Abstract
There is a strong trend toward increased brain size in mammalian evolution, with larger brains composed of more and larger neurons than smaller brains across species within each mammalian order. Does the evolution of increased numbers of brain neurons, and thus larger brain size, occur simply through the selection of individuals with more and larger neurons, and thus larger brains, within a population? That is, do individuals with larger brains also have more, and larger, neurons than individuals with smaller brains, such that allometric relationships across species are simply an extension of intraspecific scaling? Here we show that this is not the case across adult male mice of a similar age. Rather, increased numbers of neurons across individuals are accompanied by increased numbers of other cells and smaller average cell size of both types, in a trade-off that explains how increased brain mass does not necessarily ensue. Fundamental regulatory mechanisms thus must exist that tie numbers of neurons to numbers of other cells and to average cell size within individual brains. Finally, our results indicate that changes in brain size in evolution are not an extension of individual variation in numbers of neurons, but rather occur through step changes that must simultaneously increase numbers of neurons and cause cell size to increase, rather than decrease.
Highlights
Evolution—whose occurrence is evident in the morphological and genetic variations that characterize different species—is considered to feed on the raw material of intraspecific variation, shaped over generations by selective forces
This mechanism presupposes that, across individuals as across species, increased numbers of neurons are associated with increased average neuronal cell size in the same manner, such that interspecific allometric relationships between brain size and number of neurons are an extension of those relationships across individuals of a single species
Brain structure mass, brain mass and spinal cord mass had a range of variation between 1.33-fold and 3.50fold, depending on the structure, while numbers of neurons in these structures had a slightly larger range of variation (1.63- to 4.53-fold), but larger coefficients of variation (CV) than structure mass (Table 1)
Summary
Evolution—whose occurrence is evident in the morphological and genetic variations that characterize different species—is considered to feed on the raw material of intraspecific variation, shaped over generations by selective forces. The simplest mechanism to explain the evolutionary origin of brains with increased numbers of neurons associated with increased average neuronal cell size (and decreased average neuronal density; Mota and Herculano-Houzel, 2014) would be if they were the result of positive selection of those individuals within populations that carried the most neurons associated with decreased neuronal densities, and the largest brains. This mechanism presupposes that, across individuals as across species, increased numbers of neurons are associated with increased average neuronal cell size (and decreased neuronal density) in the same manner, such that interspecific allometric relationships between brain size and number of neurons are an extension of those relationships across individuals of a single species. We use the isotropic fractionator (Herculano-Houzel and Lent, 2005), which gives comparable results to stereology but in less time (Bahney and von Bartheld, 2014; Miller et al, 2014), to determine whether intraspecific variation in the size of CNS structures (brain and spinal cord) across individuals of the nonisogenic Swiss strain of mice (Mus musculus) is correlated with variation in the number of neurons and other cells that compose these structures as well as in the average cell size of neurons and other cells, inferred from neuronal and other cell densities in the different structures
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