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.

The role of food transfers in wild golden lion tamarins (Leontopithecus rosalia): Support for the informational and nutritional hypothesis.

Callitrichidae is a unique primate family not only in terms of the large number of food transfers to infants but also for the prevalence of transfers that are initiated by the adults. It has been hypothesized that, as well as provisioning infants, callitrichid food transfers might function to teach the receiver what food types to eat. If food provisioning has a teaching function, we would expect successful food transfers to be more likely with food types that are novel to the juveniles. We would also expect juveniles to learn about foods from those transfers. We introduced different types of food (some familiar, some novel) to wild groups of golden lion tamarins (Leontopithecus rosalia). While novel foods were not more successfully transferred than familiar food in the experiment, transfers were more successful (i.e., the receiver obtained food) when the donor had previous experience with that food. Moreover, we found evidence suggesting that food transfers influenced the future foraging choices of juveniles. Our findings are consistent with the first and third criteria of the functional definition of teaching, which requires that tutors (the adults) modify their behavior in the presence of a naïve individual (a juvenile), and that the naïve individual learns from the modified behavior of the demonstrator. Our findings are also consistent with the provisioning function of food transfer. Social learning seems to play an important role in the development of young tamarins' foraging preferences.

No evidence for individual recognition in threespine or ninespine sticklebacks (Gasterosteus aculeatus or Pungitius pungitius).

Recognition plays an important role in the formation and organization of animal groups. Many animals are capable of class-level recognition, discriminating, for example, on the basis of species, kinship or familiarity. Individual recognition requires that animals recognize distinct cues, and learn to associate these with the specific individual from which they are derived. In this study, we asked whether sticklebacks (Gasterosteus aculeatus and Pungitius pungitius) were capable of learning to recognize individual conspecifics. We have used these fish as model organisms for studying selective social learning, and demonstrating a capacity for individual recognition in these species would provide an exciting opportunity for studying how biases for copying specific individuals shape the dynamics of information transmission. To test for individual recognition, we trained subjects to associate green illumination with the provision of a food reward close to one of two conspecifics, and, for comparison, one of two physical landmarks. Both species were capable of recognizing the rewarded landmark, but neither showed a preference for associating with the rewarded conspecific. Our study provides no evidence for individual recognition in either species. We speculate that the fission-fusion structure of their social groups may not favour a capacity for individual recognition.

Flexible learning, rather than inveterate innovation or copying, drives cumulative knowledge gain.

Human technology is characterized by cumulative cultural knowledge gain, yet researchers have limited knowledge of the mix of copying and innovation that maximizes progress. Here, we analyze a unique large-scale dataset originating from collaborative online programming competitions to investigate, in a setting of real-world complexity, how individual differences in innovation, social-information use, and performance generate technological progress. We find that cumulative knowledge gain is primarily driven by pragmatists, willing to copy, innovate, explore, and take risks flexibly, rather than by pure innovators or habitual copiers. Our study also reveals a key role for prestige in information transfer.

Attentional coordination in demonstrator-observer dyads facilitates learning and predicts performance in a novel manual task.

Observational learning is a form of social learning in which a demonstrator performs a target task in the company of an observer, who may as a consequence learn something about it. In this study, we approach social learning in terms of the dynamics of coordination rather than the more common perspective of transmission of information. We hypothesised that observers must continuously adjust their visual attention relative to the demonstrator's time-evolving behaviour to benefit from it. We eye-tracked observers repeatedly watching videos showing a demonstrator solving one of three manipulative puzzles before attempting at the task. The presence of the demonstrator's face and the availability of his verbal instruction in the videos were manipulated. We then used recurrence quantification analysis to measure the dynamics of coordination between the overt attention of the observers and the demonstrator's manipulative actions. Bayesian hierarchical logistic regression was applied to examine (1) whether the observers' performance was predicted by such indexes of coordination, (2) how performance changed as they accumulated experience, and (3) if the availability of speech and intentional gaze of the demonstrator mediated it. Results showed that learners better able to coordinate their eye movements with the manipulative actions of the demonstrator had an increasingly higher probability of success in solving the task. The availability of speech was beneficial to learning, whereas the presence of the demonstrator's face was not. We argue that focusing on the dynamics of coordination between individuals may greatly improve understanding of the cognitive processes underlying social learning.

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.

The reach of gene-culture coevolution in animals.

Culture (behaviour based on socially transmitted information) is present in diverse animal species, yet how it interacts with genetic evolution remains largely unexplored. Here, we review the evidence for gene-culture coevolution in animals, especially birds, cetaceans and primates. We describe how culture can relax or intensify selection under different circumstances, create new selection pressures by changing ecology or behaviour, and favour adaptations, including in other species. Finally, we illustrate how, through culturally mediated migration and assortative mating, culture can shape population genetic structure and diversity. This evidence suggests strongly that animal culture plays an important evolutionary role, and we encourage explicit analyses of gene-culture coevolution in nature.

Social learning strategies regulate the wisdom and madness of interactive crowds.

Why groups of individuals sometimes exhibit collective 'wisdom' and other times maladaptive 'herding' is an enduring conundrum. Here we show that this apparent conflict is regulated by the social learning strategies deployed. We examined the patterns of human social learning through an interactive online experiment with 699 participants, varying both task uncertainty and group size, then used hierarchical Bayesian model fitting to identify the individual learning strategies exhibited by participants. Challenging tasks elicit greater conformity among individuals, with rates of copying increasing with group size, leading to high probabilities of herding among large groups confronted with uncertainty. Conversely, the reduced social learning of small groups, and the greater probability that social information would be accurate for less-challenging tasks, generated 'wisdom of the crowd' effects in other circumstances. Our model-based approach provides evidence that the likelihood of collective intelligence versus herding can be predicted, resolving a long-standing puzzle in the literature.

A four-questions perspective on public information use in sticklebacks (Gasterosteidae).

Whether learning primarily reflects general processes or species-specific challenges is a long-standing matter of dispute. Here, we present a comprehensive analysis of public information use (PI-use) in sticklebacks (Gasterosteidae). PI-use is a form of social learning by which animals are able to assess the relative quality of resources, here prey patches, by observing the behaviour of others. PI-use was highly specific with only Pungitius and their closest relative Culaea inconstans showing evidence of PI-use. We saw no effects of ontogenetic experience upon PI-use in Pungitius pungitius. Experiments with live demonstrators and animated fish revealed that heightened activity and feeding strikes by foraging conspecifics are important cues in the transmission of PI. Finally, PI-use was the only form of learning in which P. pungitius and another stickleback, Gasterosteus aculeatus differed. PI-use in sticklebacks is species-specific and may represent an 'ecological specialization' for social foraging. Whether this reflects selection on perception, attentional or cognitive processes remains to be determined.

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.

An Open Resource for Non-human Primate Imaging.

Non-human primate neuroimaging is a rapidly growing area of research that promises to transform and scale translational and cross-species comparative neuroscience. Unfortunately, the technological and methodological advances of the past two decades have outpaced the accrual of data, which is particularly challenging given the relatively few centers that have the necessary facilities and capabilities. The PRIMatE Data Exchange (PRIME-DE) addresses this challenge by aggregating independently acquired non-human primate magnetic resonance imaging (MRI) datasets and openly sharing them via the International Neuroimaging Data-sharing Initiative (INDI). Here, we present the rationale, design, and procedures for the PRIME-DE consortium, as well as the initial release, consisting of 25 independent data collections aggregated across 22 sites (total = 217 non-human primates). We also outline the unique pitfalls and challenges that should be considered in the analysis of non-human primate MRI datasets, including providing automated quality assessment of the contributed datasets.

Developmental Bias and Evolution: A Regulatory Network Perspective.

Phenotypic variation is generated by the processes of development, with some variants arising more readily than others-a phenomenon known as "developmental bias." Developmental bias and natural selection have often been portrayed as alternative explanations, but this is a false dichotomy: developmental bias can evolve through natural selection, and bias and selection jointly influence phenotypic evolution. Here, we briefly review the evidence for developmental bias and illustrate how it is studied empirically. We describe recent theory on regulatory networks that explains why the influence of genetic and environmental perturbation on phenotypes is typically not uniform, and may even be biased toward adaptive phenotypic variation. We show how bias produced by developmental processes constitutes an evolving property able to impose direction on adaptive evolution and influence patterns of taxonomic and phenotypic diversity. Taking these considerations together, we argue that it is not sufficient to accommodate developmental bias into evolutionary theory merely as a constraint on evolutionary adaptation. The influence of natural selection in shaping developmental bias, and conversely, the influence of developmental bias in shaping subsequent opportunities for adaptation, requires mechanistic models of development to be expanded and incorporated into evolutionary theory. A regulatory network perspective on phenotypic evolution thus helps to integrate the generation of phenotypic variation with natural selection, leaving evolutionary biology better placed to explain how organisms adapt and diversify.

Innovation and cumulative culture through tweaks and leaps in online programming contests.

The ability to build progressively on the achievements of earlier generations is central to human uniqueness, but experimental investigations of this cumulative cultural evolution lack real-world complexity. Here, we studied the dynamics of cumulative culture using a large-scale data set from online collaborative programming competitions run over 14 years. We show that, within each contest population, performance increases over time through frequent 'tweaks' of the current best entry and rare innovative 'leaps' (successful tweak:leap ratio = 16:1), the latter associated with substantially greater variance in performance. Cumulative cultural evolution reduces technological diversity over time, as populations focus on refining high-performance solutions. While individual entries borrow from few sources, iterative copying allows populations to integrate ideas from many sources, demonstrating a new form of collective intelligence. Our results imply that maximising technological progress requires accepting high levels of failure.

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.

Social Learning Strategies: Bridge-Building between Fields.

While social learning is widespread, indiscriminate copying of others is rarely beneficial. Theory suggests that individuals should be selective in what, when, and whom they copy, by following 'social learning strategies' (SLSs). The SLS concept has stimulated extensive experimental work, integrated theory, and empirical findings, and created impetus to the social learning and cultural evolution fields. However, the SLS concept needs updating to accommodate recent findings that individuals switch between strategies flexibly, that multiple strategies are deployed simultaneously, and that there is no one-to-one correspondence between psychological heuristics deployed and resulting population-level patterns. The field would also benefit from the simultaneous study of mechanism and function. SLSs provide a useful vehicle for bridge-building between cognitive psychology, neuroscience, and evolutionary biology.

Human mate-choice copying is domain-general social learning.

Women appear to copy other women's preferences for men's faces. This 'mate-choice copying' is often taken as evidence of psychological adaptations for processing social information related to mate choice, for which facial information is assumed to be particularly salient. No experiment, however, has directly investigated whether women preferentially copy each other's face preferences more than other preferences. Further, because prior experimental studies used artificial social information, the effect of real social information on attractiveness preferences is unknown. We collected attractiveness ratings of pictures of men's faces, men's hands, and abstract art given by heterosexual women, before and after they saw genuine social information gathered in real time from their peers. Ratings of faces were influenced by social information, but no more or less than were images of hands and abstract art. Our results suggest that evidence for domain-specific social learning mechanisms in humans is weaker than previously suggested.

Food-Offering Calls in Wild Golden Lion Tamarins (Leontopithecus rosalia): Evidence for Teaching Behavior?

Many animals emit calls in the presence of food, but researchers do not always know the function of these calls. Evidence suggests that adult golden lion tamarins (Leontopithecus rosalia) use food-offering calls to teach juveniles which substrate (i.e., microhabitat) to forage on, or in, for food. However, we do not yet know whether juveniles learn from this aspect of the adults' behavior. Here we examine whether juveniles learn to associate food-offering calls with a foraging substrate, as a step toward assessing whether these calls qualify as teaching behavior. We compared the performance of four wild juvenile golden lion tamarins that were introduced to a novel substrate while exposed to playbacks of food-offering calls (experimental condition) to the performance of three juveniles that were exposed to the novel substrate without the presence of food-offering playbacks (control condition). We varied the location of the novel substrate between trials. We found that food-offering calls had an immediate effect on juveniles' interactions with the novel substrate, whether they inserted their hands into the substrate and their eating behavior, and a long-term effect on eating behavior at the substrate. The findings imply that juvenile golden lion tamarins can learn through food-offering calls about the availability of food at a substrate, which is consistent with (but does not prove) teaching in golden lion tamarins through stimulus enhancement. Our findings support the hypothesis that teaching might be more likely to evolve in cooperatively breeding species with complex ecological niches.

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.

Why Gupta et al.'s critique of niche construction theory is off target.

Gupta et al., in their article in this issue ('Niche construction in evolutionary theory: the construction of an academic niche?'. doi:10.1007/s12041-017-0787-6), lament 'serious problems with the way science is being done' and suggest that 'niche construction theory exemplifies this state of affairs.' However, their aggressively confrontational but superficial critique of niche construction theory (NCT) only contributes to these problems by attacking claims that NCT does not make. This is unfortunate, as their poor scholarship has done a disservice to the evolutionary biology community through propagating misinformation.We correct Gupta et al.'s misunderstandings, stressing that NCT does not suggest that the fact that organisms engage in niche construction is neglected, nor does it make strong claims on the basis of its formal theory. Moreover, the treatment of niche construction as an evolutionary process has been highly productive, and is both theoretically and empirically well-validated.We end by reflecting on the potentially deleterious implications of their publication for evolutionary science.