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.

Although brain size and the concept of intelligence have been extensively used in comparative neuroscience to study cognition and its evolution, such coarse-grained traits may not be informative enough about important aspects of neurocognitive systems. By taking into account the different evolutionary trajectories and the selection pressures on neurophysiology across species, Logan and colleagues suggest that the cognitive abilities of an organism should be investigated by considering the fine-grained and species-specific phenotypic traits that characterize it. In such a way, we would avoid adopting human-oriented, coarse-grained traits, typical of the standard approach in cognitive neuroscience. We argue that this standard approach can fail in some cases, but can, however, work in others, by discussing two major topics in contemporary neuroscience as examples: general intelligence and brain asymmetries.

This paper presents 13 hypotheses regarding the specific behavioral abilities that emerged at key milestones during the 600-million-year phylogenetic history from early bilaterians to extant humans. The behavioral, intellectual, and cognitive faculties of humans are complex and varied: we have abilities as diverse as map-based navigation, theory of mind, counterfactual learning, episodic memory, and language. But these faculties, which emerge from the complex human brain, are likely to have evolved from simpler prototypes in the simpler brains of our ancestors. Understanding the order in which behavioral abilities evolved can shed light on how and why our brains evolved. To propose these hypotheses, I review the available data from comparative psychology and evolutionary neuroscience.

Animal cognition experiments frequently reveal striking individual variation but rarely consider its causes and largely ignore its potential consequences. Studies often focus on a subset of high-performing subjects, sometimes viewing evidence from a single individual as sufficient to demonstrate the cognitive capacity of a species. We argue that the emphasis on demonstrating species-level cognitive capacities detracts from the value of individual variation in understanding cognitive development and evolution. We consider developmental and evolutionary interpretations of individual variation and use meta-analyses of data from published studies to examine predictors of individual performance. We show that reliance on small sample sizes precludes robust conclusions about individual abilities as well as inter- and intraspecific differences. We advocate standardization of experimental protocols and pooling of data between laboratories to improve statistical rigour. Our analyses show that cognitive performance is influenced by age, sex, rearing conditions and previous experience. These effects limit the validity of comparative analyses unless developmental histories are taken into account, and complicate attempts to understand how cognitive traits are expressed and selected under natural conditions. Further understanding of cognitive evolution requires efforts to elucidate the heritability of cognitive traits and establish whether elevated cognitive performance confers fitness advantages in nature.