Individual variation in cognitive performance: developmental and evolutionary perspectives

Abstract

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.

Figure 1.

Variation in success rates of individuals of different species in experiments of (a) object permanence, (b) object properties and (c) causality transfers. Each dot represents a single individual; dots arranged in a single vertical line represent multiple individuals from one species. Variation among individuals within species increases with sample size, limiting the validity of between-species comparisons where few individuals have been tested. Species from left to right, with sample sizes of individuals and number of studies in brackets: (a) Ara maracana (1 individual/1 study); Macaca fuscata (1/1); Melopsittacus undulatus (1/1); Nymphicus hollandicus (1/1); Gorilla gorilla (2/2); Nomascus gabriellae (2/1); Nomascus leucogenys (2/1); Pan paniscus (2/1); Psittacus erithacus (2/2); Symphalangus syndactylus (2/1); Cebus capuchinus (3/1); Leucopsa rothschildi (3/1); Oreonax flavica (3/1); Garrulus glandarius (4/1); Hylobates lar (4/1); Streptopelia risoria (4/1); Macaca mulatta (7/2); Saimiri sciureus (7/1); Saguinus oedipus (8/1); Tursiops truncatus (8/1); Callitrhix jacchus (11/1); Pongo pygmaeus (12/3); Pan troglodytes (18/8); Canis canis (32/2); Felis catus (33/2). (b) Corvus moneduloides (2 individuals/2 studies); Octodon degus (4/1); Cactospiza pallida (5/1); Gorilla gorilla (6/1); Pongo pygmaeus (8/2); Cebus libidinosus (10/3); Cebus apella (19/3); Pan troglodytes (22/3). (c) Gorilla gorilla (3 individuals/2 studies); Bunopithecus hoolock (4/1); Corvus moneduloides (7/2); Cactospiza pallida (9/2); Pan paniscus (9/3); Pongo pygmaeus (9/3); Cebus apella (10/3); Corvus frugilegus (10/2); Pan troglodytes (18/5). Note that symbols were chosen to maximize visual contrast between different species in the figures, and are not consistent between (a), (b) and (c).

Figure 2.

Success rate by individual characteristics in experiments of (a) object permanence, (b) object properties, (c) causality transfer, (d) causality training and (e) mirror self-recognition. The black lines in the boxplots (a–d) depict the median percentage of trials solved in a given experiment, with boxes and whiskers indicating the quantiles. Values are based on raw data and can contain multiple entries per individual. The bars in (e) depict the percentage of individuals deemed by experimenters to have passed the mark test. Lines above the boxplots and bars connect values that are significantly different in GLMM analyses, correcting for other factors. Stars indicate significant differences: two stars indicate categories with significantly higher success rates than those with one star, which in turn had higher success rates than those with no stars. Note that, as the figure shows raw data, not controlling for other significant factors, some significant differences are not apparent from visual inspection alone.