The evolution of brain neuron numbers in amniotes

Abstract

Significance The 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.

Mammals, birds and non-avian reptiles have signature proportions of numbers of neurons across their brain structures: Numbers of neurons increased differently with endothermy in birds and mammals

“…Across the 242 amniote species in the dataset, the total number of brain neurons varies over 100,000 fold, from just under 2 million in the Algerian sand gecko (Kverkova et al, 2022) to 257 billion in the African elephant (Herculano-Houzel et al, 2014a). However, contrary to the fairly homogeneous distribution of non-neuronal cells across brain structures, the distribution of neurons in amniote brains is very heterogeneous across structures in an individual brain, with neuronal densities that vary by over 1,000 times across brain structures that share non-neuronal densities that vary by less than a factor of 10 (Figure S3).…”

“…300 million years ago (Kemp, 2006), and their brains still share a common developmental program (Puelles et al, 2013). The largest amniote brains are all mammalian, but mammalian brains can be as small as those of some lizards; modern bird brains, in turn, are larger than most non-avian reptilian brains, but not larger than those of dog-sized mammals (Kverkova et al, 2022). How did so much diversity in brain size arise, how come the different ranges, and how do they compare in terms of numbers of neurons?…”

“…In birds, numbers of cells were also available for the two parts of the telencephalon: the pallium (directly equivalent to the mammalian cerebral cortex; Puelles et al, 2013) and subpallium (Olkowicz et al, 2016;Kverkova et al, 2022). While it is unfortunate that the subpallium was not separated from the pallium in the telencephalon of the reptiles examined, the total number of neurons in the reptilian telencephalon is small compared to the "rest of brain" in these species (Olkowicz et al, 2016;Kverkova et al, 2022).…”

“…The study that originally reported the reptile and extended bird dataset (Kverkova et al, 2022) focused on the grade shifts in the relationship between brain and body mass that characterize amniote evolution, but did not address a number of fundamental issues in amniote brain evolution, starting with the neuronal scaling rules that apply to each clade specifically that is necessary to shed light on the evolution of the amniote brain. Further, anchoring interpretations of brain evolution on relationships to body mass is a flawed expedient that (which was not certified by peer review) is the author/funder.…”

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Modern mammals, birds, and non-avian reptiles have shared developmental and evolutionary origins in the ancestral amniotes of 300 million years ago. A previous analysis of a newly completed dataset on the cellular composition of the major parts of the brain of 242 amniote species, generated using the same cell counting method, the isotropic fractionator, argued for changes in the body-brain relationship in amniote evolution (Kverkova et al, 2022), but did not explore how the brains of amniotes diverged in their neuronal composition. Here I show, using the same dataset but focusing instead on the cellular composition of the brains regardless of body mass and phylogenetic relatedness, that the brains of extant mammalian, avian, and nonavian reptile species are characterized by signature proportions of numbers of neurons across the pallium, the cerebellum, and the rest of brain.

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