Development and aging

Children show economic trust for both ingroup and outgroup partners

Grueneisen, S., Rosati, A.G., Warneken, F. (2021) Children show economic trust for both ingroup and outgroup partners. Cognitive Development, 59: 101077

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Trust is a critical aspect of human cooperation, allowing individuals to overcome the risks posed by such interactions because of others’ presumed cooperative inclinations. Adults sometimes mitigate these risks by preferentially trusting members of their own social group, yet it is currently unclear if the early emergence of children’s trust in others’ cooperative tendencies is affected by their intergroup psychology. Here we tested whether group membership impacts two key aspects of trust-based cooperation in young children – their trust in others’ willingness to reciprocate an investment (assessed using the Investment Game, Study 1), and their trust in others’ generosity (assessed using the Faith Game, Study 2). In both studies, children assigned to novel and otherwise arbitrary groups demonstrated general preferences for ingroup members on several measures. However, group membership did not influence their decisions about economic trust. In Study 1, 4- and 6-year-old children showed high levels of trust in both ingroup and outgroup members’ tendency to reciprocate an investment. In Study 2, 6- to 7-year-old children similarly showed high levels of trust in ingroup and outgroup members’ generosity, and they did so regardless of whether their group membership was a matter of common knowledge between themselves and the trustee. These findings show that young children’s preferences for ingroup members do not result in bias due to shared group membership when making economic trust decisions. Rather, children tend to exhibit trust in the cooperativeness of others regardless of group membership.

The primate origins of human social cognition

Bettle, R. & Rosati, A.G. (2021). The primate origins of human social cognition. Language Learning and Development, 17: 96-127

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The ability to understand the mental states of other individuals is central to human social behavior, yet some theory of mind capacities are shared with other species. Comparisons of theory of mind skills across humans and other primates can provide a critical test of the cognitive prerequisites necessary for different theory of mind skills to emerge. A fundamental difference between humans and non-humans is language: while language may scaffold some developing theory of mind skills in humans, other species do not have similar capacities for or immersion in language. Comparative work can therefore provide a new line of evidence to test the role of language in the emergence of complex social cognition. Here we first provide an overview of the evidence for shared aspects of theory of mind in other primates, and then examine the evidence for apparently human-unique aspects of theory of mind that may be linked to language. We finally contrast different evolutionary processes, such as competition and cooperation, that may have been important for primate social cognition versus human-specific forms of theory of mind. We argue that this evolutionary perspective can help adjudicate between different proposals on the link between human-specific forms of social cognition and language.

Variation in primate decision-making under uncertainty and the roots of human economic behaviour

De Petrillo, F. & Rosati, A.G. (2021). Variation in primate decision-making under uncertainty and the roots of human economic behaviour. Philosophical Transactions of the Royal Society B, 376: 20190671

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Uncertainty is a ubiquitous component of human economic behaviour, yet people can vary in their preferences for risk across populations, individuals, and different points in time. As uncertainty also characterizes many aspects of animal decision-making, comparative research can help evaluate different potential mechanisms that generates this variation, including the role of biological differences or maturational change versus cultural learning, as well as identify human-unique components of economic decision-making. Here we examine decision-making under risk across primates, our closest relatives. We first review theoretical approaches and current methods for understanding decision-making in animals. We then assess current evidence for variation in animal preferences between species and populations; between individuals based on personality, sex, and age; and finally, between different contexts and individual states. We then use this primate data to evaluate the processes that can shape human decision-making strategies and identify the primate foundations of human economic behaviour.


The evolutionary origins of natural pedagogy: Rhesus monkeys show sustained attention following nonsocial cues versus social communicative signals

Bettle, R. & Rosati, A.G. (2021). The evolutionary origins of natural pedagogy: Rhesus monkeys show sustained attention following nonsocial cues versus social communicative signals. Developmental Science, 24: e12987.

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The natural pedagogy hypothesis proposes that human infants preferentially attend to communicative signals from others, facilitating rapid cultural learning. In this view, sensitivity to such signals are a uniquely human adaptation and as such nonhuman animals should not produce or utilize these communicative signals. We test these evolutionary predictions by examining sensitivity to communicative cues in 206 rhesus monkeys (Macaca mulatta) using an expectancy looking time task modeled on prior work with infants. Monkeys observed a human actor who either made eye contact and vocalized to the monkey (social cue), or waved a fruit in front of her face and produced a tapping sound (nonsocial cue). The actor then either looked at an object (referential look) or looked towards empty space (look away). We found that, unlike human infants in analogous situations, rhesus monkeys looked longer at events following nonsocial cues, regardless of the demonstrator’s subsequent looking behavior. Moreover, younger and older monkeys showed similar patterns of responses across development. These results provide support for the natural pedagogy hypothesis, while also highlighting evolutionary changes in human sensitivity to communicative signals.

Social selectivity in aging wild chimpanzees

Rosati, A.G., Hagberg, L., Enigk, D.K., Otali, E., Emery Thompson, M., Muller, M.N., Wrangham, R.W., & Machanda, Z.P., (2020) Social selectivity in aging wild chimpanzees. Science, 370: 473-476.

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Humans prioritize close, positive relationships during aging, and socioemotional selectivity theory proposes that this shift causally depends on capacities for thinking about personal future time horizons. To examine this theory, we tested for key elements of human social aging in longitudinal data on wild chimpanzees. Aging male chimpanzees have more mutual friendships characterized by high, equitable investment, whereas younger males have more one-sided relationships. Older males are more likely to be alone, but they also socialize more with important social partners. Further, males show a relative shift from more agonistic interactions to more positive, affiliative interactions over their life span. Our findings indicate that social selectivity can emerge in the absence of complex future-oriented cognition, and they provide an evolutionary context for patterns of social aging in humans.


Healthy cardiovascular biomarkers across the lifespan in wild-born chimpanzees (Pan troglodytes)

Cole, M.F., Cantwell, A., Rukundo, J. Ajarova, L., Fernandez-Navarro, S., Atencia, R. & Rosati, A.G. (2020). Healthy cardiovascular biomarkers across the lifespan in wild-born chimpanzees (Pan troglodytes). Philosophical Transactions of the Royal Society B, 375: 20190609.

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Chimpanzees (Pan troglodytes) are a crucial model for understanding the evolution of human health and longevity. Cardiovascular disease is a major source of mortality during aging in humans and therefore a key issue for comparative research. Current data indicates that compared to humans, chimpanzees have proatherogenic blood lipid profiles, an important risk factor for cardiovascular disease in humans. However, most work to date on chimpanzee lipids come from laboratory-living populations where lifestyles diverge from a wild context. Here we examined cardiovascular profiles in chimpanzees living in African sanctuaries, who semi-free-range in large forested enclosures, consume a naturalistic diet, and generally experience conditions more similar to a wild chimpanzee lifestyle. We measured blood lipids, body weight, and body fat in 75 sanctuary chimpanzees and compared them to publicly-available data from laboratory-living chimpanzees from the Primate Aging Database. We found that semi-free-ranging chimpanzees exhibited lower body weight and lower levels of lipids that are risk factors for human cardiovascular disease, and that some of these disparities increased with age. Our findings support the hypothesis that lifestyle can shape health indices in chimpanzees, similar to effects observed across human populations, and contribute to an emerging understanding of human cardiovascular health in evolutionary context.

Insights from evolutionarily-relevant models for human ageing

Emery Thompson, M., Rosati, A.G., Snyder-Mackler, N. (2020). Insights from evolutionarily-relevant models for human ageing. Philosophical Transactions of the Royal Society B, 375: 20190605.

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As the world confronts the health challenges of an aging population, there has been dramatically increased interest in the science of aging. This research has overwhelmingly focused on age-related disease, particularly in industrialized human populations and short-lived laboratory animal models. However, it has become clear that humans and long-lived primates age differently than many typical model organisms, and that many of the diseases causing death and disability in the developed world are greatly exacerbated by modern lifestyles. As such, research on how the human aging process evolved is vital to understanding the origins of prolonged human lifespan and factors increasing vulnerability to degenerative disease. In this issue, we highlight emerging comparative research on primates, highlighting the physical, physiological, behavioural, and cognitive processes of aging. This work comprises data and theory on non-human primates, as well as underrepresented data on humans living in small-scale societies, which help elucidate how environment shapes senescence. Component papers address (1) the critical processes that comprise senescence in long-lived primates; (2) the social, ecological, or individual characteristics that predict variation in the pace of aging; and (3) the complicated relationship between aging trajectories and disease outcomes. Collectively, this work provides essential comparative, evolutionary data on aging and demonstrates its unique potential to inform our understanding of the human aging process.

Shifting sociality during primate ageing

Machanda, Z.P. & Rosati, A.G. (2020). Shifting sociality during primate ageing. Philosophical Transactions of the Royal Society B, 375: 20190620.

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Humans exhibit major age-related shifts in social relationships along with changes in social and emotional psychological processes that underpin these behavioral shifts. Does social aeging in nonhuman primates follow similar patterns, and if so, what are the ultimate evolutionary consequences of these social shifts? Here we synthesize empirical evidence for shifts in social behavior and underlying psychological processes across species. Focusing on three elements of social behavior and cognition that are important for humans—propensities to engage with others, the positive versus negative valence of these interactions, and capabilities to influence others, we find evidence for wide variation in the trajectories of these characteristics across primates. Based on this, we identify potential modulators of the primate social ageing process, including social organization, sex, and dominance status. Finally, we discuss how comparative research can contextualize human social ageing.

Heterochrony in chimpanzee and bonobo spatial memory development

Rosati, A.G. (2019). Heterochrony in chimpanzee and bonobo spatial memory development. American Journal of Physical Anthropology, 169: 302-321.

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Objectives: The emergence of human-unique cognitive abilities has been linked to our species’ extended juvenile period. Comparisons of cognitive development across species can provide new insights into the evolutionary mechanisms shaping cognition. This study examined the development of different components of spatial memory, cognitive mechanisms that support complex foraging, by comparing two species with similar life history that vary in wild ecology: bonobos (Pan paniscus) and chimpanzees (Pan troglodytes). Materials and Methods: Spatial memory development was assessed using a cross-sectional experimental design comparing apes ranging from infancy to adulthood. Study 1 tested 73 sanctuary-living apes on a task examining recall of a single location after a one-week delay, compared to an earlier session. Study 2 tested their ability to recall multiple locations within a complex environment. Study 3 examined a subset of individuals from Study 2 on a motivational control task. Results: In Study 1, younger bonobos and chimpanzees of all ages exhibited improved performance in the test session compared to their initial learning experience. Older bonobos, in contrast, did not exhibit a memory boost in performance after the delay. In Study 2, older chimpanzees exhibited an improved ability to recall multiple locations, whereas bonobos did not exhibit any age-related differences. In Study 3, both species were similarly motivated to search for food in the absence of memory demands. Discussion: These results indicate that closely-related species with similar life history characteristics can exhibit divergent patterns of cognitive development, and suggests a role of socioecological niche in shaping patterns of cognition in Pan.


Developmental shifts in social cognition: socioemotional biases across the lifespan in rhesus monkeys

Rosati, A.G., Arre, A.M., Platt, M.L., & Santos, L.R. (2018). Developmental shifts in social cognition: socioemotional biases across the lifespan in rhesus monkeys.Behavioral Ecology and Sociobiology, 72: 63.

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Humans exhibit a suite of developmental changes in social cognition across the lifespan. To what extent are these developmental patterns unique? We first review several social domains in which humans undergo critical ontogenetic changes in socio-cognitive processing, including social attention and theory of mind. We then examine whether one human developmental transition—a shift in socioemotional preferences—also occurs in nonhuman primates. Specifically, we experimentally measured socioemotional processing in a large population of rhesus macaques (Macaca mulatta) ranging from infancy to old age. We tested whether macaques, like humans, also exhibited developmental shifts from a negativity bias at younger ages, indicating preferential attention to negative socioemotional stimuli, to a positivity bias at older ages. We first assessed monkeys’ (n = 337) responses to negative socioemotional stimuli by comparing their duration of looking towards photos of negative conspecific signals (threat displays) versus matched neutral expressions. In contrast to the pattern observed in humans, we found that older monkeys were more attentive to negative emotional stimuli than were younger monkeys. In a second study, we used the same method to examine monkeys’ (n = 132) attention to positive (affiliative displays) versus matched neutral expressions. Monkeys did not exhibit an overall preference for positive stimuli, nor major age-related changes in their attention. These results indicate that while monkeys show robust ontogenetic shifts in social preferences, they differ from humans by exhibiting an increasing negativity bias with age. Studies of comparative cognitive development can therefore provide insight into the evolutionary origins of human socio-cognitive development.

Tolerant Barbary macaques maintain juvenile levels of social attention in old age, but despotic rhesus macaques do not

Rosati, A. G., & Santos, L. R. (2017). Tolerant Barbary macaques maintain juvenile levels of social attention in old age, but despotic rhesus macaques do not. Animal Behaviour, 130, 199-207.

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Complex social life is thought to be a major driver of complex cognition in primates, but few studies have directly tested the relationship between a given primate species’ social system and their social cognitive skills. We experimentally compared lifespan patterns of a foundational social cognitive skill (following another’s gaze) in tolerant Barbary macaques, Macaca sylvanus, and despotic rhesus macaques, Macaca mulatta. Semi-free-ranging monkeys (N = 80 individuals from each species) followed gaze more in test trials where an actor looked up compared to control trials. However, species differed in ontogenetic trajectories: both exhibited high rates of gaze following as juveniles, but rhesus monkeys exhibited declines in social attention with age, whereas Barbary macaques did not. This pattern indicates that developmental patterns of social attention vary with social tolerance, and that diversity in social behaviour can lead to differences in social cognition across primates.

Understanding human gaze

Bettle, R., & Rosati, A. G. (2016). Understanding human gaze. In: Encyclopedia of Evolutionary Psychological Science (T. Shackelford and V. Weekes-Shackelford, eds.). Springer, pp. 1-4.

[PDF]  [Publisher’s Version]  Abstract

Social attention is a foundational component of human social behavior. Our ability to detect and think about the direction of other’s gaze involves the attribution of mental states to others and scaffolds the development of other complex cognitive skills. Gaze-following is also widespread among other primates, but the cognitive mechanisms underlying gaze-sensitive behaviors appear to differ across species. Understanding the evolutionary origins of human social attention capacities can reveal the roots of our species’ unique patterns of cognition and culture.

Rhesus monkeys show human-like changes in gaze following across the lifespan

Rosati, A. G., Arre, A. M., Platt, M. L., & Santos, L. R. (2016). Rhesus monkeys show human-like changes in gaze following across the lifespan. Proceedings of the Royal Society B , 283, 20160376.

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Gaze following, or co-orienting with others, is a foundational skill for human social behaviour. The emergence of this capacity scaffolds critical human-specific abilities such as theory of mind and language. Non-human primates also follow others’ gaze, but less is known about how the cognitive mechanisms supporting this behaviour develop over the lifespan. Here we experimentally tested gaze following in 481 semi-free-ranging rhesus macaques (Macaca mulatta) ranging from infancy to old age. We found that monkeys began to follow gaze in infancy and this response peaked in the juvenile period—suggesting that younger monkeys were especially attuned to gaze information, like humans. After sexual maturity, monkeys exhibited human-like sex differences in gaze following, with adult females showing more gaze following than males. Finally, older monkeys showed reduced propensity to follow gaze, just as older humans do. In a second study (n = 80), we confirmed that macaques exhibit similar baseline rates of looking upwards in a control condition, regardless of age. Our findings indicate that—despite important differences in human and non-human primate life-history characteristics and typical social experiences—monkeys undergo robust ontogenetic shifts in gaze following across early development, adulthood and ageing that are strikingly similar to those of humans.

Context influences spatial frames of reference in bonobos (Pan paniscus)

Rosati, A. G. (2015). Context influences spatial frames of reference in bonobos (Pan paniscus). Behaviour, 152, 375-406.

Reprinted in: Bonobo cognition and behavior (B. Hare & S. Yamamoto, eds.)

[PDF]  [Publisher’s Version]  Abstract

Primates must solve complex spatial problems when foraging, such as finding patchy resources and navigating between different locations. However, the nature of the cognitive representations supporting these types of behaviors is currently unclear. In humans, there has been great debate concerning the relative importance of egocentric representations (which are viewer-dependent) versus allocentric representations (which are based on aspects of the external environment). Comparative studies of nonhuman apes can illuminate which aspects of human spatial cognition are shared with other primates, versus which aspects are unique to our lineage. The current studies therefore examined spatial cognitive development in one of our closest living relatives, bonobos (Pan paniscus) across contexts. The first study assessed how younger bonobos encode locations in a place-response task in which apes first learn that one of two locations is consistently baited with a reward, and then must approach the two locations from a flipped perspective. The second study examined how a larger age sample of bonobos responded to a spatial relations task in which they first experience that one location is baited, and then can generalize this learning to a new set of targets. Results indicated that while bonobos exhibited a predominantly allocentric strategy in the first study, they consistently exhibited an egocentric strategy in the second. Together, these results show that bonobos can use both strategies to encode spatial information, and illuminate the complementary contributions to cognition made by egocentric and allocentric representations.

Comparative developmental psychology: How is human cognitive development unique?

Rosati, A. G., Wobber, V., Hughes, K., & Santos, L. R. (2014). Comparative developmental psychology: How is human cognitive development unique?. Evolutionary Psychology, 12, 448-473.

[PDF]  [Publisher’s Version]  Abstract

The fields of developmental and comparative psychology both seek to illuminate the roots of adult cognitive systems. Developmental studies target the emergence of adult cognitive systems over ontogenetic time, whereas comparative studies investigate the origins of human cognition in our evolutionary history. Despite the long tradition of research in both of these areas, little work has examined the intersection of the two: the study of cognitive development in a comparative perspective. In the current article, we review recent work using this comparative developmental approach to study non-human primate cognition. We argue that comparative data on the pace and pattern of cognitive development across species can address major theoretical questions in both psychology and biology. In particular, such integrative research will allow stronger biological inferences about the function of developmental change, and will be critical in addressing how humans come to acquire species-unique cognitive abilities.

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