Meta-analyses reveal support for the Social Intelligence Hypothesis.

The Social Intelligence Hypothesis (SIH) is one of the leading explanations for the evolution of cognition. Since its inception a vast body of literature investigating the predictions of the SIH has accumulated, using a variety of methodologies and species. However, the generalisability of the hypothesis remains unclear. To gain an understanding of the robustness of the SIH as an explanation for the evolution of cognition, we systematically searched the literature for studies investigating the predictions of the SIH. Accordingly, we compiled 103 studies with 584 effect sizes from 17 taxonomic orders. We present the results of four meta-analyses which reveal support for the SIH across interspecific, intraspecific and developmental studies. However, effect sizes did not differ significantly between the cognitive or sociality metrics used, taxonomy or testing conditions. Thus, support for the SIH is similar across studies using neuroanatomy and cognitive performance, those using broad categories of sociality, group size and social interactions, across taxonomic groups, and for tests conducted in captivity or the wild. Overall, our meta-analyses support the SIH as an evolutionary and developmental explanation for cognitive variation.

Juvenile social play predicts adult reproductive success in male bottlenose dolphins.

For over a century, the evolution of animal play has sparked scientific curiosity. The prevalence of social play in juvenile mammals suggests that play is a beneficial behavior, potentially contributing to individual fitness. Yet evidence from wild animals supporting the long-hypothesized link between juvenile social play, adult behavior, and fitness remains limited. In Western Australia, adult male bottlenose dolphins (Tursiops aduncus) form multilevel alliances that are crucial for their reproductive success. A key adult mating behavior involves allied males using joint action to herd individual females. Juveniles of both sexes invest significant time in play that resembles adult herding-taking turns in mature male (actor) and female (receiver) roles. Using a 32-y dataset of individual-level association patterns, paternity success, and behavioral observations, we show that juvenile males with stronger social bonds are significantly more likely to engage in joint action when play-herding in actor roles. Juvenile males also monopolized the actor role and produced an adult male herding vocalization ("pops") when playing with females. Notably, males who spent more time playing in the actor role as juveniles achieved more paternities as adults. These findings not only reveal that play behavior provides male dolphins with mating skill practice years before they sexually mature but also demonstrate in a wild animal population that juvenile social play predicts adult reproductive success.

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.

Call combination production is linked to the social environment in Western Australian magpies (Gymnorhina tibicen dorsalis).

It has recently become clear that some language-specific traits previously thought to be unique to humans (such as the capacity to combine sounds) are widespread in the animal kingdom. Despite the increase in studies documenting the presence of call combinations in non-human animals, factors promoting this vocal trait are unclear. One leading hypothesis proposes that communicative complexity co-evolved with social complexity owing to the need to transmit a diversity of information to a wider range of social partners. The Western Australian magpie (Gymnorhina tibicen dorsalis) provides a unique model to investigate this proposed link because it is a group-living, vocal learning species that is capable of multi-level combinatoriality (independently produced calls contain vocal segments and comprise combinations). Here, we compare variations in the production of call combinations across magpie groups ranging in size from 2 to 11 birds. We found that callers in larger groups give call combinations: (i) in greater diversity and (ii) more frequently than callers in smaller groups. Significantly, these observations support the hypothesis that combinatorial complexity may be related to social complexity in an open-ended vocal learner, providing an important step in understanding the role that sociality may have played in the development of vocal combinatorial complexity. This article is part of the theme issue 'The power of sound: unravelling how acoustic communication shapes group dynamics'.

Problem-solving ability: a link between cognition and conservation?

Traditionally, conservation and cognition have been disparate research disciplines. However, Audet et al.'s recent research contributes to an increasing body of evidence that innovative behaviours may determine the ability of species to respond to rapid environmental change, identifying an opportunity for cognition research to directly contribute to conservation outcomes.

Heritability of cognitive performance in wild Western Australian magpies.

Individual differences in cognitive performance can have genetic, social and environmental components. Most research on the heritability of cognitive traits comes from humans or captive non-human animals, while less attention has been given to wild populations. Western Australian magpies (Gymnorhina tibicen dorsalis, hereafter magpies) show phenotypic variation in cognitive performance, which affects reproductive success. Despite high levels of individual repeatability, we do not know whether cognitive performance is heritable in this species. Here, we quantify the broad-sense heritability of associative learning ability in a wild population of Western Australian magpies. Specifically, we explore whether offspring associative learning performance is predicted by maternal associative learning performance or by the social environment (group size) when tested at three time points during the first year of life. We found little evidence that offspring associative learning performance is heritable, with an estimated broad-sense heritability of just -0.046 ± 0.084 (confidence interval: -0.234/0.140). However, complementing previous findings, we find that at 300 days post-fledging, individuals raised in larger groups passed the test in fewer trials compared with individuals from small groups. Our results highlight the pivotal influence of the social environment on cognitive development.

High temperatures during early development reduce adult cognitive performance and reproductive success in a wild animal population.

Global warming is rapidly changing the phenology, distribution, behaviour and demography of wild animal populations. Recent studies in wild animals have shown that high temperatures can induce short-term cognitive impairment, and captive studies have demonstrated that heat exposure during early development can lead to long-term cognitive impairment. Given that cognition underpins behavioural flexibility and can be directly linked to fitness, understanding how high temperatures during early life might impact adult cognitive performance in wild animals is a critical next step to predict wildlife responses to climate change. Here, we investigated the relationship between temperatures experienced during development, adult cognitive performance, and reproductive success in wild southern pied babblers (Turdoides bicolor). We found that higher mean daily maximum temperatures during nestling development led to long-term cognitive impairment in associative learning performance, but not reversal learning performance. Additionally, a higher number of hot days (exceeding 35.5 °C, temperature threshold at which foraging efficiency and offspring provisioning decline) during post-fledging care led to reduced reproductive success in adulthood. We did not find evidence that low reproductive success was linked to impaired associative learning performance: associative learning performance was not related to reproductive success. In contrast, reversal learning performance was negatively related to reproductive success in breeding adults. This suggests that reproduction can carry a cost in terms of reduced performance in cognitively demanding tasks, confirming previous evidence in this species. Taken together, these findings indicate that naturally occurring high temperatures during early development have long-term negative effects on cognition and reproductive success in wild animals. Compounding effects of high temperatures on current nestling mortality and on the long-term cognitive and reproductive performance of survivors are highly concerning given ongoing global warming.

Chemokines form complex signals during inflammation and disease that can be decoded by extracellular matrix proteoglycans.

Chemokine-driven leukocyte recruitment is a key component of the immune response and of various diseases. Therapeutically targeting the chemokine system in inflammatory disease has been unsuccessful, which has been attributed to redundancy. We investigated why chemokines instead have specific, specialized functions, as demonstrated by multiple studies. We analyzed the expression of genes encoding chemokines and their receptors across species, tissues, and diseases. This analysis revealed complex expression patterns such that genes encoding multiple chemokines that mediated recruitment of the same leukocyte type were expressed in the same context, such as the genes encoding the CXCR3 ligands CXCL9, CXCL10, and CXCL11. Through biophysical approaches, we showed that these chemokines differentially interacted with extracellular matrix glycosaminoglycans (ECM GAGs), which was enhanced by sulfation of specific GAGs. Last, in vivo approaches demonstrated that GAG binding was critical for the CXCL9-dependent recruitment of specific T cell subsets but not of others, irrespective of CXCR3 expression. Our data demonstrate that interactions with ECM GAGs regulated whether chemokines were presented on cell surfaces or remained more soluble, thereby affecting chemokine availability and ensuring specificity of chemokine action. Our findings provide a mechanistic understanding of chemokine-mediated immune cell recruitment and identify strategies to target specific chemokines during inflammatory disease.

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.

Helpers don't help when it's hot in a cooperatively breeding bird, the Southern Pied Babbler.

Cooperative breeding, where more than two individuals invest in rearing a single brood, occurs in many bird species globally and often contributes to improved breeding outcomes. However, high temperatures are associated with poor breeding outcomes in many species, including cooperative species. We used data collected over three austral summer breeding seasons to investigate the contribution that helpers make to daytime incubation in a cooperatively breeding species, the Southern Pied Babbler Turdoides bicolor, and the ways in which their contribution is influenced by temperature. Helpers spent a significantly higher percentage of their time foraging (41.8 ± 13.7%) and a significantly lower percentage of their time incubating (18.5 ± 18.8%) than members of the breeding pair (31.3 ± 11% foraging and 37.4 ± 15.7% incubating). In groups with only one helper, the helper's contribution to incubation was similar to that of breeders. However, helpers in larger groups contributed less to incubation, individually, with some individuals investing no time in incubation on a given observation day. Helpers significantly decrease their investment in incubation on hot days (>35.5°C), while breeders tend to maintain incubation effort as temperatures increase. Our results demonstrate that pied babblers share the workload of incubation unequally between breeders and helpers, and this inequity is more pronounced during hot weather. These results may help to explain why recent studies have found that larger group size does not buffer against the impacts of high temperatures in this and other cooperatively breeding species.

Multi-level combinatoriality in magpie non-song vocalizations.

Comparative studies conducted over the past few decades have provided important insights into the capacity for animals to combine vocal segments at either one of two levels: within- or between-calls. There remains, however, a distinct gap in knowledge as to whether animal combinatoriality can extend beyond one level. Investigating this requires a comprehensive analysis of the combinatorial features characterizing a species' vocal system. Here, we used a nonlinear dimensionality reduction analysis and sequential transition analysis to quantitatively describe the non-song combinatorial repertoire of the Western Australian magpie (Gymnorhina tibicen dorsalis). We found that (i) magpies recombine four distinct acoustic segments to create a larger number of calls, and (ii) the resultant calls are further combined into larger call combinations. Our work demonstrates two levels in the combining of magpie vocal units. These results are incongruous with the notion that a capacity for multi-level combinatoriality is unique to human language, wherein the combining of meaningless sounds and meaningful words interactively occurs across different combinatorial levels. Our study thus provides novel insights into the combinatorial capacities of a non-human species, adding to the growing evidence of analogues of language-specific traits present in the animal kingdom.

Chemokine CXCL4 interactions with extracellular matrix proteoglycans mediate widespread immune cell recruitment independent of chemokine receptors.

Leukocyte recruitment from the vasculature into tissues is a crucial component of the immune system but is also key to inflammatory disease. Chemokines are central to this process but have yet to be therapeutically targeted during inflammation due to a lack of mechanistic understanding. Specifically, CXCL4 (Platelet Factor 4, PF4) has no established receptor that explains its function. Here, we use biophysical, in vitro, and in vivo techniques to determine the mechanism underlying CXCL4-mediated leukocyte recruitment. We demonstrate that CXCL4 binds to glycosaminoglycan (GAG) sugars on proteoglycans within the endothelial extracellular matrix, resulting in increased adhesion of leukocytes to the vasculature, increased vascular permeability, and non-specific recruitment of a range of leukocytes. Furthermore, GAG sulfation confers selectivity onto chemokine localization. These findings present mechanistic insights into chemokine biology and provide future therapeutic targets.

Repeated testing does not confound cognitive performance in the Western Australian magpie (Cracticus tibicen dorsalis).

A robust understanding of cognitive variation at the individual level is essential to understand selection for and against cognitive traits. Studies of animal cognition often assume that within-individual performance is highly consistent. When repeated tests of individuals have been conducted, the effects of test order (the overall sequence in which different tests are conducted) and test number (the ordinal number indicating when a specific test falls within a sequence)-in particular the potential for individual performance to improve with repeated testing-have received limited attention. In our study, we investigated test order and test number effects on individual performance in three inhibitory control tests in Western Australian magpies (Cracticus tibicen dorsalis). We presented adult magpies with three novel inhibitory control tasks (detour-reaching apparatuses) in random order to test whether experience of cognitive testing and the order in which the apparatuses were presented were predictors of cognitive performance. We found that neither test number nor test order had an effect on cognitive performance of individual magpies when presenting different variants of inhibitory control tasks. This suggests that repeated testing of the same cognitive trait, using causally identical but visually distinct cognitive tasks, does not confound cognitive performance. We recommend that repeated testing effects of cognitive performance in other species be studied to broadly determine the validity of repeated testing in animal cognition studies.

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.

Periorbital temperature responses to natural air temperature variation in wild birds.

With global temperatures rapidly increasing, biologists require tools to assess how wild animals are responding to heat. Thermal imaging of the eye region offers a potential non-invasive alternative to traditional techniques to study thermoregulation and stress responses in wild animals. However, we currently have a poor understanding of how the temperature of the eye region is regulated under increasing temperature and whether this regulation differs among individuals. Here, we use thermal imaging to repeatedly measure the maximum temperature of the eye region (periorbital temperature) in 42 wild pied babblers (Turdoides bicolor) under natural air temperatures ranging from 14.3 to 42.5 °C. Our aim was to determine the relationship between periorbital temperature and air temperature, whether this relationship is repeatable, and whether it differs according to individual attributes. Periorbital temperature showed a non-linear increase with air temperature, becoming independent of air temperature above 38 °C. Above 38 °C, periorbital temperature was not explained by any individual attributes. Below 38 °C, periorbital temperature increased more steeply in individuals with low body mass and it was lower in older compared to younger females. However, the effect of these individual attributes was small compared to the effect of wind speed, air temperature and head tilt. Additionally, the repeatability of individual periorbital temperature was low (R < 0.25) and non-significant both below and above 38 °C. Our findings warrant caution in the use of periorbital temperature to infer individual thermoregulatory responses to increasing temperatures, especially in the wild, where control over confounding non-physiological factors is limited.

Does trappability and self-selection influence cognitive performance?

Recent research has highlighted how trappability and self-selection-the processes by which individuals with particular traits may be more likely to be caught or to participate in experiments-may be sources of bias in studies of animal behaviour and cognition. It is crucial to determine whether such biases exist, and if they do, what effect they have on results. In this study, we investigated if trappability (quantified through 'ringing status'-whether or not a bird had been trapped for ringing) and self-selection are sources of bias in a series of associative learning experiments spanning 5 years in the Western Australian magpie (Gymnorhina tibicen dorsalis). We found no evidence of self-selection, with no biases in task participation associated with sex, age, group size or ringing status. In addition, we found that there was no effect of trappability on cognitive performance. These findings give us confidence in the results generated in the animal cognition literature and add to a growing body of literature seeking to determine potential sources of bias in studies of animal behaviour, and how they influence the generalizability and reproducibility of findings.

Long-term repeatability of cognitive performance.

Measures of cognitive performance, derived from psychometric tasks, have yielded important insights into the factors governing cognitive variation. However, concerns remain over the robustness of these measures, which may be susceptible to non-cognitive factors such as motivation and persistence. Efforts to quantify short-term repeatability of cognitive performance have gone some way to address this, but crucially the long-term repeatability of cognitive performance has been largely overlooked. Quantifying the long-term repeatability of cognitive performance provides the opportunity to determine the stability of cognitive phenotypes and the potential for selection to act on them. To this end, we quantified long-term repeatability of cognitive performance in wild Australian magpies over a three-year period. Cognitive performance was repeatable in two out of four cognitive tasks-associative learning and reversal-learning performance was repeatable, but spatial memory and inhibitory control performance, although trending toward significance, was not. Measures of general cognitive performance, obtained from principal components analyses carried out on each cognitive test battery, were highly repeatable. Together, these findings provide evidence that at least some cognitive phenotypes are stable, which in turn has important implications for our understanding of cognitive evolution.

Kidnapping intergroup young: an alternative strategy to maintain group size in the group-living pied babbler (Turdoides bicolor).

Both inter- and intragroup interactions can be important influences on behaviour, yet to date most research focuses on intragroup interactions. Here, we describe a hitherto relatively unknown behaviour that results from intergroup interaction in the cooperative breeding pied babbler: kidnapping. Kidnapping can result in the permanent removal of young from their natal group. Since raising young requires energetic investment and abductees are usually unrelated to their kidnappers, there appears no apparent evolutionary advantage to kidnapping. However, kidnapping may be beneficial in species where group size is a critically limiting factor (e.g. for reproductive success or territory defence). We found kidnapping was a highly predictable event in pied babblers: primarily groups that fail to raise their own young kidnap the young of others, and we show this to be the theoretical expectation in a model that predicts kidnapping to be facultative, only occurring in those cases where an additional group member has sufficient positive impact on group survival to compensate for the increase in reproductive competition. In babblers, groups that failed to raise young were also more likely to accept extragroup adults (hereafter rovers). Groups that fail to breed may either (i) kidnap intergroup young or (ii) accept rovers as an alternative strategy to maintain or increase group size. This article is part of the theme issue 'Intergroup conflict across taxa'.

Chemokine redundancy versus specificity in the context of CXCR3 and its ligands.

In a recent article published in Immunology & Cell Biology, Dalit et al. describe how correcting mutations in the C57BL/6 mouse strain can restore production of the chemokine CXCL11, although surprisingly, this expression of CXCL11 had little effect on B and T cells and the innate immune response to infection with lymphocytic choriomeningitis virus or influenza virus.