Artificial selection on brain size leads to matching changes in overall number of neurons

Abstract

Neurons are the basic computational units of the brain, but brain size is the predominant surrogate measure of brain functional capacity in comparative and cognitive neuroscience. This approach is based on the assumption that larger brains harbor higher numbers of neurons and their connections, and therefore have a higher information-processing capacity. However, recent studies have shown that brain mass may be less strongly correlated with neuron counts than previously thought. Till now, no experimental test has been conducted to examine the relationship between evolutionary changes in brain size and the number of brain neurons. Here, we provide such a test by comparing neuron number in artificial selection lines of female guppies (Poecilia reticulata) with >15% difference in relative brain mass and numerous previously demonstrated cognitive differences. Using the isotropic fractionator, we demonstrate that large-brained females have a higher overall number of neurons than small-brained females, but similar neuronal densities. Importantly, this difference holds also for the telencephalon, a key region for cognition. Our study provides the first direct experimental evidence that selection for brain mass leads to matching changes in number of neurons and shows that brain size evolution is intimately linked to the evolution of neuron number and cognition.

Keywords: Artificial selection; brain size; cognition; isotropic fractionator; number of neurons.

Figure 1

Brain and telencephalon size compared between small‐ and large‐brained selection lines. (A) Brain‐body scaling in female guppies. Note that allometric lines for small‐ and large‐brained guppies have significantly different intercepts, clearly indicating difference (grade shift) in relative brain mass (for statistics, see SI Results). Absolute brain mass (B) and body mass (C) compared between selection lines. (D) Telencephalon mass plotted as a function of brain mass. Note that relative mass of the telencephalon does not differ between the selection lines (for statistics, see Supporting Information Results). Telencephalon mass fraction (E) and absolute telencephalon mass (F) compared between selection lines. Each point in the scatterplots represents the values for one individual, the lines represent the ordinary least squares regressions for small‐brained (the dashed lines) and large‐brained (the solid lines) female guppies. Box plots denote median, 95% confidence intervals of median, first and third quartiles, total range, and outliers. The statistical significance level in box plots is indicated as follows: ^{* * *} P < 0.001; ^{* *} P < 0.01; ^* P < 0.05; n.s., nonsignificant). LB, large‐brained line; SB, small‐brained line.

Figure 2

Neuronal scaling and neuron numbers compared between small‐ and large‐brained selection lines. (A) Number of neurons plotted as a function of brain mass. Note that the relationship between brain mass and the number of brain neurons does not differ between the selection lines (for statistics, see Supporting Information Results). (B) The total number of brain neurons compared between selection lines. (C) Number of neurons plotted as a function of body mass. Note that guppies of large‐brained line have significantly more neurons for a given body mass (for statistics, see Supporting Information Results). (D) Neuronal index (i.e., residuals from the neurons‐body regression line for all female guppies) compared between selection lines (see Figure 1 for explanation).

Figure 3

Neuronal scaling, densities, and numbers in the telencephalon. (A) Number of telencephalic neurons plotted as a function of telencephalon mass. Note that the relationship between telencephalon mass and number of telencephalic neurons does not differ between the selection lines (for statistics, see Supporting Information Results). (B and C) Neuronal densities in the telencephalon (B) and absolute number of telencephalic neurons (C) compared between selection lines (see Figure 1 for explanation).

Figure 4

Individual differences in brain and telencephalon size, neuron numbers, and densities. Relationship between brain mass (A), telencephalon mass (B), and neuron counts. These variables are ranked in descending order from the largest to the smallest and individual values are given on the sides of the graphs. Solid lines connect values measured in the same individual. Crossed lines indicate individual differences in neuronal densities.