Simon M. Reader

Integrating animal temperament within ecology and evolution

Temperament describes the idea that individual behavioural differences are repeatable over time and across situations. This common phenomenon covers numerous traits, such as aggressiveness, avoidance of novelty, willingness to take risks, exploration, and sociality. The study of temperament is central to animal psychology, behavioural genetics, pharmacology, and animal husbandry, but relatively few studies have examined the ecology and evolution of temperament traits. This situation is surprising, given that temperament is likely to exert an important influence on many aspects of animal ecology and evolution, and that individual variation in temperament appears to be pervasive amongst animal species. Possible explanations for this neglect of temperament include a perceived irrelevance, an insufficient understanding of the link between temperament traits and fitness, and a lack of coherence in terminology with similar traits often given different names, or different traits given the same name. We propose that temperament can and should be studied within an evolutionary ecology framework and provide a terminology that could be used as a working tool for ecological studies of temperament. Our terminology includes five major temperament trait categories: shyness‐boldness, exploration‐avoidance, activity, sociability and aggressiveness. This terminology does not make inferences regarding underlying dispositions or psychological processes, which may have restrained ecologists and evolutionary biologists from working on these traits. We present extensive literature reviews that demonstrate that temperament traits are heritable, and linked to fitness and to several other traits of importance to ecology and evolution. Furthermore, we describe ecologically relevant measurement methods and point to several ecological and evolutionary topics that would benefit from considering temperament, such as phenotypic plasticity, conservation biology, population sampling, and invasion biology.

Brains, innovations and evolution in birds and primates

Several comparative research programs have focused on the cognitive, life history and ecological traits that account for variation in brain size. We review one of these programs, a program that uses the reported frequency of behavioral innovation as an operational measure of cognition. In both birds and primates, innovation rate is positively correlated with the relative size of association areas in the brain, the hyperstriatum ventrale and neostriatum in birds and the isocortex and striatum in primates. Innovation rate is also positively correlated with the taxonomic distribution of tool use, as well as interspecific differences in learning. Some features of cognition have thus evolved in a remarkably similar way in primates and at least six phyletically-independent avian lineages. In birds, innovation rate is associated with the ability of species to deal with seasonal changes in the environment and to establish themselves in new regions, and it also appears to be related to the rate at which lineages diversify. Innovation rate provides a useful tool to quantify inter-taxon differences in cognition and to test classic hypotheses regarding the evolution of the brain.

Brain Size Predicts the Success of Mammal Species Introduced into Novel Environments

Large brains, relative to body size, can confer advantages to individuals in the form of behavioral flexibility. Such enhanced behavioral flexibility is predicted to carry fitness benefits to individuals facing novel or altered environmental conditions, a theory known as the brain size–environmental change hypothesis. Here, we provide the first empirical link between brain size and survival in novel environments in mammals, the largest‐brained animals on Earth. Using a global database documenting the outcome of more than 400 introduction events, we show that mammal species with larger brains, relative to their body mass, tend to be more successful than species with smaller brains at establishing themselves when introduced to novel environments, when both taxonomic and regional autocorrelations are accounted for. This finding is robust to the effect of other factors known to influence establishment success, including introduction effort and habitat generalism. Our results replicate similar findings in birds, increasing the generality of evidence for the idea that enlarged brains can provide a survival advantage in novel environments.

The evolution of primate general and cultural intelligence.

There are consistent individual differences in human intelligence, attributable to a single ‘general intelligence’ factor, g. The evolutionary basis of g and its links to social learning and culture remain controversial. Conflicting hypotheses regard primate cognition as divided into specialized, independently evolving modules versus a single general process. To assess how processes underlying culture relate to one another and other cognitive capacities, we compiled ecologically relevant cognitive measures from multiple domains, namely reported incidences of behavioural innovation, social learning, tool use, extractive foraging and tactical deception, in 62 primate species. All exhibited strong positive associations in principal component and factor analyses, after statistically controlling for multiple potential confounds. This highly correlated composite of cognitive traits suggests social, technical and ecological abilities have coevolved in primates, indicative of an across-species general intelligence that includes elements of cultural intelligence. Our composite species-level measure of general intelligence, ‘primate gS’, covaried with both brain volume and captive learning performance measures. Our findings question the independence of cognitive traits and do not support ‘massive modularity’ in primate cognition, nor an exclusively social model of primate intelligence. High general intelligence has independently evolved at least four times, with convergent evolution in capuchins, baboons, macaques and great apes.

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.

Primate Innovation: Sex, Age and Social Rank Differences

Analysis of an exhaustive survey of primate behavior collated from the published literature revealed significant variation in rates of innovation among individuals of different sex, age and social rank. We searched approximately 1,000 articles in four primatology journals, together with other relevant databases, for examples of innovation. The reported incidence of innovation is higher in males and adults, and lower in females and nonadults, than would be expected by chance given the estimated relative proportions of these groups. Amongst chimpanzees, the only species for which there are sufficient data to consider alone, there is a similar sex difference in the propensity to innovate, but no effect of age. Chimpanzees of low social rank are reported as innovators more frequently than high-ranking chimpanzees are. Male chimpanzees innovate more often than females in sexual, courtship, mating and display contexts; that is, in contexts likely to increase access to mates. The largest number of recorded observations are in the foraging context, wherein contrary to expectations, there is no evidence for female chimpanzees exhibiting more innovation than males. The study is the first extensive investigation of behavioral innovation in primates and provides evidence that much individual variation in the propensity to innovate can be explained in terms of sex, age, and social rank.

Interactions between shoal size and conformity in guppy social foraging

Previous experimental studies have established that shoaling fish forage more effectively in large than small groups. We investigated how shoal size affects the foraging efficiency of laboratory populations of the guppy, Poecilia reticulata, exposed to different foraging tasks. Experiment 1 confirmed the prediction that in open water the first fish and focal fish of larger shoals locate food faster than in smaller shoals. However, a second experiment, in which shoals of fish were required to swim through a hole in an opaque partition to locate food, found the reverse pattern: smaller shoals learned to complete the task faster than large shoals. Experiment 3, in which shoals of various sizes were exposed to a transparent maze partition, clarified the apparent contradictory results of the first two experiments, with larger shoals again learning to complete the task faster than small shoals. The findings of experiments 2 and 3 can be explained in terms of positive frequency-dependent social learning, or conformity. This facilitated social learning in large groups in experiment 3 where visual contact could be maintained through the partition, but hindered it in experiment 2 where visual contact was lost once a fish had passed through the partition. The findings raise the possibility that novel behavioural innovations, particularly those that require individuals to break contact with the group, may be more likely to spread in smaller than larger groups of animals.

The relation between social rank, neophobia and individual learning in starlings

Researchers with diverse interests in topics ranging from the formation of dominance hierarchies and social intelligence to animal personalities have predicted specific, and often conflicting, relations between social rank, neophobia and learning ability. We investigated the relations between these variables in captive groups of wild-caught starlings, Sturnus vulgaris, adopting a multidimensional approach to social rank and neophobia. Both agonistic and competitive rank orders were determined for each group and we tested individuals in the absence of their groupmates for object neophobia, latency to feed in a novel environment and performance on an extractive foraging task. In each starling group, the fastest learners occupied the highest competitive ranks, supporting the hypothesis that cognitive ability is positively correlated with social dominance. Competitive rank orders, however, did not correlate significantly with agonistic rank orders. Situation-specific foraging neophobia was suggested: individuals showed consistency in their latencies to feed near a variety of novel objects, but no significant correlation was found between this measure of object neophobia and latency to feed in a novel environment. Starlings fastest to feed in the novel environment were fastest in solving the foraging task. We discuss the implications of these findings for researchers studying hierarchy formation in animal groups, social intelligence and animal personalities.

Social learning of foraging sites and escape routes in wild Trinidadian guppies

We describe two field experiments with wild guppies, Poecilia reticulata, in Trinidad that demonstrated that guppies can acquire foraging and predator escape-response information from conspecifics. In the foraging experiment, subjects were presented with two distinctly marked feeders in their home rivers. One feeder contained a conspecific shoal in a transparent container. Guppies preferred to enter the feeder containing this artificial shoal over the other feeder. In a test phase, the artificial shoal was removed and the feeders replaced at the testing site after a 5-min delay. More guppies entered the feeder that had contained the artificial shoal over the other feeder, a difference that can be explained only by the fish learning the characteristics or location of the feeder during the training phase. We suggest that subjects acquired a foraging patch preference through a propensity to approach feeding conspecifics, a local enhancement process. In the predator escape-response experiment, naive ‘observer’ guppies could avoid an approaching trawl net by escaping through either a hole to which ‘demonstrator’ guppies had been trained or through an alternative hole. When the demonstrators were present, the naive observers escaped more often and more rapidly by the demonstrated route than the alternative route. When the demonstrators were removed, observers maintained a route preference according to the training of their demonstrators, which suggests that the observers had learned an escape route through following or observing their more knowledgeable conspecifics. Thus, both experiments reveal that guppies can socially learn in the wild. Copyright 2003 Published by Elsevier Ltd on behalf of The Association for the Study of Animal Behaviour.

The origin and spread of innovations in starlings

There are numerous reports of novel learned behaviour patterns in animal populations, yet the factors influencing the invention and spread of these innovations remain poorly understood. Here we investigated to what extent the pattern of spread of innovations in captive groups of starlings, Sturnus vulgaris, could be predicted by knowledge of individual and social group variables, including association patterns, social rank orders, measures of neophobia and asocial learning performance. We presented small groups of starlings with a series of novel extractive foraging tasks and recorded the latency for each bird to contact and solve each task, as well as the orders of contacting and solving. We then explored which variables best predicted the observed diffusion patterns. Object neophobia and social rank measures characterized who was the first of the group to contact the novel foraging tasks, and the subsequent spread of contacting tasks was associated with latency to feed in a novel environment. Asocial learning performance, measured in isolation, predicted who was the first solver of the novel foraging tasks in each group. Association patterns did not predict the spread of solving. Contact latency and solving duration were negatively correlated, consistent with social learning underlying the spread of solving. Our findings indicate that we can improve our understanding of the diffusion dynamics of innovations in animal groups by investigating group-dependent and individual variables in combination. We introduce novel methods for exploring predictors of the origin and spread of behavioural innovations that could be widely applied.