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Comparative Cognition & Behavior Reviews doi: 10.3819/CCBR.2018.130008 Volume 13, 2018 Comparative Cognition & Behavior Reviews Beyond Brain Size: Uncovering the Neural Correlates of Behavioral and Cognitive Specialization Corina J. Logan Sarah Jelbert Department of Zoology, University of Cambridge Department of Psychology, University of Cambridge Shahar Avin Dieter Lukas Center for the Study of Existential Risk, University of Cambridge Department of Zoology, University of Cambridge Neeltje Boogert Rafael Mares Centre for Ecology and Conservation, University of Exeter Department of Anthropology, University of California, Davis and Smithsonian Tropical Research Institute Andrew Buskell Department of History and Philosophy of Science, Ana F. Navarrete University of Cambridge Centre for Biodiversity, University of St Andrews Fiona R. Cross Shuichi Shigeno School of Biological Sciences, University of Canterbury Department of Biology and Evolution of Marine Organisms, and International Centre of Insect Physiology and Ecology Stazione Zoologica Anton Dohrn Adrian Currie Stephen H. Montgomery Center for the Study of Existential Risk, University of Cambridge Department of Zoology, University of Cambridge Despite prolonged interest in comparing brain size and behavioral proxies of “intelligence” across taxa, the adaptive and cognitive significance of brain size variation remains elusive. Central to this problem is the continued focus on hominid cognition as a benchmark and the assumption that behavioral complexity has a simple relationship with brain size. Although comparative studies of brain size have been criticized for not reflecting how evolution actually operates, and for producing spurious, inconsistent results, the causes of these limitations have received little discussion. We show how these issues arise from implicit assumptions about what brain size measures and how it correlates with behavioral and cognitive traits. We explore how inconsistencies can arise through heterogeneity in evolutionary trajectories and selection pressures on neuroanatomy or neurophysiology across taxa. We examine how interference from ecological and life history variables complicates interpretations of brain–behavior correlations and point out how this problem is exacerbated by the limitations of brain and cognitive measures. These considerations, and the diversity of brain morphologies and behavioral capacities, suggest that comparative brain–behavior research can make greater progress by focusing on specific neuroanatomical and behavioral traits within relevant ecological and evolutionary contexts. We suggest that a synergistic combination of the “bottom-up” approach of classical neuroethology and the “top-down” approach of comparative biology/psychology within closely related but behaviorally diverse clades can limit the effects of heterogeneity, interference, and noise. We argue that this shift away from broad-scale analyses of superficial phenotypes will provide deeper, more robust insights into brain evolution. Keywords: brain evolution, cognition, comparative method, neuroethology, intelligence ISSN: 1911-4745 55 56 Logan et al. Motivation socialization. These investigations frequently emphasize One of the central motivations for research into the significance of brain size. Yet we now have a more brain measurement is its potential to reveal links sophisticated brain measurement tool kit available (e.g., between neuroanatomical structures and cognitive capa- data on neuronal density or molecular variables; Mont- bilities. Many debates on the evolution of brains and gomery, 2017). However, even with such a powerful tool complex behavior suggestive of advanced cognitive abil- kit, problems remain in establishing links between brain ities have privileged measures where humans come out size and cognitive abilities because the interpretation of on top. This bias has been built into a number of “mono- the correlated behaviors as more “complex” or “cogni- lithic” general hypotheses (Barton, 2012) claiming links tive” remain poorly elucidated (Healy & Rowe, 2007). between measures of absolute or relative brain size and Here, we argue that a fruitful approach linking a diverse range of proxy measures of complex behavior, brain measures and cognition involves deemphasizing such as “social” intelligence (Dunbar & Shultz, 2007a, coarse-grained notions of “intelligence” and whole-brain 2007b), “cultural” intelligence (Tomasello, 1999; van measurements in favor of (a) taxa-specific measurements Schaik & Burkart, 2011; van Schaik, Isler, & Burkart, of brains and ecologically meaningful behaviors, and 2012), “general” intelligence (Burkart, Schubiger, & (b) “bottom-up” extrapolation of intraspecies measures van Schaik, 2016; Reader, Hager, & Laland, 2011), and based on phylogenetic context. Based on our review of the behavioral drive (Navarrete, Reader, Street, Whalen, & various limitations that have previously been highlighted, Laland, 2016; Wyles, Kunkel, & Wilson, 1983). In each we conclude by developing a framework that incorporates of these cases, Homo sapiens emerge as the presumed bottom-up and top-down approaches to advance the field. pinnacle of a trajectory of brain evolution that correlates Central to this is a movement away from Homo sapiens with increasing behavioral flexibility, intelligence, or as the measuring stick for evaluating the neuroanatomi- cal features and behavioral capabilities of other animals. Author Note: Corina J. Logan, Department of Zoology, Uni- Aims versity of Cambridge, Downing Street, Cambridge, CB2 3EJ, We introduce a wide variety of research that exam- United Kingdom. ines brains and behavior across various phyla and Correspondence concerning this article should be addressed to discuss how lessons learned from disparate taxa can Corina J. Logan at [email protected]. inform the way we interpret brain evolution, even among more familiar taxa such as vertebrates. Our aim Acknowledgments: All authors contributed to the concepts in is to emphasize the advantages and disadvantages of this article at a workshop organized by Logan in March 2017. the different metrics, methods, and assumptions in this Montgomery structured the article. All authors wrote and edited field. Our review is structured to first provide an over- the article. Logan, Montgomery, Boogert, and Mares served view of the issues that limit interpretations of brain size as managing editors. All authors approved the final version for submission. We certify that what we have written represents studies (which readers may already be familiar with; see original scholarship. We are grateful for manuscript feedback the Limitations of Research on Brain Size and Cogni- from Nicky Clayton, Tim Clutton-Brock, Rob Barton, Anna tion section) and explain why the limitations arise in the Wilkinson, Alex DeCasien, James Higham, and two anony- context of two concepts borrowed from philosophy of mous reviewers, and we appreciate Christian Rutz for discus- science: noise and interference (see the sections Why Do sions about New Caledonian crow foraging innovations. We These Limitations of Brain–Behavior Comparative Stud- thank our funders: the Isaac Newton Trust and Leverhulme ies Arise? and Why Do Limitations in Brain–Behavior Trust for a Leverhulme Early Career Fellowship to CJL, which Comparative Studies Arise?). We end with our proposed funded the workshop on which this article is based; NERC for an framework for how to move forward in the study of Independent Research Fellowship to SHM; the European Re- brains and behavior (Beyond Brain Size section). search Council (Grant No. 3399933; SAJ); the Royal Society for a Dorothy Hodgkin Research Fellowship to NJB; the Royal • Limitations of Research on Brain Size and Cogni- Society of New Zealand Marsden Fund (UOC1301; FRC); the tion section: We review criticisms leveled against National Science Foundation (NSF BCS 1440755; RM); the comparative studies of brain size. John Templeton Foundation (AB); and the Templeton World Charity Foundation (AC; Note: The opinions expressed in this • Why Do These Limitations of Brain–Behavior publication are those of the author(s) and do not necessarily Comparative Studies Arise? Noise (p. 62) and Why Do reflect the views of Templeton World Charity Foundation). Limitations in Brain–Behavior Comparative Studies COMPARATIVE COGNITION & BEHAVIOR REVIEWS Beyond Brain Size 57 Arise? Evidence of Interference (p. 65) sections: We behavioral complexity and what we view as a cognitive go further by establishing why the recognized limi- trait (see the Assumptions and Limitations About What tations arise. By doing so, we show why broad-stroke Brains Mean for Cognition section). In each case, the narratives struggle to capture the wide diversity of lack of data supporting the validity of these assumptions neuroanatomical features and behavioral capacities directly limits our capacity to make reliable inferences in animals. on the link between brain size and cognition. • Beyond Brain Size section: We argue that a more targeted bottom-up approach that measures brains Assumptions and Limitations and behaviors at the intraspecies level to investigate of What Brain Size Measures cognitive, neuroanatomical, and behavioral diver- Brain size may seem like an easy neuroanatomical sity is needed to fully understand how behavioral trait to measure, and the ease of obtaining a data point complexity emerges from neural systems, and how for a species, using one to a few specimens, renders it a well, or poorly, brain size reflects this variation. historically
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