Evan L. MacLean

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.

Social Complexity Predicts Transitive Reasoning in Prosimian Primates.

Transitive Inference is a form of deductive reasoning that has been suggested as one cognitive mechanism by which animals could learn the many relationships within their groups dominance hierarchy. This process thus bears relevance to the social intelligence hypothesis which posits evolutionary links between various forms of social and nonsocial cognition. Recent evidence corroborates the link between social complexity and transitive inference and indicates that highly social animals may show superior transitive reasoning even in nonsocial contexts. We examined the relationship between social complexity and transitive inference in two species of prosimians, a group of primates that diverged from the common ancestor of monkeys, apes, and humans over 50 million years ago. In Experiment 1, highly social ring-tailed lemurs, Lemur catta, outperformed the less social mongoose lemurs, Eulemur mongoz, in tests of transitive inference and showed more robust representations of the underlying ordinal relationships between the stimuli. In Experiment 2, after training under a correction procedure that emphasized the underlying linear dimension of the series, both species showed similar transitive inference. This finding suggests that the two lemur species differ not in their fundamental ability to make transitive inferences, but rather in their predisposition to mentally organize information along a common underlying dimension. Together, these results support the hypothesis that social complexity is an important selective pressure for the evolution of cognitive abilities relevant to transitive reasoning.

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.

Monkeys Match and Tally Quantities across Senses.

We report here that monkeys can actively match the number of sounds they hear to the number of shapes they see and present the first evidence that monkeys sum over sounds and sights. In Experiment 1, two monkeys were trained to choose a simultaneous array of 1-9 squares that numerically matched a sample sequence of shapes or sounds. Monkeys numerically matched across (audio-visual) and within (visual-visual) modalities with equal accuracy and transferred to novel numerical values. In Experiment 2, monkeys presented with sample sequences of randomly ordered shapes or tones were able to choose an array of 2-9 squares that was the numerical sum of the shapes and sounds in the sample sequence. In both experiments, accuracy and reaction time depended on the ratio between the correct numerical match and incorrect choice. These findings suggest monkeys and humans share an abstract numerical code that can be divorced from the modality in which stimuli are first experienced.

Context specificity of inhibitory control in dogs

Across three experiments, we explored whether a dog’s capacity for inhibitory control is stable or variable across decision-making contexts. In the social task, dogs were first exposed to the reputations of a stingy experimenter that never shared food and a generous experimenter who always shared food. In subsequent test trials, dogs were required to avoid approaching the stingy experimenter when this individual offered (but withheld) a higher-value reward than the generous experimenter did. In the A-not-B task, dogs were required to inhibit searching for food in a previously rewarded location after witnessing the food being moved from this location to a novel hiding place. In the cylinder task, dogs were required to resist approaching visible food directly (because it was behind a transparent barrier), in favor of a detour reaching response. Overall, dogs exhibited inhibitory control in all three tasks. However, individual scores were not correlated between tasks, suggesting that context has a large effect on dogs’ behavior. This result mirrors studies of humans, which have highlighted intra-individual variation in inhibitory control as a function of the decision-making context. Lastly, we observed a correlation between a subject’s age and performance on the cylinder task, corroborating previous observations of age-related decline in dogs’ executive function.

Sociality, ecology, and relative brain size in lemurs

The social brain hypothesis proposes that haplorhine primates have evolved relatively large brains for their body size primarily as an adaptation for living in complex social groups. Studies that support this hypothesis have shown a strong relationship between relative brain size and group size in these taxa. Recent reports suggest that this pattern is unique to haplorhine primates; many nonprimate taxa do not show a relationship between group size and relative brain size. Rather, pairbonded social monogamy appears to be a better predictor of a large relative brain size in many nonprimate taxa. It has been suggested that haplorhine primates may have expanded the pairbonded relationship beyond simple dyads towards the evolution of complex social groups. We examined the relationship between group size, pairbonding, and relative brain size in a sample of 19 lemurs; strepsirrhine primates that last share a common ancestor with monkeys and apes approximately 75 Ma. First, we evaluated the social brain hypothesis, which predicts that species with larger social groups will have relatively larger brains. Secondly, we tested the pairbonded hypothesis, which predicts that species with a pairbonded social organization will have relatively larger brains than non-pairbonded species. We found no relationship between group size or pairbonding and relative brain size in lemurs. We conducted two further analyses to test for possible relationships between two nonsocial variables, activity pattern and diet, and relative brain size. Both diet and activity pattern are significantly associated with relative brain size in our sample. Specifically, frugivorous species have relatively larger brains than folivorous species, and cathemeral species have relatively larger brains than diurnal, but not nocturnal species. These findings highlight meaningful differences between Malagasy strepsirrhines and haplorhines, and between Malagasy strepsirrhines and nonprimate taxa, regarding the social and ecological factors associated with increases in relative brain size. The results suggest that factors such as foraging complexity and flexibility of activity patterns may have driven selection for increases in brain size in lemurs.

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.

Proteomics tools reveal startlingly high amounts of oxytocin in plasma and serum

The neuropeptide oxytocin (OT) is associated with a plethora of social behaviors, and is a key topic at the intersection of psychology and biology. However, tools for measuring OT are still not fully developed. We describe a robust nano liquid chromatography-mass spectrometry (nanoLC-MS) platform for measuring the total amount of OT in human plasma/serum. OT binds strongly to plasma proteins, but a reduction/alkylation (R/A) procedure breaks this bond, enabling ample detection of total OT. The method (R/A + robust nanoLC-MS) was used to determine total OT plasma/serum levels to startlingly high concentrations (high pg/mL-ng/mL). Similar results were obtained when combining R/A and ELISA. Compared to measuring free OT, measuring total OT can have advantages in e.g. biomarker studies.

Citizen Science as a New Tool in Dog Cognition Research

Family dogs and dog owners offer a potentially powerful way to conduct citizen science to answer questions about animal behavior that are difficult to answer with more conventional approaches. Here we evaluate the quality of the first data on dog cognition collected by citizen scientists using the Dognition.com website. We conducted analyses to understand if data generated by over 500 citizen scientists replicates internally and in comparison to previously published findings. Half of participants participated for free while the other half paid for access. The website provided each participant a temperament questionnaire and instructions on how to conduct a series of ten cognitive tests. Participation required internet access, a dog and some common household items. Participants could record their responses on any PC, tablet or smartphone from anywhere in the world and data were retained on servers. Results from citizen scientists and their dogs replicated a number of previously described phenomena from conventional lab-based research. There was little evidence that citizen scientists manipulated their results. To illustrate the potential uses of relatively large samples of citizen science data, we then used factor analysis to examine individual differences across the cognitive tasks. The data were best explained by multiple factors in support of the hypothesis that nonhumans, including dogs, can evolve multiple cognitive domains that vary independently. This analysis suggests that in the future, citizen scientists will generate useful datasets that test hypotheses and answer questions as a complement to conventional laboratory techniques used to study dog psychology.