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Hare, B., Brown, M., Williamson, C., & Tomasello, M. (2002). The domestication of social cognition in dogs. Science, 298(5598), 1634–1636.
Abstract: Dogs are more skillful than great apes at a number of tasks in which they must read human communicative signals indicating the location of hidden food. In this study, we found that wolves who were raised by humans do not show these same skills, whereas domestic dog puppies only a few weeks old, even those that have had little human contact, do show these skills. These findings suggest that during the process of domestication, dogs have been selected for a set of social-cognitive abilities that enable them to communicate with humans in unique ways.
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Brennan, P. A., & Kendrick, K. M. (2006). Mammalian social odours: attraction and individual recognition. Phil. Trans. Biol. Sci., 361(1476), 2061–2078.
Abstract: Mammalian social systems rely on signals passed between individuals conveying information including sex, reproductive status, individual identity, ownership, competitive ability and health status. Many of these signals take the form of complex mixtures of molecules sensed by chemosensory systems and have important influences on a variety of behaviours that are vital for reproductive success, such as parent-offspring attachment, mate choice and territorial marking. This article aims to review the nature of these chemosensory cues and the neural pathways mediating their physiological and behavioural effects. Despite the complexities of mammalian societies, there are instances where single molecules can act as classical pheromones attracting interest and approach behaviour. Chemosignals with relatively high volatility can be used to signal at a distance and are sensed by the main olfactory system. Most mammals also possess a vomeronasal system, which is specialized to detect relatively non-volatile chemosensory cues following direct contact. Single attractant molecules are sensed by highly specific receptors using a labelled line pathway. These act alongside more complex mixtures of signals that are required to signal individual identity. There are multiple sources of such individuality chemosignals, based on the highly polymorphic genes of the major histocompatibility complex (MHC) or lipocalins such as the mouse major urinary proteins. The individual profile of volatile components that make up an individual odour signature can be sensed by the main olfactory system, as the pattern of activity across an array of broadly tuned receptor types. In addition, the vomeronasal system can respond highly selectively to non-volatile peptide ligands associated with the MHC, acting at the V2r class of vomeronasal receptor.The ability to recognize individuals or their genetic relatedness plays an important role in mammalian social behaviour. Thus robust systems for olfactory learning and recognition of chemosensory individuality have evolved, often associated with major life events, such as mating, parturition or neonatal development. These forms of learning share common features, such as increased noradrenaline evoked by somatosensory stimulation, which results in neural changes at the level of the olfactory bulb. In the main olfactory bulb, these changes are likely to refine the pattern of activity in response to the learned odour, enhancing its discrimination from those of similar odours. In the accessory olfactory bulb, memory formation is hypothesized to involve a selective inhibition, which disrupts the transmission of the learned chemosignal from the mating male. Information from the main olfactory and vomeronasal systems is integrated at the level of the corticomedial amygdala, which forms the most important pathway by which social odours mediate their behavioural and physiological effects. Recent evidence suggests that this region may also play an important role in the learning and recognition of social chemosignals.
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Barrett, L., & Henzi, P. (2005). The social nature of primate cognition. Proc Biol Sci, 272(1575), 1865–1875.
Abstract: The hypothesis that the enlarged brain size of the primates was selected for by social, rather than purely ecological, factors has been strongly influential in studies of primate cognition and behaviour over the past two decades. However, the Machiavellian intelligence hypothesis, also known as the social brain hypothesis, tends to emphasize certain traits and behaviours, like exploitation and deception, at the expense of others, such as tolerance and behavioural coordination, and therefore presents only one view of how social life may shape cognition. This review outlines work from other relevant disciplines, including evolutionary economics, cognitive science and neurophysiology, to illustrate how these can be used to build a more general theoretical framework, incorporating notions of embodied and distributed cognition, in which to situate questions concerning the evolution of primate social cognition.
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Tibbetts, E. A. (2002). Visual signals of individual identity in the wasp Polistes fuscatus. Proc. Roy. Soc. Lond. B Biol. Sci., 269(1423), 1423–1428.
Abstract: Individual recognition is an essential component of interactions in many social systems, but insects are often thought incapable of the sophistication necessary to recognize individuals. If this were true, it would impose limits on the societies that insects could form. For example, queens and workers of the paper wasp Polistes fuscatus form a linear dominance hierarchy that determines how food, work and reproduction are divided within the colony. Such a stable hierarchy would be facilitated if individuals of different ranks have some degree of recognition. P. fuscatus wasps have, to our knowledge, previously undocumented variability in their yellow facial and abdominal markings that are intriguing candidates for signals of individual identity. Here, I describe these highly variable markings and experimentally test whether P. fuscatus queens and workers use these markings to identify individual nest-mates visually. I demonstrate that individuals whose yellow markings are experimentally altered with paint receive more aggression than control wasps who are painted in a way that does not alter their markings. Further, aggression declines towards wasps with experimentally altered markings as these novel markings become familiar to their nestmates. This evidence for individual recognition in P. fuscatus indicates that interactions between insects may be even more complex than previously anticipated.
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Bates, L. A., Sayialel, K. N., Njiraini, N. W., Poole, J. H., Moss, C. J., & Byrne, R. W. (2008). African elephants have expectations about the locations of out-of-sight family members. Biol Lett, 4(1), 34–36.
Abstract: Monitoring the location of conspecifics may be important to social mammals. Here, we use an expectancy-violation paradigm to test the ability of African elephants (Loxodonta africana) to keep track of their social companions from olfactory cues. We presented elephants with samples of earth mixed with urine from female conspecifics that were either kin or unrelated to them, and either unexpected or highly predictable at that location. From behavioural measurements of the elephants' reactions, we show that African elephants can recognize up to 17 females and possibly up to 30 family members from cues present in the urine-earth mix, and that they keep track of the location of these individuals in relation to themselves.
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Drummond, H. (2006). Dominance in vertebrate broods and litters. Quarterly Review of Biology, 81(1), 3–32.
Abstract: Drawing on the concepts and theory of dominance in adult vertebrates, this article categorizes the relationships of dominance between infant siblings, identifies the behavioral mechanisms that give rise to those relationships, and proposes a model to explain their evolution. Dominance relationships in avian broods can be classified according to the agonistic roles of dominants and subordinates as “aggression-submission,” “aggression-resistance, ” “aggression-aggression,” “aggression-avoidance,” “rotating dominance,” and “flock dominance.” These relationships differ mainly in the submissiveness/pugnacity of subordinates, which is pivotal, and in the specificity/generality of the learning processes that underlie them. As in the dominance hierarchies of adult vertebrates, agonistic roles are engendered and maintained by several mechanisms, including differential fighting ability, assessment, trained winning and losing (especially in altricial species), learned individual relationships (especially in precocial species), site-specific learning, and probably group-level effects. An evolutionary framework in which the species-typical dominance relationship is determined by feeding mode, confinement, cost of subordination, and capacity for individual recognition, can be extended to mammalian litters and account for the aggression-submission and aggression-resistance observed in distinct populations of spotted hyenas and the “site-specific dominance” (teat ownership) of some pigs, felids, and hyraxes. Little is known about agonism in the litters of other mammals or broods of poikilotherms, but some species of fish and crocodilians have the potential for dominance among broodmates. Copyright © 2006 by The University of Chicago. All rights reserved.
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Flack, J. C., de Waal, F. B. M., & Krakauer, D. C. (2005). Social structure, robustness, and policing cost in a cognitively sophisticated species. Am Nat, 165(5), E126–139.
Abstract: Conflict management is one of the primary requirements for social complexity. Of the many forms of conflict management, one of the rarest and most interesting is third-party policing, or intervening impartially to control conflict. Third-party policing should be hard to evolve because policers personally pay a cost for intervening, while the benefits are diffused over the whole group. In this study we investigate the incidence and costs of policing in a primate society. We report quantitative evidence of non-kin policing in the nonhuman primate, the pigtailed macaque. We find that policing is effective at reducing the intensity of or terminating conflict when performed by the most powerful individuals. We define a measure, social power consensus, that predicts effective low-cost interventions by powerful individuals and ineffective, relatively costly interventions by low-power individuals. Finally, we develop a simple probabilistic model to explore whether the degree to which policing can effectively reduce the societal cost of conflict is dependent on variance in the distribution of power. Our data and simple model suggest that third-party policing effectiveness and cost are dependent on power structure and might emerge only in societies with high variance in power.
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Plotnik, J. M., de Waal, F. B. M., & Reiss, D. (2006). Self-recognition in an Asian elephant. Proc. Natl. Acad. Sci. U.S.A., 103(45), 17053–17057.
Abstract: Considered an indicator of self-awareness, mirror self-recognition (MSR) has long seemed limited to humans and apes. In both phylogeny and human ontogeny, MSR is thought to correlate with higher forms of empathy and altruistic behavior. Apart from humans and apes, dolphins and elephants are also known for such capacities. After the recent discovery of MSR in dolphins (Tursiops truncatus), elephants thus were the next logical candidate species. We exposed three Asian elephants (Elephas maximus) to a large mirror to investigate their responses. Animals that possess MSR typically progress through four stages of behavior when facing a mirror: (i) social responses, (ii) physical inspection (e.g., looking behind the mirror), (iii) repetitive mirror-testing behavior, and (iv) realization of seeing themselves. Visible marks and invisible sham-marks were applied to the elephants' heads to test whether they would pass the litmus “mark test” for MSR in which an individual spontaneously uses a mirror to touch an otherwise imperceptible mark on its own body. Here, we report a successful MSR elephant study and report striking parallels in the progression of responses to mirrors among apes, dolphins, and elephants. These parallels suggest convergent cognitive evolution most likely related to complex sociality and cooperation.
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Grosenick, L., Clement, T. S., & Fernald, R. D. (2007). Fish can infer social rank by observation alone. Nature, 445(7126), 429–432.
Abstract: Transitive inference (TI) involves using known relationships to deduce unknown ones (for example, using A > B and B > C to infer A > C), and is thus essential to logical reasoning. First described as a developmental milestone in children, TI has since been reported in nonhuman primates, rats and birds. Still, how animals acquire and represent transitive relationships and why such abilities might have evolved remain open problems. Here we show that male fish (Astatotilapia burtoni) can successfully make inferences on a hierarchy implied by pairwise fights between rival males. These fish learned the implied hierarchy vicariously (as 'bystanders'), by watching fights between rivals arranged around them in separate tank units. Our findings show that fish use TI when trained on socially relevant stimuli, and that they can make such inferences by using indirect information alone. Further, these bystanders seem to have both spatial and featural representations related to rival abilities, which they can use to make correct inferences depending on what kind of information is available to them. Beyond extending TI to fish and experimentally demonstrating indirect TI learning in animals, these results indicate that a universal mechanism underlying TI is unlikely. Rather, animals probably use multiple domain-specific representations adapted to different social and ecological pressures that they encounter during the course of their natural lives.
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Paz-y-Miño C. G., Bond, A. B., Kamil, A. C., & Balda, R. P. (2004). Pinyon jays use transitive inference to predict social dominance. Nature, 430(7001), 778–781.
Abstract: Living in large, stable social groups is often considered to favour the evolution of enhanced cognitive abilities, such as recognizing group members, tracking their social status and inferring relationships among them. An individual's place in the social order can be learned through direct interactions with others, but conflicts can be time-consuming and even injurious. Because the number of possible pairwise interactions increases rapidly with group size, members of large social groups will benefit if they can make judgments about relationships on the basis of indirect evidence. Transitive reasoning should therefore be particularly important for social individuals, allowing assessment of relationships from observations of interactions among others. Although a variety of studies have suggested that transitive inference may be used in social settings, the phenomenon has not been demonstrated under controlled conditions in animals. Here we show that highly social pinyon jays (Gymnorhinus cyanocephalus) draw sophisticated inferences about their own dominance status relative to that of strangers that they have observed interacting with known individuals. These results directly demonstrate that animals use transitive inference in social settings and imply that such cognitive capabilities are widespread among social species.
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