Cognition presents evolutionary research with one of its greatest challenges. Cognitive evolution has been explained at the proximate level by shifts in absolute and relative brain volume and at the ultimate level by differences in social and dietary complexity. However, no study has integrated the experimental and phylogenetic approach at the scale required to rigorously test these explanations. Instead, previous research has largely relied on various measures of brain size as proxies for cognitive abilities. We experimentally evaluated these major evolutionary explanations by quantitatively comparing the cognitive performance of 567 individuals representing 36 species on two problem-solving tasks measuring self-control. Phylogenetic analysis revealed that absolute brain volume best predicted performance across species and accounted for considerably more variance than brain volume controlling for body mass. This result corroborates recent advances in evolutionary neurobiology and illustrates the cognitive consequences of cortical reorganization through increases in brain volume. Within primates, dietary breadth but not social group size was a strong predictor of species differences in self-control. Our results implicate robust evolutionary relationships between dietary breadth, absolute brain volume, and self-control. These findings provide a significant first step toward quantifying the primate cognitive phenome and explaining the process of cognitive evolution.psychology | behavior | comparative methods | inhibitory control | executive function S ince Darwin, understanding the evolution of cognition has been widely regarded as one of the greatest challenges for evolutionary research (1). Although researchers have identified surprising cognitive flexibility in a range of species (2-40) and potentially derived features of human psychology (41-61), we know much less about the major forces shaping cognitive evolution (62-71). With the notable exception of Bitterman's landmark studies conducted several decades ago (63, 72-74), most research comparing cognition across species has been limited to small taxonomic samples (70, 75). With limited comparable experimental data on how cognition varies across species, previous research has largely relied on proxies for cognition (e.g., brain size) or metaanalyses when testing hypotheses about cognitive evolution (76-92). The lack of cognitive data collected with similar methods across large samples of species precludes meaningful species comparisons that can reveal the major forces shaping cognitive evolution across species, including humans (48,70,89,(93)(94)(95)(96)(97)(98). SignificanceAlthough scientists have identified surprising cognitive flexibility in animals and potentially unique features of human psychology, we know less about the selective forces that favor cognitive evolution, or the proximate biological mechanisms underlying this process. We tested 36 species in two problemsolving tasks measuring self-control and evaluated the leading hypotheses regarding how ...

Strong evidence indicates that non-human primates possess a numerical representation system, but the inherent nature of that system is still debated. Two cognitive mechanisms have been proposed to account for non-human primate numerical performance: (1) a discrete object-file system limited to quantities <4, and (2) an analog system which represents quantities comparatively but is limited by the ratio between two quantities. To test the underlying nature of non-human primate quantification, we asked eight experiment-naive olive baboons (Papio anubis) to discriminate between number pairs containing small (<4), large (>4), or span (small vs. large) numbers of food items presented simultaneously or sequentially. The prediction from the object-file hypothesis is that baboons will only accurately choose the larger quantity in small pairs, but not large or span pairs. Conversely, the analog system predicts that baboons will be successful with all numbers, and that success will be dependent on numerical ratio. We found that baboons successfully discriminated all pair types at above chance levels. In addition, performance significantly correlated with the ratio between the numerical values. Although performance was better for simultaneous trials than sequential trials, evidence favoring analog numerical representation emerged from both conditions, and was present even in the first exposure to number pairs. Together, these data favor the interpretation that a single, coherent analog representation system underlies spontaneous quantitative abilities in primates.

Olfactory cues can exert priming effects on many mammalian species. Paternally experienced marmosets, Callithrix jacchus, exposed to direct isolated olfactory contact with their own infant's scent show rapid decreases in testosterone levels within 20 minutes, whereas paternally inexperienced males do not. The following study tests whether there is a differential steroid response to exposure of infant scent from dependent infants (own and novel) and independent infants (own and novel). We examined the serum levels of estradiol, estrone, testosterone, dihydrotestosterone (DHT), and combined estrogens and androgens in eight male marmosets 20 minutes after exposure to isolated infant scent. Testosterone and androgen levels combined were significantly lower with exposure to own infant scent than a novel infant scent when the infants were at a dependent age but not at an independent age. Estrogen levels elevated significantly in response to own infant scent when the infants were at a dependent age but not at an independent age. These results suggest that marmoset fathers are more responsive to priming cues from related infants and hormonal responses from fathers are greatest when the infant is at a dependent age.

Humans’ ability to ‘count’ by verbally labeling discrete quantities is unique in animal cognition. The evolutionary origins of counting algorithms are not understood. We report that non-human primates exhibit a cognitive ability that is algorithmically and logically similar to human counting. Monkeys were given the task of choosing between two food caches. Monkeys saw one cache baited with some number of food items, one item at a time. Then, a second cache was baited with food items, one at a time. At the point when the second set approximately outnumbered the first set, monkeys spontaneously moved to choose the second set even before it was completely baited. Using a novel Bayesian analysis, we show that monkeys used an approximate counting algorithm to increment and compare quantities in sequence. This algorithm is structurally similar to formal counting in humans and thus may have been an important evolutionary precursor to human counting.

Laboratory rhesus macaques are often housed in pairs and may be temporarily or permanently separated for research, health, or management reasons. While both long-term social separations and introductions can stimulate a stress response that impacts inflammation and immune function, the effects of short-term overnight separations and whether qualities of the pair relationship mediate these effects are unknown. In this study, we investigated the effects of overnight separations on the urinary cortisol concentration of 20 differentially paired adult female rhesus macaques (Macaca mulatta) at the California National Primate Research Center. These females were initially kept in either continuous (no overnight separation) or intermittent (with overnight separation) pair-housing and then switched to the alternate pair-housing condition part way through the study. Each study subject was observed for 5 weeks, during which we collected measures of affiliative, aggressive, anxious, abnormal, and activity-state behaviors in both pair-housing conditions. Additionally, up to three urine samples were collected from each subject per week and assayed for urinary free cortisol and creatinine. Lastly, the behavioral observer scored each pair on four relationship quality attributes ("Anxious," "Tense," "Well-meshed," and "Friendly") using a seven-point scale. Data were analyzed using a generalized linear model with gamma distribution and an information theoretic approach to determine the best model set. An interaction between the intermittent pairing condition and tense pair adjective rating was in the top three models of the best model set. Dominance and rates of affiliation were also important for explaining urinary cortisol variation. Our results suggest that to prevent significant changes in HPA-axis activation in rhesus macaque females, which could have unintended effects on research outcomes, pairs with "Tense" relationships and overnight separations preventing tactile contact should be avoided.