Early life adversity has sex-dependent effects on survival across the lifespan in rhesus macaques.

Exposure to adversity during early life is linked to lasting detrimental effects on evolutionary fitness across many taxa. However, due to the challenges of collecting longitudinal data, especially in species where one sex disperses, direct evidence from long-lived species remains relatively scarce. Here we test the effects of early life adversity on male and female longevity in a free-ranging population of rhesus macaques (Macaca mulatta) at Cayo Santiago, Puerto Rico. We leveraged six decades of data to quantify the relative importance of ten forms of early life adversity for 6,599 macaques (3,230 male, 3,369 female), with a smaller sample size (N=299) for one form of adversity (maternal social isolation) which required high-resolution behavioral data. We found that individuals who experienced more early life adversity died earlier than those who experienced less adversity. Mortality risk was highest during early life, defined as birth to four years old, suggesting acute survival effects of adversity, but heightened mortality risk was also present in macaques who survived to adulthood. Females and males were affected differently by some forms of adversity, and these differences might be driven by varying energetic demands, female philopatry, and male dispersal. By leveraging data on thousands of macaques collected over decades, our results show that the fitness consequences of early life adversity are not uniform across individuals but vary as a function of the type of adversity, timing, and social context, and thus contribute to our limited but growing understanding of the evolution of early life sensitivities in long-lived species.

How do communicative cues shape the way that dogs (Canis familiaris) encode objects?

Our human capacity to efficiently learn from other individuals is unparalleled in any nonhuman species. Some scholars argue that our propensity to learn socially is supported by an early-emerging expectation that communicative cues will convey generic information (Csibra & Gergely, 2011). In the current 2 studies, we examine whether this expectation about generic information is unique to humans by testing a species that readily attends to human cues-dogs. Specifically, we adapted a violation of expectation paradigm previously used with human infants to examine whether communicative cues lead dogs to selectively encode generic, kind-relevant information about objects (e.g., shape). Prior work has demonstrated that human infants are more likely to notice unexpected changes in kind-relevant information in communicative contexts (i.e., when an agent points to the object; Yoon et al., 2008). In contrast, across 2 studies (N = 136), dogs were no more likely to notice kind-relevant changes in communicative contexts than noncommunicative contexts. These findings suggest that although dogs attend to human communicative cues, such cues do not shape the way that dogs encode objects. More broadly, this finding lends support to the claim that our early-emerging generic expectation crucially supports our human capacity to efficiently learn from one another. (PsycInfo Database Record (c) 2021 APA, all rights reserved).

Macaque species with varying social tolerance show no differences in understanding what other agents perceive.

A growing body of work demonstrates that a species' socioecology can impact its cognitive abilities. Indeed, even closely related species with different socioecological pressures often show different patterns of cognitive performance on the same task. Here, we explore whether major differences in social tolerance in two closely related macaque species can impact a core sociocognitive ability, the capacity to recognize what others see. Specifically, we compared the performance of Barbary macaques (Macaca sylvanus, n = 80) and rhesus macaques (Macaca mulatta, n = 62) on a standard test of visual perspective understanding. In contrast to the difference in performance, one might expect from these species' divergent socioecologies that our results show similar performance across Barbary and rhesus macaques, with both species forming expectations about how another agent will act based on that agent's visual perspective. These results suggest that differences in socioecology may not play as big of a role in the evolution of some theory of mind capacities as they do in other decision-making or foraging contexts.

Do young rhesus macaques know what others see?: A comparative developmental perspective.

Humans undergo robust ontogenetic shifts in the theory of mind capabilities. Are these developmental changes unique to human development or are they shared with other closely related non-human species? To explore this issue, we tested the development of the theory of mind capacities in a population of 236 infant and juvenile rhesus macaques (Macaca mulatta). Using a looking-time method, we examined what developing monkeys know about others' perceptions. Specifically, we tested whether younger monkeys predict that a person will reach for an object where she last saw it. Overall, we found a significant interaction between a monkey's age and performance on this task (p = .014). Juvenile monkeys (between two and 5 years of age) show a nonsignificant trend towards human infant-like patterns of performance, looking longer during the unexpected condition as compared to the expected condition, though this difference is nonsignificant (p = .09). However, contrary to findings in human infants, infant rhesus macaques show a different trend. Infant monkeys on average look slightly longer on average during the expected condition than the unexpected condition, though this pattern was not significant (p = .06). Our developmental results in monkeys provide some hints about the development of the theory of mind capacities in non-humans. First, young rhesus macaques appear to show some interest in the perception of other agents. Second, young rhesus seems able to make predictions based on the visual perspective of another agent, though the developmental pattern of this ability is not as clear nor as robust as in humans. As such, though an understanding of others' perceptions is early-emerging in human infants, it may require more experience interacting with other social agents in our non-human relatives.

One-to-one correspondence without language.

A logical rule important in counting and representing exact number is one-to-one correspondence, the understanding that two sets are equal if each item in one set corresponds to exactly one item in the second set. The role of this rule in children's development of counting remains unclear, possibly due to individual differences in the development of language. We report that non-human primates, which do not have language, have at least a partial understanding of this principle. Baboons were given a quantity discrimination task where two caches were baited with different quantities of food. When the quantities were baited in a manner that highlighted the one-to-one relation between those quantities, baboons performed significantly better than when one-to-one correspondence cues were not provided. The implication is that one-to-one correspondence, which requires intuitions about equality and is a possible building block of counting, has a pre-linguistic origin.

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

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.