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A phylogeny of the species included in this study. Branch lengths are proportional to time except where long branches have been truncated by parallel diagonal lines (split between mammals and birds ∼ 292 Mya). 

A phylogeny of the species included in this study. Branch lengths are proportional to time except where long branches have been truncated by parallel diagonal lines (split between mammals and birds ∼ 292 Mya). 

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Cognition presents evolutionary research with one of its greatest challenges. Cognitive evolution has been explained at the proximate level by shifts in absolute and relative brain volume and at the ultimate level by differences in social and dietary complexity. However, no study has integrated the experimental and phylogenetic approach at the scal...

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... address these challenges we measured cognitive skills for self-control in 36 species of mammals and birds ( Fig. 1 and Tables S1-S4) tested using the same experimental procedures, and evaluated the leading hypotheses for the neuroanatomical under- pinnings and ecological drivers of variance in animal cognition. At the proximate level, both absolute (77, 99-107) and relative brain size (108-112) have been proposed as mechanisms supporting cognitive ...
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... predictor of any of the cognitive measures (Fig. 3, Table 2, and Table S7). However, dietary breadth covaried strongly with our measures of self-control (Fig. 3, Table 2, and Table S7). Supplemental analyses involving home range size, day journey length, the defensibility index, and substrate use revealed no significant associations (SI Text and Fig. ...
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... Darwin, understanding the evolution of cognition has been widely regarded as one of the greatest challenges for evolutionary research (1). Although researchers have identified surprising cognitive flexibility in a range of species (2 – 40) and potentially derived features of human psychology (41 – 61), we know much less about the major forces shaping cognitive evolution (62 – 71). With the notable exception of Bitterman ’ s landmark studies conducted several decades ago (63, 72 – 74), most research comparing cognition across species has been limited to small taxonomic samples (70, 75). With limited comparable experimental data on how cognition varies across species, previous research has largely relied on proxies for cognition (e.g., brain size) or metaanalyses when testing hypotheses about cognitive evolution (76 – 92). The lack of cognitive data collected with similar methods across large samples of species precludes meaningful species comparisons that can reveal the major forces shaping cognitive evolution across species, including humans (48, 70, 89, 93 – 98). To address these challenges we measured cognitive skills for self-control in 36 species of mammals and birds (Fig. 1 and Tables S1 – S4) tested using the same experimental procedures, and evaluated the leading hypotheses for the neuroanatomical under- pinnings and ecological drivers of variance in animal cognition. At the proximate level, both absolute (77, 99 – 107) and relative brain size (108 – 112) have been proposed as mechanisms supporting cognitive evolution. Evolutionary increases in brain size (both absolute and relative) and cortical reorganization are hallmarks of the human lineage and are believed to index commensurate changes in cognitive abilities (52, 105, 113 – 115). Further, given the high metabolic costs of brain tissue (116 – 121) and remarkable variance in brain size across species (108, 122), it is expected that the ener- getic costs of large brains are offset by the advantages of improved cognition. The cortical reorganization hypothesis suggests that selection for absolutely larger brains — and concomitant cortical reorganization — was the predominant mechanism supporting cognitive evolution (77, 91, 100 – 106, 120). In contrast, the encephalization hypothesis argues that an increase in brain volume relative to body size was of primary importance (108, 110, 111, 123). Both of these hypotheses have received support through analyses aggre- gating data from published studies of primate cognition and reports of “ intelligent ” behavior in nature — both of which correlate with measures of brain size (76, 77, 84, 92, 110, 124). With respect to selective pressures, both social and dietary complexities have been proposed as ultimate causes of cognitive evolution. The social intelligence hypothesis proposes that increased social complexity (frequently indexed by social group size) was the major selective pressure in primate cognitive evolution (6, 44, 48, 50, 87, 115, 120, 125 – 141). This hypothesis is supported by studies showing a positive correlation between a species ’ typical group size and the neocortex ratio (80, 81, 85 – 87, 129, 142 – 145), cognitive differences between closely related species with different group sizes (130, 137, 146, 147), and evidence for cognitive convergence between highly social species (26, 31, 148 – 150). The foraging hypothesis posits that dietary complexity, indexed by field reports of dietary breadth and reliance on fruit (a spatiotemporally distributed resource), was the primary driver of primate cognitive evolution (151 – 154). This hypothesis is supported by studies linking diet quality and brain size in primates (79, 81, 86, 142, 155), and experimental studies documenting species differences in cognition that relate to feeding ecology (94, 156 – 166). Although each of these hypotheses has received empirical support, a comparison of the relative contributions of the different proximate and ultimate explanations requires ( i ) a cognitive dataset covering a large number of species tested using comparable experimental procedures; ( ii ) cognitive tasks that allow valid measure- ment across a range of species with differing morphology, percep- tion, and temperament; ( iii ) a representative sample within each species to obtain accurate estimates of species-typical cognition; ( iv ) phylogenetic comparative methods appropriate for testing evolutionary hypotheses; and ( v ) unprecedented collaboration to collect these data from populations of animals around the world (70). Here, we present, to our knowledge, the first large-scale col- laborative dataset and comparative analysis of this kind, focusing on the evolution of self-control. We chose to measure self-control — the ability to inhibit a prepotent but ultimately counter- productive behavior — because it is a crucial and well-studied component of executive function and is involved in diverse decision-making processes (167 – 169). For example, animals require self-control when avoiding feeding or mating in view of a higher-ranking individual, sharing food with kin, or searching for food in a new area rather than a previously rewarding foraging site. In humans, self-control has been linked to health, economic, social, and academic achievement, and is known to be heritable (170 – 172). In song sparrows, a study using one of the tasks reported here found a correlation between self-control and song repertoire size, a predictor of fitness in this species (173). In primates, performance on a series of nonsocial self-control control tasks was related to variability in social systems (174), illustrating the potential link between these skills and socioecology. Thus, tasks that quantify self-control are ideal for comparison across taxa given its robust behavioral correlates, heritable basis, and potential impact on reproductive success. In this study we tested subjects on two previously implemented self-control tasks. In the A-not-B task (27 species, n = 344), subjects were first familiarized with finding food in one location (container A) for three consecutive trials. In the test trial, subjects initially saw the ...

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... Why would bumblebees have evolved to use only memories for ordinal comparisons while humans and starlings evolved to retain and recall both absolute and ranking memories? Breadth of diet has been suggested to play a role in the evolution of cognition (Hemingway et al., 2017;MacLean et al., 2014;Simons and Tibbetts, 2019). Humans and starlings forage on a range of different foods, whereas adult bumblebees feed almost exclusively on nectar and pollen from flowers. ...
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Are animals' preferences determined by absolute memories for options (e.g. reward sizes) or by their remembered ranking (better/worse)? The only studies examining this question suggest humans and starlings utilise memories for both absolute and relative information. We show that bumblebees' learned preferences are based only on memories of ordinal comparisons. A series of experiments showed that after learning to discriminate pairs of different flowers by sucrose concentration, bumblebees preferred flowers (in novel pairings) with (1) higher ranking over equal absolute reward, (2) higher ranking over higher absolute reward, and (3) identical qualitative ranking but different quantitative ranking equally. Bumblebees used absolute information in order to rank different flowers. However, additional experiments revealed that, even when ranking information was absent (i.e. bees learned one flower at a time), memories for absolute information were lost or could no longer be retrieved after at most 1 hr. Our results illuminate a divergent mechanism for bees (compared to starlings and humans) of learned preferences that may have arisen from different adaptations to their natural environment. Editor's evaluation This is a very informative and nicely controlled study showing that, when retrieving the value of a food type, bumblebees guide their choices by remembered ranking of feeders instead of focusing on their absolute rewards.
... Self-control is another cognitive ability to be enhanced when the degree of fission-fusion dynamics is high [88]. ...
Article
Communicative complexity relates to social complexity, as individuals in more complex social systems either use more signals or more complex signals than individuals living in less complex ones. Taking the individual group member's perspective, here we examine communicative complexity in relation to social complexity, which arises from two components of social systems: social structure and social organization. We review the concepts of social relationships and social complexity and evaluate their implications for communicative and cognitive complexity using examples from primate species. We focus on spider monkeys ( Ateles geoffroyi ), as their social organization is characterized by flexibility in grouping dynamics and they use a variety of communicative signals. We conclude that no simple relationship exists among social complexity, communicative complexity and cognitive complexity, with social complexity not necessarily implying cognitive complexity, and communicative and cognitive complexity being independently linked to social complexity. To better understand the commonly implied link between social complexity and cognitive complexity it is crucial to recognize the complementary role of communicative complexity. A more elaborated communicative toolkit provides the needed flexibility to deal with dynamic and multifaceted social relationships and high variation in fission–fusion dynamics. This article is part of the theme issue ‘Cognition, communication and social bonds in primates’.
... Second, because measuring cognition in a sufficiently large number of individuals is time-consuming, many studies compared few species (often only two) and considered only one or two aspects of their cognitive abilities (MacLean et al. 2012;Krasheninnikova et al. 2020). Notable exceptions include a study on problem-solving in 39 carnivore species (Benson-Amram et al. 2016), a study on habituation in 13 pit vipers (Krochmal et al. 2018), a study on associative learning in 16 bee species (Collado et al. 2021), and a study on inhibitory control across 36 mammal and bird species (MacLean et al. 2014). Low taxon sampling hampers the identification of environmental drivers of among-species variation in cognitive performance; focusing on single cognitive skills may produce a myopic view of species' cognition. ...
Article
Cognition is an essential tool for animals to deal with environmental challenges. Nonetheless, the ecological forces driving the evolution of cognition throughout the animal kingdom remain enigmatic. Large‐scale comparative studies on multiple species and cognitive traits have been advanced as the best way to facilitate our understanding of cognitive evolution, but such studies are rare. Here, we tested 13 species of lacertid lizards (Reptilia: Lacertidae) using a battery of cognitive tests measuring inhibitory control, problem‐solving, and spatial and reversal learning. Next, we tested the relationship between species’ performance and a) resource availability (temperature and precipitation), habitat complexity (NDVI) and habitat variability (seasonality) in their natural habitat, and b) their life‐history (size at hatching and maturity, clutch size and frequency). Although species differed markedly in their cognitive abilities, such variation was mostly unrelated to their ecology and life‐history. Yet, species living in more variable environments exhibited lower behavioural flexibility, likely due to energetic constrains in such habitats. Our standardised protocols provide opportunities for collaborative research, allowing increased sample sizes and replication, essential for moving forward in the field of comparative cognition. Follow‐up studies could include more detailed measures of habitat structure and look at other potential selective drivers such as predation. This article is protected by copyright. All rights reserved
... In primate cognition research, collaborative work has demonstrated to be fruitful (Amici et al., 2008;Amici et al., 2018;Burkart et al., 2014;Herrmann et al., 2007;Joly et al., 2017;MacLean et al., 2014). These collaborations have offered new theoretical approaches and important data to investigate the evolution of the primate mind. ...
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Researchers have studied non-human primate cognition along different paths, including social cognition, planning and causal knowledge, spatial cognition and memory, and gestural communication, as well as comparative studies with humans. This volume describes how primate cognition is studied in labs, zoos, sanctuaries, and in the field, bringing together researchers examining similar issues in all of these settings and showing how each benefits from the others. Readers will discover how lab-based concepts play out in the real world of free primates. This book tackles pressing issues such as replicability, research ethics, and open science. With contributors from a broad range of comparative, cognitive, neuroscience, developmental, ecological, and ethological perspectives, the volume provides a state-of-the-art review pointing to new avenues for integrative research.
... Inhibitory control is one of the key skills of executive function and is considered to be a general cognitive ability. Inhibitory control is a crucial and well-studied component of executive function and involves decision-making processes (Hare et al. 2009;Bray et al. 2014;MacLean et al. 2014). We were curious whether the performance of subjects in the two problem-solving tasks is connected to the strength of handedness and expected to further support the enhanced cognition hypothesis. ...
... The A-not-B task was originally proposed by Piaget (1954) to test the development of object permanence in children. MacLean et al. (2014) developed the revised A-not-B task to conduct a large-scale cross-species study to evaluate the evolution of inhibitory control. Three identical and aligned caps of drink bottles (3-cm diameter and 1.5-cm high) were employed in this test (Fig. 1). ...
... Following the large-scale cross-species study undertaken by MacLean et al. (2014), the cylinder task (also known as one of the detour tasks) came to the forefront of comparative cognition as a measure of inhibitory control. Subjects were first trained to obtain pieces of food hidden inside an opaque cylinder during the training phase. ...
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Brain lateralization, a trait ubiquitous in vertebrates and invertebrates, refers to structural differences between the left and right sides of the brain or to the left and right sides controlling different functions or processing information in different ways. Many studies have looked into the advantages of lateralized brains and discovered that cerebral lateralization confers a fitness advantage. Enhancing cognitive ability has been proposed as one of the potential benefits of the lateralized brain, however, this has not been widely validated. In this study, we investigated the handedness of 34 subjects from four groups of Callitrichids, as well as their performance in two inhibitory control tasks (the revised A-not-B task and the cylinder task). The subjects had strong individual hand preferences, and only a few zoo-born individuals were ambidextrous. Sex and generation influence the strength of hand preference. In the cylinder task, the subjects showed differences between groups, and the performance of the second-generation was better than that of the first-generation. We found that neither the strength of hand preferences (ABS-HI) or direction of hand preferences (HI) was linked with success on the two inhibitory tasks. That is, we were unable to support the enhanced cognitive function hypothesis. We believe that individual ontogeny and the type of cognitive task have an impact on the support of this hypothesis. The advantages of lateralized brain may be reflected in tests that require multiple cognitive abilities.
... Our puzzle box was made of transparent plexiglass with holes allowing both visual and olfactory cues, Fig. 4 Relationship between persistence (s) and increasing number of successful trials (a) and behavioral diversity (b) but individuals could not access the reward directly and instead had to use one of the three access points. Individuals who reduced their behavioral diversity in later, more effective trials, may have been exhibiting inhibitory control, a cognitive trait where individuals must stop a motor reaction and perform a correct movement (MacLean et al. 2014). Additional evidence for cognitive traits underlying success is that persistence also decreased across successful trials (M3), suggesting that individuals were learning how to open the puzzle more efficiently. ...
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Innovation — the ability to solve problems in a novel way — is not only associated with cognitive abilities and relative brain size, but also by noncognitive traits, such as personality and motivation. We used a novel foraging task with three access options to determine how neophobia, exploration, and persistence influence innovation in 12 habituated bat-eared foxes (Otocyon megalotis) in the Kalahari Desert. Bat-eared foxes offer a unique system to understand cognition as they have the smallest relative brain size of measured canids and a specialized, termite-based diet, yet have displayed foraging innovations. Interestingly, most of our individuals solved the task at least once and six individuals solved the task in every trial. Neophobia did not influence success on the first trial, but both exploration and persistence influenced success across all trials. Those individuals that solved the puzzle over multiple trials became faster over time, suggesting that they learned how to open the box more efficiently. We found some variation in the method to open the puzzle box with six individuals solving the puzzle using two methods and one individual using all three methods. This is the first study to show innovation in a novel foraging task in wild bat-eared foxes.
... Moreover, inhibitory control can play a role in the maintenance of social tolerance (Box 1, Figure 1a). Inhibitory control has been investigated in wolves, dogs and coyotes [67,68], and studies conducted on dogs found a positive correlation between inhibitory control ability and problem-solving success [69,70]. The role of inhibitory control on cooperation was shown in the delayed loose-string paradigm where successful wolves and dogs waited for their partner to arrive, inhibiting themselves from pulling the rope [71]. ...
... Direct reciprocity might require individuals to memorise previous interactions (calculated reciprocity) or might be triggered by emotional states either short-term based on the partner's previous attitude ('attitudinal reciprocity') or longterm through the formation of social bonds ['emotional bookkeeping', 66,92]. Self-control: The ability or capacity to obtain a subjectively more valuable outcome rather than a subjectively less valuable outcome through choosing and then tolerating a longer delay or a greater effort requirement for obtaining that more valuable outcome [67]. It is a form of behavioural inhibition which not only implies suppressing impulsive reactions, but also decide as to whether a delayed gain is worth waiting for. ...
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Canids are believed to be clever animals applying sophisticated social and hunting strategies. However, current studies under natural conditions do not indicate higher cognitive requirements beyond associative learning, but likely also underestimate them as applied methods are still in a fledgling stage. Experimental studies on captive canids — almost exclusively on wolves and dogs — indicate role understanding, perspective taking skills and numerical competence. However, such studies do not inform us if and how such skills are used in the wild. Apart from urging researchers to combine both approaches, we also highlight the need to investigate the embodied cognition of canids, as their specific ecological needs and perceptual capabilities likely led to specialised neuroethological pattern recognition skills.
... Inhibitory control (a.k.a., impulse control, Coppens et al. 2010) is an aspect of cognition which typically varies between individuals of the same species (e.g., MacLean et al. 2014;Langley et al. 2020;Lucon-Xicatto et al. 2020a;Szabo et al. 2020). However, we do not know yet how inhibitory control is affected by selection. ...
... Some studies find connections between these impulsive behaviours (e.g., Garner and Mason 2002), whereas others do not (e.g., Brucks et al. 2017;Johnson-Ulrich and Holekamp 2020;van Horik et al. 2018). Along with affecting impulsivity, inhibitory control can also influence how individuals make decisions (MacLean et al. 2014) and adapt to changing situations (Gilbert and Burgess, 2008;Lucon-Xicatto et al. 2017). Thus, variation in inhibitory control could be expected to affect individual outcomes in ways which could have evolutionary consequences. ...
... We used a detour test (Boogert et al. 2011;MacLean et al. 2014) to measure impulsive action and persistence, therefore, assessing inhibitory control. We conducted pretraining for the detour test, and the test itself, in an arena (82 × 53 × 50 cm; L x W x H). ...
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Individual variation in cognition, seen in many taxa, is not well understood, despite its potential evolutionary consequences. Inhibitory control is an aspect of cognition which differs between individuals. However, how selection could act on this variation remains unclear. First, individual consistency over time of behaviours affected by inhibitory control, and how these behaviours relate to each other, is not well understood. Second, consequences in ecologically relevant contexts of variation in behaviours affected by inhibitory control, are scarcely investigated. Therefore, we explored the temporal consistency and inter-relatedness of two behaviours influenced by inhibitory control (impulsive action and persistence) and how these link to social rank, foraging efficiency, and risk taking in adult female red junglefowl ( Gallus gallus ). We measured impulsive action in a detour test, and persistence in both a detour test and a foraging test. Impulsive action and persistence, measured in a detour test, were moderately consistent over time, and positively correlated. This implies that selection could act on inhibitory control via these behaviours, and selection on one behaviour could affect the other. However, we found no evidence of links between inhibitory control and social rank, foraging efficiency, or risk taking. This implies that selection may not act on inhibitory control via these measures, and that, in general, there may be a lack of strong selection on inhibitory control. This, in turn, could help explain individual variation in this aspect of cognition. Future research should explore the specificity of when inhibitory control has implications for individuals, and continue to investigate how variation in cognitive traits influences how individuals behave in contexts with potential evolutionary implications.
... For example, in the "cylinder task," a reward is placed in the center of a transparent cylinder and can only be accessed through openings on either end. The cylinder task has been adapted to a wide range of species in order to evaluate phylogenetic and ontogenetic mechanisms of inhibitory control (Kabadayi, Jacobs et al., 2017;Maclean et al., 2014). In dogs, the cylinder task has become an increasingly popular method for assessing subject characteristics influencing inhibitory control (Foraita et al., 2021), demonstrating sensitivity to temperament (Bray et al., 2015), development , domestication status (Marshall-Pescini et al., 2015), sex (Junttila et al., 2021), and working ability (Tiira et al., 2020). ...
Article
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The cylinder task, which requires detouring around an obstacle to retrieve a reward, is a popular method for assessing inhibitory control in dogs and other species. However, performance on the cylinder task has poor construct validity represented by its lack of correlations with other inhibitory control measures, ceiling effects, and influence of non-cognitive factors. In the current study we examined whether reward type affected dogs’ performance in the cylinder task. We compared working-line Labrador retrievers' (n = 38) performance on two conditions of the cylinder task, one with a treat and another with a ball reward, and found that dogs performed significantly better when a treat was used. Our secondary goal was to determine if how we defined a dog’s response changed interpretation of the results. We found better performance when a narrower definition of an inhibitory control failure was used. Further, under one condition of reward type and response definition, cylinder task performance was predicted by another measure of inhibitory control (Dog Impulsivity Assessment Scale scores). These findings are the first to show the effect of reward type on cylinder task performance as well as a relationship between the cylinder task and another measure of inhibitory control in dogs. We discuss these results in relation to previous findings on the effects of task features on cylinder task performance and its construct validity.
... Some studies have tested multiple species to understand the evolution of intelligence. For example, a study of 23 primates showed that species with greater dietary breadth, but not those living in larger groups, exhibited greater motor inhibitory control (MacLean et al., 2014), whereas another study tied inhibitory control to fission-fusion social systems (Amici et al., 2008). However, these studies focused primarily on motor inhibition, whereas research from cognitive science and neurobiology has shown that cognitive control is a multidimensional set of processes that also includes flexible updating and planning (Diamond, 2013;Friedman & Miyake, 2017;Völter et al., 2018). ...
... To implement these tasks, we drew on the methods of recent work that used a battery of tasks to assess multiple aspects of cognition in tandem on animals (e.g., Fichtel et al., 2020;Herrmann et al., 2007;Joly et al., 2017;Schmitt et al., 2012). These tasks have also been well validated in prior studies of nonhuman primates (Amici et al., 2008(Amici et al., , 2010Deaner et al., 2006;MacLean et al., 2014;Rosati et al., 2007). We then used this battery to examine cognitive control in primates with clear variation in both social and ecological characteristics. ...
... We then used this battery to examine cognitive control in primates with clear variation in both social and ecological characteristics. Importantly, both the social-and ecological-intelligence hypotheses provide plausible pathways for the emergence of cognitive control: Flexible adoption of new behavioral strategies could provide an advantage in ecological contexts, such as by allowing individuals to adjust to changing environmental circumstances (MacLean et al., 2014), but also in social contexts, by allowing individuals to deal with a shifting social landscape caused by others' unpredictable behaviors (Amici et al., 2018). ...
Article
Cognitive control, or executive function, is a key feature of human cognition, allowing individuals to plan, acquire new information, or adopt new strategies when the circumstances change. Yet it is unclear which factors promote the evolution of more sophisticated executive-function abilities such as those possessed by humans. Examining cognitive control in nonhuman primates, our closest relatives, can help to identify these evolutionary processes. Here, we developed a novel battery to experimentally measure multiple aspects of cognitive control in primates: temporal discounting, motor inhibition, short-term memory, reversal learning, novelty responses, and persistence. We tested lemur species with targeted, independent variation in both ecological and social features (ruffed lemurs, Coquerel’s sifakas, ring-tailed lemurs, and mongoose lemurs; N = 39) and found that ecological rather than social characteristics best predicted patterns of cognitive control across these species. This highlights the importance of integrating cognitive data with species’ natural history to understand the origins of complex cognition.