i.e., the effect of previous grooming on the behavior of food possessors was limited to the grooming partner. Grooming did not affect subsequent sharing by the groomer, only by the groomee. The effect of grooming was greatest for pairs of adults who rarely groomed. Nevertheless, the effect was general: 31 dyadic directions showed an increase in sharing following grooming, and only 11 a decrease. Food possessors actively resisted approaches by individuals who had not groomed them. After food trials there was a significant reduction of grooming by previous possessors towards those individuals with whom they had shared.
The second edition of this best-selling book has been thoroughly revised and expanded to reflect the significant changes and advances made in systematic reviewing. New features include discussion on the rationale, meta-analyses of prognostic and diagnostic studies and software, and the use of systematic reviews in practice.
This chapter discusses the dynamics of cooperation in primate groups; reviews observational and experimental evidence about turn‐taking, collaboration, and coordination in primate groups; and describe four gametheoretic models in which individuals can benefit from providing help to others, arguing that the formal payoff structures derived from these models provide a clear and cogent framework for understanding the processes underlying various types of cooperative interactions. It also focuses on the situations in which animals must work together to achieve a joint reward—a situation that corresponds loosely to the payoff structure of the Stag Hunt model.
People feel grateful when they have benefited from someone's costly, intentional, voluntary effort on their behalf. Experiencing gratitude motivates beneficiaries to repay their benefactors and to extend generosity to third parties. Expressions of gratitude also reinforce benefactors for their generosity. These social features distinguish gratitude from related emotions such as happiness and feelings of indebtedness. Evolutionary theories propose that gratitude is an adaptation for reciprocal altruism (the sequential exchange of costly benefits between nonrelatives) and, perhaps, upstream reciprocity (a pay-it-forward style distribution of an unearned benefit to a third party after one has received a benefit from another benefactor). Gratitude therefore may have played a unique role in human social evolution.
ALTRUISM is behaviour that benefits another individual at some cost to the altruist, costs and benefits being measured in terms of individual fitness. ‘Reciprocal altruism’ (ref. 1) implies the exchange of altruistic acts between unrelated individuals as well as between relatives. If the benefits to the recipient of an altruistic act exceed the costs to the altruist, and if the recipient is likely to reciprocate at a later time, then the cumulative benefits for both individuals will have exceeded the cumulative costs of their altruism. Natural selection would favour individuals that engaged in reciprocal altruism if they distributed their altruism with respect to the altruistic tendencies of the recipient, preferring individuals that were most likely to reciprocate and excluding nonaltruists from the benefits of further altruism. This model has been difficult to test because it is usually impossible to be certain that an example of altruism is not the product of ‘kin selection’2. The genetic relationships between individuals in animal populations are seldom known and reciprocal altruism can only be cited when it can be found to occur regularly between unrelated individuals. I report here that altruistic behaviour involving the formation of coalitions among male olive baboons (Papio anubis) fulfils the criteria for reciprocal altruism.
As a supplement to my textbook on animal behavior, this new text on human ethology is based on the latter half of my life's work. The findings on animal ethology are only occasionally cited in this work and then only to the extent that they contribute to the understanding of ethological concepts.
I hope that this first text on human ethology presents itself as a unified work, even though not every area could be treated with equal depth. For example, a branch of ethology has developed in the past decades which places particular emphasis on ecology and population genetics. This field, known as sociobiology, has enriched discussion beyond the boundaries of behavioral biology through its stimulating, and often provocative, theses. I will discuss some of its contributions when appropriate in this volume, but, of course, cannot cover this new field in depth.
This work offers a biological point of view for discussion and includes data from my own cross-cultural work and research from the staff of our institute. It confirms, above all else, the astonishing unity of mankind and paints a basically positive picture of how we are moved by the same passions, jealousies, friendliness, and active curiosity. (PsycINFO Database Record (c) 2012 APA, all rights reserved)
After three decades of worldwide research on reciprocal altruism and related phenomena, no more than a modest number of animal examples have been identified. Even in primates, evidence for reciprocity is surprisingly scarce. In contrast to the shortage of support, reciprocal altruism and Tit-for-Tat-like behavior have been used as the prime explanation for cooperation among nonkin. From models based on this line of reasoning, one easily gets the impression that reciprocity should be widespread among social animals. Why is there such a discrepancy between theory and facts? A look at the best known examples of reciprocity shows that simple models of repeated games do not properly reflect the natural circumstances under which evolution takes place. Most repeated animal interactions do not even correspond to repeated games. Partner switching and mobility often counteract the evolutionary stability of reciprocal altruism. Moreover, if learning is involved in mental implementation, then the timescale in which reciprocity can occur is often dramatically shortened. In the few known examples, quick reciprocation seems to be the rule, yet standard game theory fails to account for this empirical finding. More generally, it must be emphasized that mental mechanisms shape the evolution of reciprocity. An impressive mental machinery is required for nontrivial examples of reciprocity, as illustrated by the attribution problem (i.e., the problem of classifying other individuals' actions as cooperative, intentionally uncooperative, or unintentionally uncooperative). Emotions may play a role in the machinery underlying cooperation, but current game theory is conceptually not designed to account for the role emotions play. Collectively, this shows that many obstacles can impede the evolution of reciprocity and that evolutionary game theory needs new conceptual tools to understand these obstacles adequately. (PsycINFO Database Record (c) 2012 APA, all rights reserved)
Studied interchange of support for being groomed by giving individual long-tailed macaques the opportunity to support others under 3 conditions: being groomed by the other, after grooming the other, and without prior grooming. Results provided direct evidence that after being groomed recently by another, a monkey is more likely to support its groomer than without prior grooming. Results concern aggressor support only, since victim support did not occur. The tendency to support others was not increased by any grooming interaction. (PsycINFO Database Record (c) 2012 APA, all rights reserved)
Cooperation is common across nonhuman animal taxa, from the hunt-ing of large game in lions to the harvesting of building materials in ants. Theorists have proposed a number of models to explain the evolution of cooperative behavior. These ultimate explanations, however, rarely consider the proximate constraints on the im-plementation of cooperative behavior. Here we review several types of cooperation and propose a suite of cognitive abilities required for each type to evolve. We propose that several types of cooperation, though theoretically possible and functionally adaptive, have not evolved in some animal species because of cognitive constraints. We argue, therefore, that future modeling efforts and experimental investigations into the adaptive function of cooperation in animals must be grounded in a realistic assessment of the psychological ingredients required for cooperation. Such an approach can account for the puzzling distribution of cooperative behaviors across taxa, especially the seemingly unique occurrence of cooperation observed in our own species.
The scarcity of evidence for contingent reciprocity has led to a growing interest in how market forces shape the distribution of exchanges in animal groups. In a biological market, supply and demand determines the value of an exchange, and individuals choose to trade with the partner offering the highest value. Partners maximize their immediate benefits without the need to monitor the balance of their exchange over time. Applied to grooming exchanges in primate groups, a market model predicts that females will primarily balance the amount of grooming they trade within single bouts, particularly when all partners offer similar value. If some partners can offer other benefits, like reduced aggression, females may exchange grooming for those benefits. In such cases, grooming will not be evenly balanced within bouts. Here, we examine the patterning of grooming in a group of free-ranging olive baboons (Papio anubis). In contrast to predictions derived from a biological market model, two-thirds of all grooming bouts in this group were completely one-sided and females did not consistently provide more grooming to higher-ranking partners. Grooming was more evenly balanced across multiple bouts than within single bouts, suggesting that females are not constrained to complete exchanges within single transactions.
Recent theoretical and experimental studies argued that reciprocity is constrained by the cognitive limitations of most animals and that, when reciprocation occurs, it should necessarily be short term. In this study, we examined the time frame of partner choice in the reciprocal grooming of captive female tufted capuchin monkeys (Cebus apella). Female capuchins groomed preferentially those individuals that overall groomed them most. Tufted capuchins did sometimes reciprocate grooming immediately. We quantified the time course and probability of immediate reciprocation, and excluded from the analysis cases of immediate reciprocation. We then showed that, even excluding immediate reciprocation, female capuchins still preferred to groom those individuals that groom them most. Our results show that partner choice is not necessarily based on immediate reciprocation and suggest that capuchins are able to reciprocate over longer time frames. These findings argue against the hypothesis that long-term reciprocation is absent in species lacking sophisticated cognitive abilities. We suggest that reciprocal altruism over long time frames relies on a system of emotional bookkeeping.
Despite its widespread practice among primates writ large, social scientists have given mutual grooming among humans little
attention. This research provides an important first step in describing mutual grooming among humans. A scale was developed
to measure self-reported giving and receiving of grooming. In Study 1, 184 female and 94 male participants first indicated
their closest emotional relationship (for example, romantic partner, best friend, etcetera). They then completed the grooming
measure pertaining to that emotionally close target person. Finally, they completed indices of relationship trust, relationship
satisfaction, and parental/familial affection. Individuals who focused on their romantic partners (N = 134) reported more mutual grooming than individuals who focused on other types of relationships. Relationship satisfaction,
previous experience of familial affection, and trust were positively correlated with mutual grooming for romantically involved
individuals. Study 2 (N = 71 heterosexual couples) explored psychological correlates of mutual grooming within romantic dyads. Individuals with more
promiscuous attitudes and those who scored high on the anxiety subscale of an adult attachment style measure reported grooming
their partners most frequently. Findings were consistent with several proposed functions of grooming: (a) potential parental-investment
indicator, (b) developing trust, and (c) courtship/flirtation—all of which play roles in pair-bonding. At first glance, humans
may not appear to groom each other with the same fervor as other primates. However, we posit that humans are, in actuality,
groomers par excellence.
It is often (implicitly) assumed that the expectation of reciprocation motivates animal altruism, and thus that animals “plan”
their social interactions. We tested this hypothesis by studying a captive group of mandrills (Mandrillus sphinx). In our focal group, the alpha male was more likely to provide agonistic support in the minutes after the receipt of grooming
than in the absence of previous grooming. This offered other group members the possibility of manipulating the male’s support
by grooming him before engaging in an aggression. We used survival analysis to test the hypothesis that the other group members
systematically groomed the alpha male just before engaging in aggression, which would suggest that the expectation of reciprocation
motivated their grooming. Contrary to the prediction of our hypothesis, we found that other group members did not groom the
alpha male just before engaging in aggression, and thus did not benefit from increased support from the most effective ally.
These results suggest that mandrills do not plan their social interactions and that the expectation of reciprocation does
not motivate them to groom.
KeywordsAggression–Grooming–
Mandrillus sphinx
–Proximate causation–Reciprocation
Agonistic intervention behavior was observed in captive groups of chimpanzees (Pan troglodytes), rhesus monkeys (Macaca mulatta), and stumptail monkeys (M. arctoides). Reciprocity correlations of interventions were determined while removing from the data the effects of several symmetrical relationship characteristics, that is, matrillineal kinship, proximity relations, and same-sex combination. It was considered likely that if significant reciprocity persisted after controlling for these characteristics, the reciprocity was based on cognitive mechanisms. Statistical significance was tested by means of recently developed matrix permutation procedures. All three species exhibited significant reciprocity with regard to beneficial interventions, even after controlling for symmetrical traits. Harmful interventions were, however, reciprocal among chimpanzees only. This species showed a “revenge system”, that is, if A often intervened against B, B did the same to A. In contrast, both macaque species showed significantly inversed reciprocity in their harmful interventions: if A often intervened against B, B rarely intervened against A. Further analysis indicates that the strict hierarchy of macaques prevents them from achieving complete reciprocity. Compared to chimpanzees, macaques rarely intervene against higher ranking group members. The observed contrast can be partially explained on the basis of differences in available space, as indicated by a comparison of indoor and outdoor living conditions for the chimpanzee colony. Yet, even when such spatial factors are taken into account, substantial behavior differences between chimpanzees and macaques remain.
Male savanna baboons, Papio cynocephalus, form coalitions with each other as a technique for gaining access to a female in consort with another male. Reciprocal altruism has been invoked as the primary mechanism which underlies this reproductive tactic, but a 19-month field study of the reproductive behaviour of olive baboons, P. c. anubis, in Kenya contradicted this interpretation. Males who solicited others for coalition formation were not more likely to gain access to consort females than were their fellow coalition members. Males who refused to participate in a coalition at one time were still sought as coalition partners at other times by the same male. Coalitions were generally formed by older, middle- to lower-ranking males and targeted at younger, higher-ranking males. Coalitions are a low risk reproductive tactic and the benefits are not partitioned according to initiator/joiner status. Coalitions are likely to be an outcome of cooperation between males which results from the pursuit of self-interest.
The parcelling model of reciprocity predicts that grooming partners will alternate between giving and receiving grooming within grooming bouts, and that each partner will perform approximately as much grooming as it receives within each bout (‘time matching’). Models of allogrooming based on biological markets theory predict that individuals of lower dominance rank will exchange grooming for tolerance from high-rankers, and therefore an inverse relation will be found between grooming partners' dominance rank distance and how closely they match each other's grooming contributions within each bout. We used weighted logistic regression and weighted least-squares regression to test these predictions using data from female white-faced capuchins, Cebus capucinus, and bonnet macaques, Macaca radiata. Only 5–7% of macaque grooming bouts, and 12–27% of capuchin grooming bouts, were reciprocated. However, (1) the duration of grooming by the first groomer significantly predicted whether the groomee would reciprocate at all, and (2) when bouts were reciprocated, the duration of grooming by the first groomer significantly predicted the duration of grooming by the second groomer. Grooming was most balanced among females of similar dominance ranks. Both the time-matching and rank-related effects were weak, although significant. These results indicate that although some form of time matching may be a general characteristic of grooming in female-bonded primate species, time matching accounts for relatively little of the variation in the distribution of grooming within bouts. We also draw attention to weighted regression as a technique that avoids pseudoreplication while using all available data.
This paper reviews recent work on reciprocal altruism in primates with the aim of highlighting the roles that reciprocal partner choice may have had in the evolution of primate altruism, and that emotions may play in supporting primates' ability to exert such reciprocal partner choice. Individual studies and meta‐analyses show that primates reciprocate a variety of behaviors that benefit other individuals (be they altruistic or mutualistic). These behaviors include grooming, agonistic support, and food sharing. Analyses of the time frame of these reciprocal exchanges suggest primates deploy their altruistic behaviors among group mates on the basis of long‐term accounts of altruism received, and are thus not constrained to immediate reciprocation. We argue that a system of emotional bookkeeping of benefits received may be at the basis of primate reciprocation. This hypothesis is consistent with behavioral data and with our current knowledge about primate cognitive abilities and the neurobiological correlates of affiliative behaviors. Investigations of the role that emotions play in the social life of primates may help us bridging the gap between the apparent complexity of their social life and the relative simplicity of their cognitive abilities.
The growing number of empirical studies performed in ecology and evolution creates a need for quantitative summaries of research domains to generate higher-order conclusions about general trends and patterns. Recent developments In meta-analysis (the area of statistics that is designed for summarizing and analyzing multiple independent studies) have opened up new and exciting possibilities. Unlike more traditional qualitative and narrative reviews, meta-analysis allows powerful quantitative analyses of the magnitude of effects and has a high degree of objectivity because it is based on a standardized set of statistical procedures. The first pioneering applications in ecology and evolution demonstrate that meta-analysis is both tractable and powerful.
Since the development of game theory, the analysis of animal behaviour using the theories of economics has become a growing field of biological research in which models of games and markets play an importantbrole. Studies of sexuak selection, interspecific mutualism and intraspecific cooperation show that individuals exchange commodities to their mutual benefit; the exchange values of commodities are a source of conflict, and behavioural mechnisms such as partner choice and contest between competitors determines the composition of trading pairs or groups. These 'biological markets' can be examined to gain a better understanding of the underlying principles of evolutionary ecology. In this volume scientists from different disciplines combine indights from economics, evolutionary biology and the social sciences to look at comparative aspects of economic behaviour in humans and other animals. Aimed primarily at evolutionary biologists and anthropologists, it will also appeal tp psychologists and economists interested in the evolutionary approach
Grooming and agonistic support are 2 common primate behaviors that have been hypothesized to constitute examples of reciprocal
altruism. In particular, because primates often direct their grooming up the dominance hierarchy, it has been suggested that
they may exchange grooming for agonistic support. Empirical tests of this hypothesis have resulted in highly inconsistent
findings. I synthesized the published literature on the relation between grooming and agonistic support in primates using
modern meta-analytical techniques. A meta-analysis of 36 studies carried out on 14 different species showed that a significant
positive relation exists between grooming and agonistic support (weighted average r = 0.154, corrected for publication bias). These findings suggest that grooming and agonistic support may have evolved as
part of a system of low-cost reciprocal altruism. They also highlight the potential of meta-analysis in tackling the study
of behavioral phenomena characterized by low overall frequency and small effect sizes.
Several hypotheses have been proposed to explain the evolution of altruistic behaviours. Their relative roles in explaining actual cases of animal altruism are, however, unclear. In particular, while kin selection is widely believed to have a pervasive influence on animal behaviour, reciprocity is generally thought to be rare. Despite this general agreement, there has been no direct test comparing the relative roles of kinship and reciprocity in explaining animal altruism. In this paper, we report on the results of such a test based on a meta-analysis of allogrooming in primates, grooming being probably the most common altruistic behaviour among mammals. In direct contrast to the prevailing view, reciprocity played a much larger role than kinship in explaining primate allogrooming. These results point to a more significant role of reciprocity in the evolution of animal altruism than is generally acknowledged.
Ecology Letters (2010) 13: 45–50