Aaron A. Sandel

The Evolution of Self-Control

Significance Although 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 problem-solving tasks measuring self-control and evaluated the leading hypotheses regarding how and why cognition evolves. Across species, differences in absolute (not relative) brain volume best predicted performance on these tasks. Within primates, dietary breadth also predicted cognitive performance, whereas social group size did not. These results suggest that increases in absolute brain size provided the biological foundation for evolutionary increases in self-control, and implicate species differences in feeding ecology as a potential selective pressure favoring these skills. 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.

How does cognition evolve? Phylogenetic comparative psychology

Now more than ever animal studies have the potential to test hypotheses regarding how cognition evolves. Comparative psychologists have developed new techniques to probe the cognitive mechanisms underlying animal behavior, and they have become increasingly skillful at adapting methodologies to test multiple species. Meanwhile, evolutionary biologists have generated quantitative approaches to investigate the phylogenetic distribution and function of phenotypic traits, including cognition. In particular, phylogenetic methods can quantitatively (1) test whether specific cognitive abilities are correlated with life history (e.g., lifespan), morphology (e.g., brain size), or socio-ecological variables (e.g., social system), (2) measure how strongly phylogenetic relatedness predicts the distribution of cognitive skills across species, and (3) estimate the ancestral state of a given cognitive trait using measures of cognitive performance from extant species. Phylogenetic methods can also be used to guide the selection of species comparisons that offer the strongest tests of a priori predictions of cognitive evolutionary hypotheses (i.e., phylogenetic targeting). Here, we explain how an integration of comparative psychology and evolutionary biology will answer a host of questions regarding the phylogenetic distribution and history of cognitive traits, as well as the evolutionary processes that drove their evolution.

Evidence from four lemur species that ringtailed lemur social cognition converges with that of haplorhine primates

Many haplorhine primates flexibly exploit social cues when competing for food. Whether strepsirrhine primates possess similar abilities is unknown. To explore the phylogenetic origins of such skills among primates, we tested ringtailed lemurs, Lemur catta, for their ability to exploit social cues while competing for food. We found that in two contexts ringtailed lemurs spontaneously approached food out of their competitor’s view. To assess whether these skills are related to the relatively complex social structure seen in ringtailed lemurs or shared more broadly across a range of strepsirrhines, we then compared ringtailed lemurs to three lemur species with less complex societies in the same food competition task (N ¼ 50 lemurs). Although all species skilfully avoided food proximate to a competitor in a pretest, only ringtailed lemurs performed above chance in the food competition task that required subjects to avoid food that an experimenter was facing in favour of one that he was not facing. We also compared all four species in a noncompetitive gaze-following task. Ringtailed lemurs were again the only species that looked up more frequently when an experimenter gazed into space than when an experimenter gazed forward (although at relatively low frequencies). These results are consistent with the hypothesis that ringtailed lemurs have undergone convergent social-cognitive evolution with haplorhines, possibly as an adaptation for living in the largest and most complex social groups among strepsirrhines. Results are discussed in terms of lemur cognitive evolution as well as the social intelligence hypothesis. 2011 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.

Group Size Predicts Social but Not Nonsocial Cognition in Lemurs

The social intelligence hypothesis suggests that living in large social networks was the primary selective pressure for the evolution of complex cognition in primates. This hypothesis is supported by comparative studies demonstrating a positive relationship between social group size and relative brain size across primates. However, the relationship between brain size and cognition remains equivocal. Moreover, there have been no experimental studies directly testing the association between group size and cognition across primates. We tested the social intelligence hypothesis by comparing 6 primate species (total N = 96) characterized by different group sizes on two cognitive tasks. Here, we show that a species’ typical social group size predicts performance on cognitive measures of social cognition, but not a nonsocial measure of inhibitory control. We also show that a species’ mean brain size (in absolute or relative terms) does not predict performance on either task in these species. These data provide evidence for a relationship between group size and social cognition in primates, and reveal the potential for cognitive evolution without concomitant changes in brain size. Furthermore our results underscore the need for more empirical studies of animal cognition, which have the power to reveal species differences in cognition not detectable by proxy variables, such as brain size.

Data Quality and the Comparative Method: The Case of Primate Group Size

The comparative method is frequently employed to study primate behavior and evolution. The method is used to infer adaptations, and considerable improvements have been made with respect to its implementation. Despite these advances, scant attention has been given to the nature of the data that are used in comparative analyses. This creates a potential problem as data are often compiled from studies conducted by multiple researchers, whose methods may differ, resulting in variation in data quality. In this article, we investigate the quality of data employed in studies of primate group size. Several issues concerning data quality arise when assembling data on group size. For example, data quality may be compromised if group sizes are estimated from censuses, unhabituated groups, or groups with unrecognized individuals. To mitigate these and other data quality issues, we gathered data from the literature on 23 monkeys and apes using well-defined and biologically relevant criteria for inclusion. We compare our results with those of eight published compilations of group size. Most studies did not provide details regarding the criteria for including data. We found that our group size values were uncorrelated or weakly correlated with those from three other studies and differed in a consistent fashion from those of one other study. Because conclusions derived from comparative analyses are only as accurate as the data that they use, future studies should provide details regarding data collection to ensure their reliability.

Transparency, usability, and reproducibility: Guiding principles for improving comparative databases using primates as examples

Recent decades have seen rapid development of new analytical methods to investigate patterns of interspecific variation. Yet these cutting‐edge statistical analyses often rely on data of questionable origin, varying accuracy, and weak comparability, which seem to have reduced the reproducibility of studies. It is time to improve the transparency of comparative data while also making these improved data more widely available. We, the authors, met to discuss how transparency, usability, and reproducibility of comparative data can best be achieved. We propose four guiding principles: 1) data identification with explicit operational definitions and complete descriptions of methods; 2) inclusion of metadata that capture key characteristics of the data, such as sample size, geographic coordinates, and nutrient availability (for example, captive versus wild animals); 3) documentation of the original reference for each datum; and 4) facilitation of effective interactions with the data via user friendly and transparent interfaces. We urge reviewers, editors, publishers, database developers and users, funding agencies, researchers publishing their primary data, and those performing comparative analyses to embrace these standards to increase the transparency, usability, and reproducibility of comparative studies.

Affiliation, dominance and friendship among companion dogs

Dog social behaviour has been well studied, but little is known about affiliative relationships between dogs. We report a yearlong study of dominance and affiliation in 24 dogs at a dog daycare facility and provide additional details on dog relationships through long-term observations of pairs of dogs who lived together in the same household or met frequently for years. Companion dogs formed highly differentiated relationships with one another. At daycare, some dyads affiliated and displayed one-way submission (formal dominance), others affiliated without a dominance relationship (egalitarian), and the majority of dyads did not affiliate at all (agonistic or non-interactive). The dogs in household environments showed formal and egalitarian relationships, and two dyads exchanged two-way agonism without submission (unresolved). Sex influenced the types of relationships dogs formed, with mixed sex dyads more likely to affiliate and less likely to exhibit dominance than same-sex pairs. Dominance influenced the nature of affiliation in relationships; egalitarian dyads were more likely to play and showed more equitable gentle affiliation. Gentle affiliation was reciprocal in the group as a whole, but it was highly skewed in many dyads, especially those with dominance relationships. Gentle affiliation was usually, but not always, directed up the hierarchy. Certain dyads affiliated at much higher rates than others, indicating that the dogs formed friendships. Most friends were mixed sex and/or egalitarian pairs, but friendships occurred in all of the sex class/dominance combinations. Long-term observations demonstrated how dyadic relationships can change over time. Such highly differentiated relationships suggest significant social complexity in dogs.