The evolution of brain neuron numbers in amniotes

Abstract

SignificanceThe evolution of brain processing capacity has traditionally been inferred from data on brain size. However, similarly sized brains of distantly related species can differ in the number and distribution of neurons, their basic computational units. Therefore, a finer-grained approach is needed to reveal the evolutionary paths to increased cognitive capacity. Using a new, comprehensive dataset, we analyzed brain cellular composition across amniotes. Compared to reptiles, mammals and birds have dramatically increased neuron numbers in the telencephalon and cerebellum, which are brain parts associated with higher cognition. Astoundingly, a phylogenetic analysis suggests that as few as four major changes in neuron-brain scaling in over 300 million years of evolution pave the way to intelligence in endothermic land vertebrates.

Keywords: brain size; cognition; evolution; intelligence; number of neurons.

Fig. 1.

Absolute and relative brain sizes mapped to amniote phylogeny. Relative brain size expressed as residuals from PGLS regression of log-transformed brain mass on log-transformed body mass is mapped on the tree, with the internal nodes showing relative brain sizes based on an ancestral reconstruction of brain and body mass. The outer bars represent log-transformed absolute brain mass. The Inset graphs show the density distribution of absolute and relative brain sizes in birds, mammals, and nonavian reptiles. Silhouette illustrations are from phylopic.org (see SI Appendix for detailed credits).

Fig. 2.

Absolute brain neuron numbers in amniotes and their allocations to major brain parts. (A) Absolute brain neuron numbers are plotted on the amniote phylogenetic tree. Bar lengths correspond to neuron numbers (note that the bars for the five species with the highest numbers of neurons have been truncated), while bar color indicates body mass on a logarithmic scale. The bars for reptiles have been enlarged 30 times in the Inset. (B) Allocation of total brain neurons to major brain parts. The gray-scale bars indicate the proportion of brain neurons found in the telencephalon, rest of brain, and cerebellum. Cerebellum is the dominant fraction in all mammals, while there are two distinct patterns in birds, with cerebellum being predominant in basally diverging birds and telencephalon in core land birds (Telluraves). In reptiles, the cerebellum generally contains fewer neurons than the rest of brain, which accounts for a negligible fraction of brain neurons in endotherms. An evolutionary trend of increasing cerebellar neuronal fraction is seen in turtles and crocodiles. Silhouette illustrations are from phylopic.org (see SI Appendix for detailed credits).

Fig. 3.

Shifts in neuron–brain scaling in amniotes and scaling of convergent allometric regimes. (A) Tree colors correspond to neuron density in the whole brain, with blue colors indicating low density and red colors high density. The arrows indicate the branches with shifts in allometric relationship between structure mass and neuron number (resulting in either an increase in neurons, arrow up; or a decrease in neurons, arrow down) for the whole brain, telencephalon, cerebellum, and rest of brain, identified by reversible-jump Markov chain Monte Carlo analysis with posterior probability of >0.7 for clades including more than three species. (B–E) Log-log plots of neuron number for structure mass with regression lines for the distinct regimes identified by PGLS analysis.

Fig. 4.

Phenograms showing the evolution of brain neuron numbers relative to body mass over time. Colors in phenograms correspond to major reptile lineages (squamates, turtles, crocodiles), primates and core land birds (the groups identified as having experienced significant shifts in allometric scaling), and other birds and mammals. The Inset graphs show the σ² for residuals from PGLS as estimated by a multiple-variance Brownian motion model, corresponding to the strength of allometric integration. All nonavian reptiles are grouped in red color. Primates are characterized by weaker allometric integration of the number of neurons with body mass relative to all other groups.

Fig. 5.

Large relative brain size tends to co-occur with high relative neuron density across amniotes. (A) Ancestral reconstruction of the relative number of brain neurons for brain mass is mapped on a phylogenetic tree. The outer bars represent relative brain size (calculated as residuals from PGLS regression of brain mass on body mass across the amniote dataset). (B–E) Plots of relative neuron density against relative brain size calculated across amniotes (B), birds (C), reptiles (D), and mammals (E). When analyzed across all amniotes, there is a significant positive association between larger relative brain size and higher relative neuron density (B) (PGLS;t₂₄₉ = 5.85, P < 0.001, λ = 0.92). This pattern holds also within birds (C) (PGLS;t₆₃ = 6.01, P < 0.001, λ = 0.52) and reptiles (D) (PGLS;t₁₀₈ = 3.74, P < 0.001, λ = 0.37), but not within mammals (E) (PGLS;t₇₄ = 1.15, P = 0.25, λ = 0.96). However, primates show a positive association between the analyzed traits (PGLS;t₉ = 2.77, P = 0.02, λ = 0.3; SI Appendix, Fig. S9). Silhouette illustrations are from phylopic.org (see SI Appendix for detailed credits).