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Phylogenetic signal in the cognitive data

Phylogenetic signal in the cognitive data

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Significance Although scientists have identified surprising cognitive flexibility in animals and potentially unique features of human psychology, we know less about the selective forces that favor cognitive evolution, or the proximate biological mechanisms underlying this process. We tested 36 species in two problem-solving tasks measuring self-con...

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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 evolution. Evolutionary increases in brain size (both ab- solute and relative) and cortical reorganization are hallmarks of the human lineage and are believed to index commensurate changes in cognitive abilities (52,105,(113)(114)(115). Further, given the high metabolic costs of ...
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... the two tasks assessed complementary but not identical abilities, the composite score serves as a broader index of self-control across tasks. Phylogenetic analyses revealed that scores were more similar among closely related species, with the maximum likelihood estimate of λ, a measure of phylogenetic signal, significantly greater than zero in most cases (Table 1). For both tasks, scores from multiple populations of the same species (collected by different researchers at different sites) were highly correlated (cylinder task: r = 0.95, n = 5, P = 0.01; A-not-B task: r = 0.87, n = 6, P = 0.03; SI Text and Table S6). ...

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... To determine the structural features associated with high intelligence, one can survey the numerous studies of cognition in animals, and search for those taxa that stand out as having exceptional abilities in general features like learning and problem solving -and what structural features they share. Many lines of evidence indicate that larger brains (ideally measured as the number of neurons and synapses; Herculano-Houzel 2009; Olkowicz et al. 2016, but usually measured more crudely by volume or weight) typically have increased learning and problemsolving ability (Deaner et al. 2007;MacLean et al. 2014), although encephalization in combination with large brain size may also contribute to intelligence (Benson-Amram et al. 2016). Broadscale comparisons across the animal taxa on Earth ( Figure 1) indicate that the general features leading to large brain size are: large body size (Isler et al. 2013;Tsuboi et al. 2018;, endothermic homeothermy (Yu et al. 2014), a high quality diet (DeCasien et al. 2017), and given these three traits, inclusion in an outlier clade that for unresolved reasons have higher than average encephalization, e.g. ...
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When animals evolve sufficient intelligence and dexterity to be able to learn to fabricate utility products (UPs) like tools, the UP's they produce become part of an induced-reproduction system that intrinsically shares many life-like traits with biological organisms, including genome-like fabrication and operation information that is physically-encoded in the animal fabricator’s neural networks. When this set of life- like traits includes a sufficient capacity for system-improving cultural evolution (UP-evolvability), the UPs become ‘para-alive’, i.e., nearly alive, or a form of non-biological UP-paralife that is equivalent to the life- status of biological viruses, plasmids, and transposons. In the companion paper I focus on the evolution of UP-paralife in the context of modern, language-capable humans and its predicted evolution going forward in time (Rice 2022). Here I look backward in time and focus on the origin of UP-paralife and its subsequent coevolution with human intelligence. I begin by determining the pathways leading to the evolution of large brains in the rare lineages of biological life that have sufficient intelligence to learn to fabricate tools –a critical first step in the evolution of UP-paralife. The simplest forms of these learning- based UPs, made by species like chimpanzees and New Caledonian crows, represent only proto-UP- paralife because they lack sufficient UP-evolvability. Expanded UP-evolvability required a combination of three attributes that enabled continuous niche-expansion of the animal fabricator via a new and advanced form of UP-mediated teamwork (TW): i) self-domestication that facilitated TW among low-related individuals, ii) learned volitional words (protolanguage) that represent ephemeral UPs that coordinate TW, and iii) learned fabrication of simple flaked-stone tools with cutting and chopping capabilities (a UP to make other structural UPs) that expanded teammate phenotypes and TW capabilities. This specific triad of attributes is synergistic because each one acts as a TW-enhancer that can gradually erode different components of the three major constraints on TW operation and expansion: too much selfishness, insufficient coordination signals, and insufficient physical traits of teammates. The increase in UP- evolvability was transformative and marked the origin of UP-paralife and the initiation of coevolution between UP-paralife (cultural evolution) and the intelligence of its hominin/human symbiont (genetic evolution) that fostered 2.5 million years of: i) continuous brain size increase and niche-expansion within the genus Homo, and ii) parallel advances in the diversity, complexity and uses of UP-paralife. This coevolution also fostered evolutionary expansion of word-based communication, and eventually language, that acted in a catalyst-like manner to facilitate the evolution of increasingly complex forms of imagination, reasoning, mentalizing, and UP-generating technology. I next focus on the evolution of creativity in the human lineage –in the form of divergent thinking and creative imagination. I conclude that the evolution of this advanced cognitive feature required a preadaptation of sufficient intelligence and is the component of human cognition that was the major causal factor generating the greatly expanded diversity and complexity of UP-paralife currently associated with modern humans. Lastly, I apply my findings to the issue of the prevalence of extraterrestrial intelligent life. I conclude that any exoplanets with detected chemical life will very rarely (e.g., probability ~10-5 for a planet closely matching Earth’s characteristics) have evolved intelligence equalling or exceeding that of humans.
... In this paradigm, a food reward is placed behind a transparent barrier, and the animal must inhibit the prepotent response of directly approaching or reaching for the food reward to demonstrate inhibitory control (Kabadayi et al. 2018). Inhibitory control has frequently been explored in wolves and domestic dogs Brucks et al. 2019;Gnanadesikan et al. 2020;MacLean et al. 2014;Marshall-Pescini et al. 2015). Comparisons between these species have attempted to pinpoint the effects of domestication on this executive function, but Marshall-Pescini et al (2015) found that wolves outperformed dogs on a detour task (animals must detour around a fence to reach food), while dogs outperformed wolves on a cylinder task (animals must detour to an open side of a transparent cylinder to reach food), suggesting that these two paradigms may measure different aspects of inhibitory control. ...
... Outside of these species, inhibitory control has been limitedly explored in Carnivora. Spotted hyena, narrow-striped mongooses (Mungotictis decemlineata), coyotes, and domestic cats have been tested on inhibitory control Johnson-Ulrich et al. 2018MacLean et al. 2014;Rasolofoniaina et al. 2021a). These studies have shown the effects of social environments (Rasolofoniaina et al. 2021a), brain size , and testing apparatuses Marshall-Pescini et al. 2015) on inhibitory control performance. ...
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The field of animal cognition has advanced rapidly in the last 25 years. Through careful and creative studies of animals in captivity and in the wild, we have gained critical insights into the evolution of intelligence, the cognitive capacities of a diverse array of taxa, and the importance of ecological and social environments, as well as individual variation, in the expression of cognitive abilities. The field of animal cognition, however, is still being influenced by some historical tendencies. For example, primates and birds are still the majority of study species in the field of animal cognition. Studies of diverse taxa improve the generalizability of our results, are critical for testing evolutionary hypotheses, and open new paths for understanding cognition in species with vastly different morphologies. In this paper, we review the current state of knowledge of cognition in mammalian carnivores. We discuss the advantages of studying cognition in Carnivorans and the immense progress that has been made across many cognitive domains in both lab and field studies of carnivores. We also discuss the current constraints that are associated with studying carnivores. Finally, we explore new directions for future research in studies of carnivore cognition.
... For example, greater inhibitory control is advantageous when it is beneficial to behave flexibly (Coomes et al., 2021), such as to delay feeding in the presence of a socially dominant individual (Johnson-Ulrich & Holekamp, 2020), or refrain from engaging in sexual behaviour at inappropriate times (Rodriguez-Nieto et al., 2019). Strong inhibitory control is associated with greater intelligence in humans (Shamosh et al., 2008), and improved behavioural flexibility and larger brain size in primates (Amici et al., 2008;MacLean et al., 2014). Within species there is often high variability in inhibitory control among individuals, as seen in mammals (Johnson-Ulrich & Holekamp, 2020), birds (Kabadayi, Jacobs, et al., 2017;Kabadayi, Krasheninnikova, et al., 2017;Meier et al., 2017) and fish Macario et al., 2021;Savaş çı et al., 2021). ...
Article
Inhibitory control requires an individual to suppress impulsive actions in favour of more appropriate behaviours to gain a delayed reward. It plays an important role in activities such as foraging and initiating mating, but high within-species variation suggests that some individuals have greater inhibitory control than others. A standard index of inhibitory control used in many taxa is measuring how long an animal persists in trying to move itself or an appendage (e.g. its hand) through a transparent barrier to reach a reward. Although recent nonhuman studies have investigated how different factors are associated with variation in inhibitory control, these studies have rarely considered how these factors interact. Here we investigated how sex, age, personality (boldness) and the type of reward stimulus interact to predict the degree of motor inhibitory control in eastern mosquitofish, Gambusia holbrooki. We measured inhibitory control using a standard detour assay, ‘boldness’ (time to emergence in a novel environment), and the rate of learning. There were three different reward stimuli: a shoal of females, a shoal of males or a mixed-sex shoal. Individuals were tested in four consecutive trials, always with the same reward type, to quantify short-term learning. These measures were repeated at 7, 14 and 21 weeks after maturation to examine the effect of age. Females had significantly greater inhibitory control than males. Regardless of sex, older fish had significantly greater inhibitory control than younger fish, and boldness predicted learning ability. The type of reward stimuli had no sex-specific effect on inhibitory control. We discuss the biological significance of these sources of variation in inhibitory control, and the importance of accounting for them in studies examining individual differences in cognitive abilities.
... Similarly, the 'ecological intelligence' hypothesis predicts that a larger brain allows individuals to solve ecological problems such as managing spatial and temporal information associated with foraging (Clutton-Brock & Harvey, 1980;Parker & Gibson, 1977;Reader & Laland, 2002;Shultz & Dunbar, 2006). Correlational studies have indeed shown that organisms with larger brains exhibit greater cognitive flexibility (Buechel et al., 2018;Lefebvre et al., 2004;MacLean et al., 2014;van der Bijl et al., 2015), and that a larger brain is positively correlated with increased survival, a longer lifespan, enhanced foraging and an improved ability to colonise and survive in novel environments (Amiel et al., 2011;Garamszegi et al., 2002;González-Lagos et al., 2010;Jiménez-Ortega et al., 2020;Sayol et al., 2018;Sol et al., 2007Sol et al., , 2008Sol & Lefebvre, 2000;Yu et al., 2018; but see Drake, 2007). Experimental tests of the connection between brain size and fitness have the potential to provide new insights into the drivers of vertebrate brain size evolution. ...
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The extent to which the evolution of a larger brain is adaptive remains controversial. Trinidadian killifish (Anablepsoides hartii) are found in sites that differ in predation intensity; fish that experience decreased predation and increased intraspecific competition exhibit larger brains. We evaluated the connection between brain size and fitness (survival and growth) when killifish are found in their native habitats and when fish are transplanted from sites with predators to high‐competition sites that lack predators. Selection for a larger brain was absent within locally adapted populations. Conversely, there was a strong positive relationship between brain size and growth in transplanted but not resident fish in high‐competition environments. We also observed significantly larger brain sizes in the transplanted fish that were recaptured at the end of the experiment versus those that were not. Our results provide experimental support that larger brains increase fitness and are favoured in high‐competition environments.
... However, co-representation is also present in marmoset monkeys (Miss and Burkart, 2018), capuchin monkeys, and Tonkean macaques (Miss et al., 2022a) (see paragraph 4.3 on phylogeny). None of these three species has ToM abilities comparable to 4-to 5-year-old children, and also their inhibitory control abilities are clearly inferior (MacLean et al., 2014). Solving this puzzle requires us to scrutinize the potential mechanisms and modulating factors of the joint Simon effects in adult humans, as well as the emergence of co-representation at the neurobiological, ontogenetic, and phylogenetic level. ...
... Tonkean macaques and capuchin monkeys, in contrast, are independent breeders and thus comparatively less cooperative in their daily life (Burkart et al., , 2022Janson, 1985;Mendres and de Waal, 2000;Petit et al., 1992;Thierry et al., 1994). They too show inhibitory control and ToM abilities that by far do not match 4-year-old humans (MacLean et al., 2014). ...
Article
Joint action has increasingly become a key topic to understand the emergence of the human mind. The phenomenon is closely linked to several theoretical concepts, such as shared intentionality, which are difficult to operationalize empirically. We therefore employ a paradigm-driven, bottom-up approach, and as such discuss co-representing the partner’s and one’s own actions as key mechanism for joint action. After embedding co-representation in the broader landscape of related theoretical concepts, we review neurobiological, ontogenetic, and phylogenetic studies, with a focus on whether co-representation and its flexible deployment should be construed as a low- or high-level cognitive process. The empirical findings convergently suggest that co-representation does not require strong inhibitory skills or mentalistic understanding and occurs automatically. Moreover, more cooperative species are better at flexibly suppressing co-representation when required for cooperation success, and frequently rely on cooperation markers, such as mutual gaze. We thus contribute to closing the current gap between theoretical concepts related to joint action research and their empirical investigation, and end by highlighting additional approaches for doing so.
... The capacity for self-control has been described as the backbone of civilization (Freud, 1930) and of our development as a species (MacLean et al., 2014). Over the last 30 years, trait selfcontrol (i.e., the capacity to alter, override, or regulate dominant response tendencies) has been implicated as a powerful predictor of many behavioral outcomes of importance (De Ridder et al., 2012). ...
Article
Introduction: Trait self-control is one of the most robust predictors of important life outcomes. Recent evidence suggests at least two domains of self-control: inhibitory self-control (refraining from more attractive but goal-inconsistent behaviors) and initiatory self-control (engaging in and persisting in less attractive but goal-consistent behaviors). Methods: We examined longitudinal associations between these two self-control domains and subsequent post-incarceration behaviors in 492 jail inmates with a combination of self-reported questionnaires and official arrest records. Results: The two constructs were moderately associated, evidencing a similar-yet-distinct association of the same magnitude as depression and anxiety. Structural equation modeling demonstrated that inhibitory self-control uniquely predicted less recidivism and substance dependence, and better community adjustment. Initiatory self-control uniquely predicted less recidivism and better community adjustment. As expected, inhibitory self-control was a significantly better predictor of substance dependence than initiatory self-control. Discussion: These results have theoretical implications for the measurement of self-control and practical implications for the prediction of impactful post-incarceration behaviors and more precise interventions targeting specific self-control deficits.
... Even if it turns out that sentience is not the product of convergent evolution, we will end up relying heavily on the field of comparative cognition. The good news is that there has been a recent surge of interest in comparing species across metrics that may bear on questions about welfare ranges (MacLean et al., 2014;Cauchoix et al., 2018;Miller et al., 2022). There has been a concomitant surge in theoretical discussions about how to compare features across species, as seen in Weiss et al. (2019), which outlines a quantitative measure of social complexity that works across species. ...
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The number of animals bred, raised, and slaughtered each year is on the rise, resulting in increasing impacts to welfare. Farmed animals are also becoming more diverse, ranging from pigs to bees. The diversity and number of species farmed invites questions about how best to allocate currently limited resources towards safeguarding and improving welfare. This is of the utmost concern to animal welfare funders and effective altruism advocates, who are responsible for targeting the areas most likely to cause harm. For example, is tail docking worse for pigs than beak trimming is for chickens in terms of their pain, suffering, and general experience? Or are the welfare impacts equal? Answering these questions requires making an interspecies welfare comparison; a judgment about how good or bad different species fare relative to one another. Here, we outline and discuss an empirically-based methodology that aims to improve our ability to make interspecies welfare comparisons by investigating welfare range, which refers to how good or bad animals can fare. We begin our proposal with a theory of welfare. We operationalize that theory of welfare by identifying metrics that are defensible proxies for measuring welfare, including cognitive, affective, behavioral, and neuro-biological measures. We assign differential weights to those proxies that reflect their evidential value for the determinants of welfare, such as the “Delphi'' structured deliberation method with a panel of experts. Then we review the evidence and score its quality to ascertain whether a particular taxa may possess the proxies in question to construct a taxa-level welfare range profile. Finally, we use a Monte Carlo simulation to generate an overall estimate of comparative welfare range relative to our hypothetical index species - humans. Interspecies welfare comparisons will help facilitate empirically informed decision-making to streamline the allocation of resources and to ultimately better prioritize and improve animal welfare.
... 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.
... 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