Global drivers of variation in cup nest size in passerine birds.

The size of a bird's nest can play a key role in ensuring reproductive success and is determined by a variety of factors. The primary function of the nest is to protect offspring from the environment and predators. Field studies in a number of passerine species have indicated that higher-latitude populations in colder habitats build larger nests with thicker walls compared to lower-latitude populations, but that these larger nests are more vulnerable to predation. Increases in nest size can also be driven by sexual selection, as nest size can act as a signal of parental quality and prompt differential investment in other aspects of care. It is unknown, however, how these microevolutionary patterns translate to a macroevolutionary scale. Here, we investigate potential drivers of variation in the outer and inner volume of open cup nests using a large dataset of nest measurements from 1117 species of passerines breeding in a diverse range of environments. Our dataset is sourced primarily from the nest specimens at the Natural History Museum (UK), complemented with information from ornithological handbooks and online databases. We use phylogenetic comparative methods to test long-standing hypotheses about potential macroevolutionary correlates of nest size, namely nest location, clutch size and variables relating to parental care, together with environmental and geographical factors such as temperature, rainfall, latitude and insularity. After controlling for phylogeny and parental body size, we demonstrate that the outer volume of the nest is greater in colder climates, in island-dwelling species and in species that nest on cliffs or rocks. By contrast, the inner cup volume is associated solely with average clutch size, increasing with the number of chicks raised in the nest. We do not find evidence that nest size is related to the length of parental care for nestlings. Our study reveals that the average temperature in the breeding range, along with several key life-history traits and proxies of predation threat, shapes the global interspecific variation in passerine cup nest size. We also showcase the utility of museum nest collections-a historically underused resource-for large-scale studies of trait evolution.

Animal learning as a source of developmental bias.

As a form of adaptive plasticity that allows organisms to shift their phenotype toward the optimum, learning is inherently a source of developmental bias. Learning may be of particular significance to the evolutionary biology community because it allows animals to generate adaptively biased novel behavior tuned to the environment and, through social learning, to propagate behavioral traits to other individuals, also in an adaptively biased manner. We describe several types of developmental bias manifest in learning, including an adaptive bias, historical bias, origination bias, and transmission bias, stressing that these can influence evolutionary dynamics through generating nonrandom phenotypic variation and/or nonrandom environmental states. Theoretical models and empirical data have established that learning can impose direction on adaptive evolution, affect evolutionary rates (both speeding up and slowing down responses to selection under different conditions) and outcomes, influence the probability of populations reaching global optimum, and affect evolvability. Learning is characterized by highly specific, path-dependent interactions with the (social and physical) environment, often resulting in new phenotypic outcomes. Consequently, learning regularly introduces novelty into phenotype space. These considerations imply that learning may commonly generate plasticity first evolution.

Coevolution of cultural intelligence, extended life history, sociality, and brain size in primates.

Explanations for primate brain expansion and the evolution of human cognition and culture remain contentious despite extensive research. While multiple comparative analyses have investigated variation in brain size across primate species, very few have addressed why primates vary in how much they use social learning. Here, we evaluate the hypothesis that the enhanced reliance on socially transmitted behavior observed in some primates has coevolved with enlarged brains, complex sociality, and extended lifespans. Using recently developed phylogenetic comparative methods we show that, across primate species, a measure of social learning proclivity increases with absolute and relative brain volume, longevity (specifically reproductive lifespan), and social group size, correcting for research effort. We also confirm relationships of absolute and relative brain volume with longevity (both juvenile period and reproductive lifespan) and social group size, although longevity is generally the stronger predictor. Relationships between social learning, brain volume, and longevity remain when controlling for maternal investment and are therefore not simply explained as a by-product of the generally slower life history expected for larger brained species. Our findings suggest that both brain expansion and high reliance on culturally transmitted behavior coevolved with sociality and extended lifespan in primates. This coevolution is consistent with the hypothesis that the evolution of large brains, sociality, and long lifespans has promoted reliance on culture, with reliance on culture in turn driving further increases in brain volume, cognitive abilities, and lifespans in some primate lineages.

Some topics in theoretical population genetics: Editorial commentaries on a selection of Marc Feldman's TPB papers.

This article consists of commentaries on a selected group of papers of Marc Feldman published in Theoretical Population Biology from 1970 to the present. The papers describe a diverse set of population-genetic models, covering topics such as cultural evolution, social evolution, and the evolution of recombination. The commentaries highlight Marc Feldman's role in providing mathematically rigorous formulations to explore qualitative hypotheses, in many cases generating surprising conclusions.

Selective copying of the majority suggests children are broadly "optimal-" rather than "over-" imitators.

Human children, in contrast to other species, are frequently cast as prolific "over-imitators". However, previous studies of "over-imitation" have overlooked many important real-world social dynamics, and may thus provide an inaccurate account of this seemingly puzzling and potentially maladaptive phenomenon. Here we investigate this topic using a cultural evolutionary approach, focusing particularly on the key adaptive learning strategy of majority-biased copying. Most "over-imitation" research has been conducted using consistent demonstrations to the observer, but we systematically varied the frequency of demonstrators that 4- to 6-year-old children observed performing a causally irrelevant action. Children who "over-imitate" inflexibly should copy the majority regardless of whether the majority solution omits or includes a causally irrelevant action. However, we found that children calibrated their tendency to acquire the majority behavior, such that copying did not extend to majorities that performed irrelevant actions. These results are consistent with a highly functional, adaptive integration of social and causal information, rather than explanations implying unselective copying or causal misunderstanding. This suggests that our species might be better characterized as broadly "optimal-" rather than "over-" imitators.

Primate Brain Anatomy: New Volumetric MRI Measurements for Neuroanatomical Studies.

Since the publication of the primate brain volumetric dataset of Stephan and colleagues in the early 1980s, no major new comparative datasets covering multiple brain regions and a large number of primate species have become available. However, technological and other advances in the last two decades, particularly magnetic resonance imaging (MRI) and the creation of institutions devoted to the collection and preservation of rare brain specimens, provide opportunities to rectify this situation. Here, we present a new dataset including brain region volumetric measurements of 39 species, including 20 species not previously available in the literature, with measurements of 16 brain areas. These volumes were extracted from MRI of 46 brains of 38 species from the Netherlands Institute of Neuroscience Primate Brain Bank, scanned at high resolution with a 9.4-T scanner, plus a further 7 donated MRI of 4 primate species. Partial measurements were made on an additional 8 brains of 5 species. We make the dataset and MRI scans available online in the hope that they will be of value to researchers conducting comparative studies of primate evolution.

The evolution of social learning mechanisms and cultural phenomena in group foragers.

BACKGROUND: Advanced cognitive abilities are widely thought to underpin cultural traditions and cumulative cultural change. In contrast, recent simulation models have found that basic social influences on learning suffice to support both cultural phenomena. In the present study we test the predictions of these models in the context of skill learning, in a model with stochastic demographics, variable group sizes, and evolved parameter values, exploring the cultural ramifications of three different social learning mechanisms. RESULTS: Our results show that that simple forms of social learning such as local enhancement, can generate traditional differences in the context of skill learning. In contrast, we find cumulative cultural change is supported by observational learning, but not local or stimulus enhancement, which supports the idea that advanced cognitive abilities are important for generating this cultural phenomenon in the context of skill learning. CONCLUSIONS: Our results help to explain the observation that animal cultures are widespread, but cumulative cultural change might be rare.

The magnitude of innovation and its evolution in social animals.

Innovative behaviour in animals, ranging from invertebrates to humans, is increasingly recognized as an important topic for investigation by behavioural researchers. However, what constitutes an innovation remains controversial, and difficult to quantify. Drawing on a broad definition whereby any behaviour with a new component to it is an innovation, we propose a quantitative measure, which we call the magnitude of innovation, to describe the extent to which an innovative behaviour is novel. This allows us to distinguish between innovations that are a slight change to existing behaviours (low magnitude), and innovations that are substantially different (high magnitude). Using mathematical modelling and evolutionary computer simulations, we explored how aspects of social interaction, cognition and natural selection affect the frequency and magnitude of innovation. We show that high-magnitude innovations are likely to arise regularly even if the frequency of innovation is low, as long as this frequency is relatively constant, and that the selectivity of social learning and the existence of social rewards, such as prestige and royalties, are crucial for innovative behaviour to evolve. We suggest that consideration of the magnitude of innovation may prove a useful tool in the study of the evolution of cognition and of culture.

Extended spider cognition.

There is a tension between the conception of cognition as a central nervous system (CNS) process and a view of cognition as extending towards the body or the contiguous environment. The centralised conception requires large or complex nervous systems to cope with complex environments. Conversely, the extended conception involves the outsourcing of information processing to the body or environment, thus making fewer demands on the processing power of the CNS. The evolution of extended cognition should be particularly favoured among small, generalist predators such as spiders, and here, we review the literature to evaluate the fit of empirical data with these contrasting models of cognition. Spiders do not seem to be cognitively limited, displaying a large diversity of learning processes, from habituation to contextual learning, including a sense of numerosity. To tease apart the central from the extended cognition, we apply the mutual manipulability criterion, testing the existence of reciprocal causal links between the putative elements of the system. We conclude that the web threads and configurations are integral parts of the cognitive systems. The extension of cognition to the web helps to explain some puzzling features of spider behaviour and seems to promote evolvability within the group, enhancing innovation through cognitive connectivity to variable habitat features. Graded changes in relative brain size could also be explained by outsourcing information processing to environmental features. More generally, niche-constructed structures emerge as prime candidates for extending animal cognition, generating the selective pressures that help to shape the evolving cognitive system.

Skill learning and the evolution of social learning mechanisms.

BACKGROUND: Social learning is potentially advantageous, but evolutionary theory predicts that (i) its benefits may be self-limiting because social learning can lead to information parasitism, and (ii) these limitations can be mitigated via forms of selective copying. However, these findings arise from a functional approach in which learning mechanisms are not specified, and which assumes that social learning avoids the costs of asocial learning but does not produce information about the environment. Whether these findings generalize to all kinds of social learning remains to be established. Using a detailed multi-scale evolutionary model, we investigate the payoffs and information production processes of specific social learning mechanisms (including local enhancement, stimulus enhancement and observational learning) and their evolutionary consequences in the context of skill learning in foraging groups. RESULTS: We find that local enhancement does not benefit foraging success, but could evolve as a side-effect of grouping. In contrast, stimulus enhancement and observational learning can be beneficial across a wide range of environmental conditions because they generate opportunities for new learning outcomes. CONCLUSIONS: In contrast to much existing theory, we find that the functional outcomes of social learning are mechanism specific. Social learning nearly always produces information about the environment, and does not always avoid the costs of asocial learning or support information parasitism. Our study supports work emphasizing the value of incorporating mechanistic detail in functional analyses.

How culture shaped the human genome: bringing genetics and the human sciences together.

Researchers from diverse backgrounds are converging on the view that human evolution has been shaped by gene-culture interactions. Theoretical biologists have used population genetic models to demonstrate that cultural processes can have a profound effect on human evolution, and anthropologists are investigating cultural practices that modify current selection. These findings are supported by recent analyses of human genetic variation, which reveal that hundreds of genes have been subject to recent positive selection, often in response to human activities. Here, we collate these data, highlighting the considerable potential for cross-disciplinary exchange to provide novel insights into how culture has shaped the human genome.

The extended evolutionary synthesis: its structure, assumptions and predictions.

Scientific activities take place within the structured sets of ideas and assumptions that define a field and its practices. The conceptual framework of evolutionary biology emerged with the Modern Synthesis in the early twentieth century and has since expanded into a highly successful research program to explore the processes of diversification and adaptation. Nonetheless, the ability of that framework satisfactorily to accommodate the rapid advances in developmental biology, genomics and ecology has been questioned. We review some of these arguments, focusing on literatures (evo-devo, developmental plasticity, inclusive inheritance and niche construction) whose implications for evolution can be interpreted in two ways­one that preserves the internal structure of contemporary evolutionary theory and one that points towards an alternative conceptual framework. The latter, which we label the 'extended evolutionary synthesis' (EES), retains the fundaments of evolutionary theory, but differs in its emphasis on the role of constructive processes in development and evolution, and reciprocal portrayals of causation. In the EES, developmental processes, operating through developmental bias, inclusive inheritance and niche construction, share responsibility for the direction and rate of evolution, the origin of character variation and organism-environment complementarity. We spell out the structure, core assumptions and novel predictions of the EES, and show how it can be deployed to stimulate and advance research in those fields that study or use evolutionary biology.

The development of adaptive conformity in young children: effects of uncertainty and consensus.

Human culture relies on extensive use of social transmission, which must be integrated with independently acquired (i.e. asocial) information for effective decision-making. Formal evolutionary theory predicts that natural selection should favor adaptive learning strategies, including a bias to copy when uncertain, and a bias to disproportionately copy the majority (known as 'conformist transmission'). Although the function and causation of these evolved strategies has been comparatively well studied, little is known of their development. We experimentally investigated the development of the bias to copy-when-uncertain and conformist transmission in children from the ages of 3 to 7, testing predictions derived from theoretical models. Children first attempted to solve a binary-choice quantity discrimination task themselves using asocial information, but were then given the decisions of informants, and an opportunity to revise their answer. We investigated whether children's revised judgments were adaptively contingent on (i) the difficulty of the trial and (ii) the degree of consensus amongst informants. As predicted, older but not younger children copied others more on more difficult trials than on easier trials, even though older children also showed a tendency to stick with their initial, asocial decision. We also found that older children, like adults, were disproportionately receptive to non-total majorities (i.e. were conformist) whereas younger children were receptive only to total (i.e. unanimous) majorities. We conclude that, whilst the mechanism for incorporating social information into decision-making is initially very blunt, across the course of early childhood it converges on the adaptive learning mechanisms observed in adults and predicted by cultural evolutionary theory. A video abstract of this article can be viewed at http://youtu.be/Qb6JINGYqVk.

The local enhancement conundrum: in search of the adaptive value of a social learning mechanism.

Social learning mechanisms are widely thought to vary in their degree of complexity as well as in their prevalence in the natural world. While learning the properties of a stimulus that generalize to similar stimuli at other locations (stimulus enhancement) prima facie appears more useful to an animal than learning about a specific stimulus at a specific location (local enhancement), empirical evidence suggests that the latter is much more widespread in nature. Simulating populations engaged in a producer-scrounger game, we sought to deploy mathematical models to identify the adaptive benefits of reliance on local enhancement and/or stimulus enhancement, and the alternative conditions favoring their evolution. Surprisingly, we found that while stimulus enhancement readily evolves, local enhancement is advantageous only under highly restricted conditions: when generalization of information was made unreliable or when error in social learning was high. Our results generate a conundrum over how seemingly conflicting empirical and theoretical findings can be reconciled. Perhaps the prevalence of local enhancement in nature is due to stimulus enhancement costs independent of the learning task itself (e.g. predation risk), perhaps natural habitats are often characterized by unreliable yet highly rewarding payoffs, or perhaps local enhancement occurs less frequently, and stimulus enhancement more frequently, than widely believed.

Darwin in mind: new opportunities for evolutionary psychology.

Evolutionary Psychology (EP) views the human mind as organized into many modules, each underpinned by psychological adaptations designed to solve problems faced by our Pleistocene ancestors. We argue that the key tenets of the established EP paradigm require modification in the light of recent findings from a number of disciplines, including human genetics, evolutionary biology, cognitive neuroscience, developmental psychology, and paleoecology. For instance, many human genes have been subject to recent selective sweeps; humans play an active, constructive role in co-directing their own development and evolution; and experimental evidence often favours a general process, rather than a modular account, of cognition. A redefined EP could use the theoretical insights of modern evolutionary biology as a rich source of hypotheses concerning the human mind, and could exploit novel methods from a variety of adjacent research fields.

Environmental complexity influences association network structure and network-based diffusion of foraging information in fish shoals.

Socially transmitted information can significantly affect the ways in which animals interact with their environments. We used network-based diffusion analysis, a novel and powerful tool for exploring information transmission, to model the rate at which sticklebacks (Gasterosteus aculeatus) discovered prey patches, comparing shoals foraging in open and structured environments. We found that for groups in the open environment, individuals tended to recruit to both the prey patch and empty comparison patches at similar times, suggesting that patch discovery was not greatly affected by direct social transmission. In contrast, in structured environments we found strong evidence that information about prey patch location was socially transmitted and moreover that the pathway of information transmission followed the shoals' association network structures. Our findings highlight the importance of considering habitat structure when investigating the diffusion of information through populations and imply that association networks take on greater ecological significance in structured than open environments.

Tradeoffs between the strength of conformity and number of conformists in variable environments.

Organisms often respond to environmental change phenotypically, through learning strategies that enhance fitness in variable and changing conditions. But which strategies should we expect in population exposed to those conditions? We address this question by developing a mathematical model that specifies the consequences of different mixtures of individual and social learning strategies on the frequencies of different cultural variants in temporally and spatially changing environments. Assuming that alternative cultural variants are differently well-adapted to diverse environmental conditions, we are able to evaluate which mixture of learning strategies maximises the mean fitness of the population. We find that, even in rapidly changing environments, a high proportion of the population will always engage in social learning. In those environments, the highest adaptation levels are achieved through relatively high fractions of individual learning and a strong conformist bias. We establish a negative relationship between the proportion of the population learning socially and the strength of conformity operating in a population: strong conformity requires fewer conformists (i.e. larger proportion of individual learning), while many conformists can only be found when conformist transmission is weak. Investigations of cultural diversity show that in frequently changing environments high levels of adaptation require high level of cultural diversity. Finally, we demonstrate how the developed mathematical framework can be applied to time series of usage or occurrence data of cultural traits. Using Approximate Bayesian Computation we are able to infer information about the underlying learning processes that could have produced observed patterns of variation in the dataset.