Aggressive interactions influence cognitive performance in Western Australian magpies.

Extensive research has investigated the relationship between the social environment and cognition, suggesting that social complexity may drive cognitive evolution and development. However, evidence for this relationship remains equivocal. Group size is often used as a measure of social complexity, but this may not capture intraspecific variation in social interactions. Social network analysis can provide insight into the cognitively demanding challenges associated with group living at the individual level. Here, we use social networks to investigate whether the cognitive performance of wild Western Australian magpies (Gymnorhina tibicen dorsalis) is related to group size and individual social connectedness. We quantified social connectedness using four interaction types: proximity, affiliative, agonistic and vocal. Consistent with previous research on this species, individuals in larger groups performed better on an associative learning task. However, social network position was also related to cognitive performance. Individuals receiving aggressive interactions performed better, while those involved in aggressive interactions with more group members performed worse. Overall, this suggests that cognitive performance is related to specific types of social interaction. The findings from this study highlight the value of considering fine-grained metrics of sociality that capture the challenges associated with social life when testing the relationship between the social environment and cognition.

Cognitive performance is linked to group size and affects fitness in Australian magpies.

The social intelligence hypothesis states that the demands of social life drive cognitive evolution. This idea receives support from comparative studies that link variation in group size or mating systems with cognitive and neuroanatomical differences across species, but findings are contradictory and contentious. To understand the cognitive consequences of sociality, it is also important to investigate social variation within species. Here we show that in wild, cooperatively breeding Australian magpies, individuals that live in large groups show increased cognitive performance, which is linked to increased reproductive success. Individual performance was highly correlated across four cognitive tasks, indicating a 'general intelligence factor' that underlies cognitive performance. Repeated cognitive testing of juveniles at different ages showed that the correlation between group size and cognition emerged in early life, suggesting that living in larger groups promotes cognitive development. Furthermore, we found a positive association between the task performance of females and three indicators of reproductive success, thus identifying a selective benefit of greater cognitive performance. Together, these results provide intraspecific evidence that sociality can shape cognitive development and evolution.

Competition and generalization impede cultural formation in wild jackdaws.

Animal cultures have now been demonstrated experimentally in diverse taxa from flies to great apes. However, experiments commonly use tasks with unrestricted access to equal pay-offs and innovations seeded by demonstrators who are trained to exhibit strong preferences. Such conditions may not reflect those typically found in nature. For example, the learned preferences of natural innovators may be weaker, while competition for depleting resources can favour switching between strategies and generalizing from past experience. Here we show that in experiments where wild jackdaws (Corvus monedula) can freely discover depleting supplies of novel foods, generalization has a powerful effect on learning, allowing individuals to exploit multiple new opportunities through both social and individual learning. Further, in contrast to studies with trained demonstrators, individuals that were first to innovate showed weak preferences. As a consequence, many individuals ate all available novel foods, displaying no strong preference and no group-level culture emerged. Individuals followed a 'learn from adults' strategy, but other demographic factors played a minimal role in shaping social transmission. These results demonstrate the importance of generalization in allowing animals to exploit new opportunities and highlight how natural competitive dynamics may impede the formation of culture.

High temperatures are associated with reduced cognitive performance in wild southern pied babblers.

Global temperatures are increasing rapidly. While considerable research is accumulating regarding the lethal and sublethal effects of heat on wildlife, its potential impact on animal cognition has received limited attention. Here, we tested wild southern pied babblers (Turdoides bicolor) on three cognitive tasks (associative learning, reversal learning and inhibitory control) under naturally occurring heat stress and non-heat stress conditions. We determined whether cognitive performance was explained by temperature, heat dissipation behaviours, individual and social attributes, or proxies of motivation. We found that temperature, but not heat dissipation behaviours, predicted variation in associative learning performance. Individuals required on average twice as many trials to learn an association when the maximum temperature during testing exceeded 38°C compared with moderate temperatures. Higher temperatures during testing were also associated with reduced inhibitory control performance, but only in females. By contrast, we found no temperature-related decline in performance in the reversal learning task, albeit individuals reached learning criterion in only 14 reversal learning tests. Our findings provide novel evidence of temperature-mediated cognitive impairment in a wild animal and indicate that its occurrence depends on the cognitive trait examined and individual sex.

Cognition mediates response to anthropogenic noise in wild Western Australian magpies (Gmynorhina tibicen dorsalis).

Anthropogenic noise is a pollutant of growing concern, with wide-ranging effects on taxa across ecosystems. Until recently, studies investigating the effects of anthropogenic noise on animals focused primarily on population-level consequences, rather than individual-level impacts. Individual variation in response to anthropogenic noise may result from extrinsic or intrinsic factors. One such intrinsic factor, cognitive performance, varies between individuals and is hypothesised to aid behavioural response to novel stressors. Here, we combine cognitive testing, behavioural focals and playback experiments to investigate how anthropogenic noise affects the behaviour and anti-predator response of Western Australian magpies (Gymnorhina tibicen dorsalis), and to determine whether this response is linked to cognitive performance. We found a significant population-level effect of anthropogenic noise on the foraging effort, foraging efficiency, vigilance, vocalisation rate and anti-predator response of magpies, with birds decreasing their foraging, vocalisation behaviours and anti-predator response, and increasing vigilance when loud anthropogenic noise was present. We also found that individuals varied in their response to playbacks depending on their cognitive performance, with individuals that performed better in an associative learning task maintaining their anti-predator response when an alarm call was played in anthropogenic noise. Our results add to the growing body of literature documenting the adverse effects of anthropogenic noise on wildlife and provide the first evidence for an association between individual cognitive performance and behavioural responses to anthropogenic noise.

Genetic and context-specific effects on individual inhibitory control performance in the guppy (Poecilia reticulata).

Among-individual variation in cognitive traits, widely assumed to have evolved under adaptive processes, is increasingly being demonstrated across animal taxa. As variation among individuals is required for natural selection, characterizing individual differences and their heritability is important to understand how cognitive traits evolve. Here, we use a quantitative genetic study of wild-type guppies repeatedly exposed to a 'detour task' to test for genetic variance in the cognitive trait of inhibitory control. We also test for genotype-by-environment interactions (GxE) by testing related fish under alternative experimental treatments (transparent vs. semi-transparent barrier in the detour-task). We find among-individual variation in detour task performance, consistent with differences in inhibitory control. However, analysis of GxE reveals that heritable factors only contribute to performance variation in one treatment. This suggests that the adaptive evolutionary potential of inhibitory control (and/or other latent variables contributing to task performance) may be highly sensitive to environmental conditions. The presence of GxE also implies that the plastic response of detour task performance to treatment environment is genetically variable. Our results are consistent with a scenario where variation in individual inhibitory control stems from complex interactions between heritable and plastic components.

General cognitive performance declines with female age and is negatively related to fledging success in a wild bird.

Identifying the causes and fitness consequences of intraspecific variation in cognitive performance is fundamental to understand how cognition evolves. Selection may act on different cognitive traits separately or jointly as part of the general cognitive performance (GCP) of the individual. To date, few studies have examined simultaneously whether individual cognitive performance covaries across different cognitive tasks, the relative importance of individual and social attributes in determining cognitive variation, and its fitness consequences in the wild. Here, we tested 38 wild southern pied babblers (Turdoides bicolor) on a cognitive test battery targeting associative learning, reversal learning and inhibitory control. We found that a single factor explained 59.5% of the variation in individual cognitive performance across tasks, suggestive of a general cognitive factor. GCP varied by age and sex; declining with age in females but not males. Older females also tended to produce a higher average number of fledglings per year compared to younger females. Analysing over 10 years of breeding data, we found that individuals with lower general cognitive performance produced more fledglings per year. Collectively, our findings support the existence of a trade-off between cognitive performance and reproductive success in a wild bird.

Velocity correlations in jackdaw flocks in different ecological contexts.

Velocity correlation is an important feature for animal groups performing collective motions. Previous studies have mostly focused on the velocity correlation in a single ecological context. It is unclear whether correlation characteristics vary in a single species in different contexts. Here, we studied the velocity correlations in jackdaw flocks in two different contexts: transit flocks where birds travel from one location to another, and mobbing flocks where birds respond to an external stimulus. We found that in both contexts, although the interaction rules are different, the velocity correlations remain scale-free, i.e. the correlation length (the distance over which the velocity of two individuals is similar) increases linearly with the group size. Furthermore, we found that the correlation length is independent of the group density for transit flocks, but increases with increasing group density in mobbing flocks. This result confirms a previous observation that birds obey topological interactions in transit flocks, but switch to metric interactions in mobbing flocks. Finally, in both contexts, the impact of group polarization on correlation length is not significant. Our results suggest that wild animals are always able to respond coherently to perturbations regardless of context.

A deepening understanding of animal culture suggests lessons for conservation.

A key goal of conservation is to protect biodiversity by supporting the long-term persistence of viable, natural populations of wild species. Conservation practice has long been guided by genetic, ecological and demographic indicators of risk. Emerging evidence of animal culture across diverse taxa and its role as a driver of evolutionary diversification, population structure and demographic processes may be essential for augmenting these conventional conservation approaches and decision-making. Animal culture was the focus of a ground-breaking resolution under the Convention on the Conservation of Migratory Species of Wild Animals (CMS), an international treaty operating under the UN Environment Programme. Here, we synthesize existing evidence to demonstrate how social learning and animal culture interact with processes important to conservation management. Specifically, we explore how social learning might influence population viability and be an important resource in response to anthropogenic change, and provide examples of how it can result in phenotypically distinct units with different, socially learnt behavioural strategies. While identifying culture and social learning can be challenging, indirect identification and parsimonious inferences may be informative. Finally, we identify relevant methodologies and provide a framework for viewing behavioural data through a cultural lens which might provide new insights for conservation management.

Experimentally induced innovations lead to persistent culture via conformity in wild birds.

In human societies, cultural norms arise when behaviours are transmitted through social networks via high-fidelity social learning. However, a paucity of experimental studies has meant that there is no comparable understanding of the process by which socially transmitted behaviours might spread and persist in animal populations. Here we show experimental evidence of the establishment of foraging traditions in a wild bird population. We introduced alternative novel foraging techniques into replicated wild sub-populations of great tits (Parus major) and used automated tracking to map the diffusion, establishment and long-term persistence of the seeded innovations. Furthermore, we used social network analysis to examine the social factors that influenced diffusion dynamics. From only two trained birds in each sub-population, the information spread rapidly through social network ties, to reach an average of 75% of individuals, with a total of 414 knowledgeable individuals performing 57,909 solutions over all replicates. The sub-populations were heavily biased towards using the technique that was originally introduced, resulting in established local traditions that were stable over two generations, despite a high population turnover. Finally, we demonstrate a strong effect of social conformity, with individuals disproportionately adopting the most frequent local variant when first acquiring an innovation, and continuing to favour social information over personal information. Cultural conformity is thought to be a key factor in the evolution of complex culture in humans. In providing the first experimental demonstration of conformity in a wild non-primate, and of cultural norms in foraging techniques in any wild animal, our results suggest a much broader taxonomic occurrence of such an apparently complex cultural behaviour.

The value of teaching increases with tool complexity in cumulative cultural evolution.

Human cumulative cultural evolution (CCE) is recognized as a powerful ecological and evolutionary force, but its origins are poorly understood. The long-standing view that CCE requires specialized social learning processes such as teaching has recently come under question, and cannot explain why such processes evolved in the first place. An alternative, but largely untested, hypothesis is that these processes gradually coevolved with an increasing reliance on complex tools. To address this, we used large-scale transmission chain experiments (624 participants), to examine the role of different learning processes in generating cumulative improvements in two tool types of differing complexity. Both tool types increased in efficacy across experimental generations, but teaching only provided an advantage for the more complex tools. Moreover, while the simple tools tended to converge on a common design, the more complex tools maintained a diversity of designs. These findings indicate that the emergence of cumulative culture is not strictly dependent on, but may generate selection for, teaching. As reliance on increasingly complex tools grew, so too would selection for teaching, facilitating the increasingly open-ended evolution of cultural artefacts.

Supporting the weight of the elephant in the room: Technical intelligence propped up by social cognition and language.

We consider the evolutionary plausibility of Osiurak and Reynaud's (O&R) arguments. We argue that technical reasoning is not quite the magic bullet that O&R assume, and instead propose a co-evolutionary account of the interplay between technical reasoning and social learning, with language emerging as a vital issue neglected in O&R's account.

Local interactions and their group-level consequences in flocking jackdaws.

As one of nature's most striking examples of collective behaviour, bird flocks have attracted extensive research. However, we still lack an understanding of the attractive and repulsive forces that govern interactions between individuals within flocks and how these forces influence neighbours' relative positions and ultimately determine the shape of flocks. We address these issues by analysing the three-dimensional movements of wild jackdaws ( Corvus monedula) in flocks containing 2-338 individuals. We quantify the social interaction forces in large, airborne flocks and find that these forces are highly anisotropic. The long-range attraction in the direction perpendicular to the movement direction is stronger than that along it, and the short-range repulsion is generated mainly by turning rather than changing speed. We explain this phenomenon by considering wingbeat frequency and the change in kinetic and gravitational potential energy during flight, and find that changing the direction of movement is less energetically costly than adjusting speed for birds. Furthermore, our data show that collision avoidance by turning can alter local neighbour distributions and ultimately change the group shape. Our results illustrate the macroscopic consequences of anisotropic interaction forces in bird flocks, and help to draw links between group structure, local interactions and the biophysics of animal locomotion.

Evidence for individual discrimination and numerical assessment in collective antipredator behaviour in wild jackdaws (Corvus monedula).

Collective responses to threats occur throughout the animal kingdom but little is known about the cognitive processes underpinning them. Antipredator mobbing is one such response. Approaching a predator may be highly risky, but the individual risk declines and the likelihood of repelling the predator increases in larger mobbing groups. The ability to appraise the number of conspecifics involved in a mobbing event could therefore facilitate strategic decisions about whether to join. Mobs are commonly initiated by recruitment calls, which may provide valuable information to guide decision-making. We tested whether the number of wild jackdaws responding to recruitment calls was influenced by the number of callers. As predicted, playbacks simulating three or five callers tended to recruit more individuals than playbacks of one caller. Recruitment also substantially increased if recruits themselves produced calls. These results suggest that jackdaws use individual vocal discrimination to assess the number of conspecifics involved in initiating mobbing events, and use this information to guide their responses. Our results show support for the use of numerical assessment in antipredator mobbing responses and highlight the need for a greater understanding of the cognitive processes involved in collective behaviour.

Smarter through group living: A response to Smulders.

We recently identified a strong, positive relationship between group size and individual cognitive performance, and a strong, positive relationship between female cognitive performance and reproductive success (Ashton, Ridley, Edwards, & Thornton in Nature, 554, 364-367, 2018). An opinion piece by Smulders (Learning & Behavior, https://doi.org/10.3758/s13420-018-0335-0, 2018) raised the interesting notion that these patterns may be underlined by motivational factors. In this commentary, we highlight why none of the available data are consistent with this explanation, but instead support the argument that the demands of group living influence cognitive development, with knock-on consequences for fitness.

What is cumulative cultural evolution?

In recent years, the phenomenon of cumulative cultural evolution (CCE) has become the focus of major research interest in biology, psychology and anthropology. Some researchers argue that CCE is unique to humans and underlies our extraordinary evolutionary success as a species. Others claim to have found CCE in non-human species. Yet others remain sceptical that CCE is even important for explaining human behavioural diversity and complexity. These debates are hampered by multiple and often ambiguous definitions of CCE. Here, we review how researchers define, use and test CCE. We identify a core set of criteria for CCE which are both necessary and sufficient, and may be found in non-human species. We also identify a set of extended criteria that are observed in human CCE but not, to date, in other species. Different socio-cognitive mechanisms may underlie these different criteria. We reinterpret previous theoretical models and observational and experimental studies of both human and non-human species in light of these more fine-grained criteria. Finally, we discuss key issues surrounding information, fitness and cognition. We recommend that researchers are more explicit about what components of CCE they are testing and claiming to demonstrate.

Evolution of iris colour in relation to cavity nesting and parental care in passerine birds.

Strong selection pressures are known to act on animal coloration. Although many animals vary in eye colour, virtually no research has investigated the functional significance of these colour traits. Passeriformes have a range of iris colours, making them an ideal system to investigate how and why iris colour has evolved. Using phylogenetic comparative methods, we tested the hypothesis that conspicuous iris colour in passerine birds evolved in response to (a) coordination of offspring care and (b) cavity nesting, two traits thought to be involved in intra-specific gaze sensitivity. We found that iris colour and cooperative offspring care by two or more individuals evolved independently, suggesting that bright eyes are not important for coordinating parental care through eye gaze. Furthermore, we found that evolution between iris colour and nesting behaviour did occur in a dependent manner, but contrary to predictions, transitions to coloured eyes were not more frequent in cavity nesters than non-cavity nesters. Instead, our results indicate that selection away from having bright eyes was much stronger in non-cavity nesters than cavity nesters, perhaps because conspicuous eye coloration in species not concealed within a cavity would be more visible to predators.

Wild jackdaws' reproductive success and their offspring's stress hormones are connected to provisioning rate and brood size, not to parental neophobia.

Many species show individual variation in neophobia and stress hormones, but the causes and consequences of this variation in the wild are unclear. Variation in neophobia levels could affect the number of offspring animals produce, and more subtly influence the rearing environment and offspring development. Nutritional deficits during development can elevate levels of stress hormones that trigger long-term effects on learning, memory, and survival. Therefore measuring offspring stress hormone levels, such as corticosterone (CORT), helps determine if parental neophobia influences the condition and developmental trajectory of young. As a highly neophobic species, jackdaws (Corvus monedula) are excellent for exploring the potential effects of parental neophobia on developing offspring. We investigated if neophobic responses, alongside known drivers of fitness, influence nest success and offspring hormone responses in wild breeding jackdaws. Despite its consistency across the breeding season, and suggestions in the literature that it should have importance for reproductive fitness, parental neophobia did not predict nest success, provisioning rates or offspring hormone levels. Instead, sibling competition and poor parental care contributed to natural variation in stress responses. Parents with lower provisioning rates fledged fewer chicks, chicks from larger broods had elevated baseline CORT levels, and chicks with later hatching dates showed higher stress-induced CORT levels. Since CORT levels may influence the expression of adult neophobia, variation in juvenile stress responses could explain the development and maintenance of neophobic variation within the adult population.

The proximate-ultimate confusion in teaching and cooperation.

Kline does an admirable job of extending the functionalist framework developed by comparative researchers to help understand the function and form of human teaching. Functionalist approaches consider the adaptive value and underlying mechanisms of behaviour as separate but complementary questions, avoiding the conflation of ultimate and proximate explanations that has long hindered research on teaching and other forms of cooperation.