Larger Fish Have Larger Brains With More Neurons Across but Not Within Cohorts Raised in Different Growth Conditions

Comparative work on brain size variation across vertebrates has shown that larger species have larger brains and that larger brains have more neurons across species in each clade. This trend supports the expectation that larger bodies require larger brains with more neurons but is at odds with the finding that within a species, larger animals do not necessarily have larger brains, and larger brains do not have more neurons. While the latter finding is inconsistent with the expectation that larger brained species evolve through selection of larger brained individuals, the lack of correlation between brain size and numbers of neurons across individuals of a same species might be due to the small range of variation that is typically found within a species. Here, we take advantage of ecologically regulated indeterminate growth exhibited by the cichlid fish tilapia (Oreochromis mossambicus) raised under different population densities to generate an over 30-fold variation in body mass across adult individuals of the same age. We find that across the cohorts of individuals raised with different growth opportunities provided by different population densities, larger animals have larger brains with more neurons that occur at similar neuronal densities, as applies to interspecific scaling in several vertebrate clades. Within each cohort raised at a given population density, however, those animals with more neurons have higher neuronal densities, but not larger brains or bodies, though the latter scale together—as applies to intraspecific scaling in mice and chickens. We conclude that brain size and number of neurons are determined independently across individuals in a population but scale together across cohorts, in step changes that accompany varying opportunities for growth, in the absence of any selection pressure. Based on these results, we propose a model of brain evolution through plastic changes in response to changing environmental opportunities that accounts for intra-, inter-, and clade-specific patterns of brain scaling and diversity.