Artificial selection on relative brain size in the guppy reveals costs and benefits of evolving a larger brain

Abstract

The large variation in brain size that exists in the animal kingdom has been suggested to have evolved through the balance between selective advantages of greater cognitive ability and the prohibitively high energy demands of a larger brain (the "expensive-tissue hypothesis"). Despite over a century of research on the evolution of brain size, empirical support for the trade-off between cognitive ability and energetic costs is based exclusively on correlative evidence, and the theory remains controversial. Here we provide experimental evidence for costs and benefits of increased brain size. We used artificial selection for large and small brain size relative to body size in a live-bearing fish, the guppy (Poecilia reticulata), and found that relative brain size evolved rapidly in response to divergent selection in both sexes. Large-brained females outperformed small-brained females in a numerical learning assay designed to test cognitive ability. Moreover, large-brained lines, especially males, developed smaller guts, as predicted by the expensive-tissue hypothesis, and produced fewer offspring. We propose that the evolution of brain size is mediated by a functional trade-off between increased cognitive ability and reproductive performance and discuss the implications of these findings for vertebrate brain evolution.

Figure 1

Relative Brain Size Responds Rapidly to Divergent Selection F0 is the parental generation; F1 and F2 are the first and second brain weight-selected generation, respectively. Depending on replicate, second-generation large- and small-brained females (left panel) differ by 8.0%–9.3% (p < 0.001) in relative brain size, while second-generation large- and small-brained males (right panel) differ by 5.0%–8.3% (p < 0.001). Depicted are the mean and SE values for residuals of brain weight regressed on body size within each generation and replicate. See also Figure S1 for experimental procedures and plots of raw data, and Table S1 for detailed results.

Figure 2

Cognitive Ability Improves with Increased Brain Size Large-brained females outperform small-brained females in a numerical learning task (p = 0.006), whereas there is no difference in males (p = 0.535). Depicted are the mean and SE values for the number of times, out of eight tests, that an individual chose the correct option (after accounting for the number of times each individual participated in the trials) of either two or four objects in females and males selected for large and small brain size. See Figure S2 for scheme of the testing apparatus.

Figure 3

Individuals Selected for Large Brain Size Decrease Gut Size and Offspring Production (A) In guppies selected for large and small brain size, gut size differed by 8% in females and 20% in males (p < 0.001, after controlling for body size). Depicted are the mean and SE values. See Table S3 for detailed results. (B) Pairs selected for large brain size showed a 19% decrease in the number of offspring in the first clutch (p = 0.01, after controlling for female age at reproduction). Depicted are the mean and SE values. See Table S4 for detailed results.