Neeltje J. Boogert

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.

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.

Technical innovations drive the relationship between innovativeness and residual brain size in birds

The hypothesis that large brains allow animals to produce novel behaviour patterns is supported by the correlation between brain size, corrected for body size, and the frequency of foraging innovations reported in the literature for both birds and primates. In birds, foraging innovations have been observed in over 800 species, and include behaviours that range from eating a novel food to using tools. Previous comparative studies have quantified innovativeness by summing all reports of innovative behaviour, regardless of the nature of the innovation. Here, we use the variety of foraging innovations recorded for birds to see which of two classic hypotheses best accounts for the relationship between innovativeness and brain size: the technical intelligence hypothesis or the opportunistic-generalism intelligence hypothesis. We classified 2182 innovation cases into 12 categories to quantify the diversity of innovations performed by each of 76 avian families. We found that families with larger brains had a greater repertoire of innovations, and that innovation diversity was a stronger predictor of residual brain size than was total number of innovations. Furthermore, the diversity of technical innovations displayed by bird families was a much better predictor of residual brain size than was the number of food type innovations, providing support for the technical intelligence hypothesis. Our results suggest that the cognitive capacity required to perform a wide variety of novel foraging techniques underpins the positive relationship between innovativeness and brain size in birds. We include a summary of innovation data for 803 species as Supplementary Material.

Song complexity correlates with learning ability in zebra finch males.

In species with mate choice, the choosy sex selects its mate based on traits that are thought to indicate the mates quality. In several bird species, females prefer males that sing more complex songs but it is unclear which aspect of male quality is signalled by this trait. Here we tested the hypothesis that a males song complexity conveys information about his learning capacity. We recorded the songs of 27 male zebra finches, Taeniopygia guttata, and quantified their complexity by measuring average song phrase duration, the total number of elements and the number of unique elements per song phrase. We then presented each male with a novel foraging task and recorded the number of trials he required to solve the task. We found a positive correlation between song complexity and learning proficiency: males with more song phrase elements required fewer learning trials to solve the novel foraging task. This result suggests that a males song complexity signals his learning ability, which may have contributed to the selective pressures driving females to choose males with more complex songs.

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.

Detecting social transmission in networks

In recent years researchers have drawn attention to a need for new methods with which to identify the spread of behavioural innovations through social transmission in animal populations. Network-based analyses seek to recognise diffusions mediated by social learning by detecting a correspondence between patterns of association and the flow of information through groups. Here we introduce a new order of acquisition diffusion analysis (OADA) and develop established time of acquisition diffusion analysis (TADA) methods further. Through simulation we compare the merits of these and other approaches, demonstrating that OADA and TADA have greater power and lower Type I error rates than available alternatives, and specifying when each approach should be deployed. We illustrate the new methods by applying them to reanalyse an established dataset corresponding to the diffusion of foraging innovations in starlings, where OADA and TADA detect social transmission that hitherto had been missed. The methods are potentially widely applicable by researchers wishing to detect social learning in natural and captive populations of animals, and to facilitate this we provide code to implement OADA and TADA in the statistical package R.

Song repertoire size in male song sparrows correlates with detour reaching, but not with other cognitive measures

Song learning is a cognitive task in which juvenile birds acquire, store and use information about adult song to shape their own song production. Comparative studies show that across bird species, performance on different cognitive tasks is usually positively correlated. If the same holds true within species, then the complexity of a male’s learned song ought to be correlated with other cognitive abilities. To test this hypothesis, we measured correlations between song repertoire size and cognitive performance in wild song sparrows, Melospiza melodia . Females prefer males with larger song repertoires in this species, and song repertoire size correlates with various fitness measures. We recorded males’ song repertoires in the field and tested these males in captivity on motor, colour association and reversal learning tasks, as well as on a detour-reaching task that measures inhibitory control. We found that individuals’ performance on the colour association task correlated positively with their performance on the reversal task, but performance did not correlate across the other learning tasks. Males with larger song repertoires were faster to solve the detour-reaching task, but performed worse on the reversal task than males with smaller song repertoires. Although our results suggest that song repertoire size does correlate with one measure of cognitive performance, more detailed song analyses and further cognitive tests are required to answer the questions raised by our findings.

The Implications of Niche Construction and Ecosystem Engineering for Conservation Biology

Abstract Although strategies to conserve biodiversity (e.g., the establishment of reserves and the management of flagship, umbrella, indicator, and keystone species) are valuable, they entail practical and conceptual difficulties. A focus on niche construction and ecosystem engineering, however, could provide new insights and methods for conservation biology. Many organisms modulate the availability of resources to other species by causing state changes in biotic or abiotic materials (ecosystem engineering), in the process frequently changing the selection to which the ecosystem engineers and other organisms are exposed (niche construction). We describe growing evidence that organisms have significant nontrophic impacts on ecosystem structure, function, and biodiversity, and outline established means of identifying key species involved in niche construction. On the basis of this engineering perspective, we propose a number of measures that could be employed to enhance conservation efforts.

Problem-solving performance is correlated with reproductive success in a wild bird population

Although interindividual variation in problem-solving ability is well documented, its relation to variation in fitness in the wild remains unclear. We investigated the relationship between performance on a problem-solving task and measures of reproductive success in a wild population of great tits, Parus major. We presented breeding pairs during the nestling provisioning period with a novel string-pulling task requiring the parents to remove an obstacle with their leg that temporarily blocked access to their nestbox. We found that nests where at least one parent solved the task had higher nestling survival until fledging than nests where both parents were nonsolvers. Furthermore, clutch size, hatching success and fledgling number were positively correlated with speed in solving the task. Our study suggests that natural selection may directly act on interindividual variation in problem-solving performance. In light of these results, the mechanisms maintaining between-individual variation in problem-solving performance in natural populations need further investigation.

Climatic Patterns Predict the Elaboration of Song Displays in Mockingbirds

Climatic variability and unpredictability affect the distribution and abundance of resources and the timing and duration of breeding opportunities. In vertebrates, climatic variability selects for enhanced cognition when organisms compensate for environmental changes through learning and innovation. This hypothesis is supported by larger brain sizes, higher foraging innovation rates, higher reproductive flexibility, and higher sociality in species living in more variable climates. Male songbirds sing to attract females and repel rivals. Given the reliance of these displays on learning and innovation, we hypothesized that they could also be affected by climatic patterns. Here we show that in the mockingbird family (Aves: Mimidae), species subject to more variable and unpredictable climates have more elaborate song displays. We discuss two potential mechanisms for this result, both of which acknowledge that the complexity of song displays is largely driven by sexual selection. First, stronger selection in more variable and unpredictable climates could lead to the elaboration of signals of quality. Alternatively, selection for enhanced learning and innovation in more variable and unpredictable climates might lead to the evolution of signals of intelligence in the context of mate attraction.