The evolution of brain neuron numbers in amniotes

Reconstructing the evolution of brain information-processing capacity is paramount for understanding the rise of complex cognition. Comparative studies of brain evolution typically use brain size as a proxy. However, to get a less biased picture of the evolutionary paths leading to high cognitive power, we need to compare brains not by mass but by numbers of neurons, which are their basic computational units. This study reconstructs the evolution of brains across amniotes by directly analyzing neuron numbers by using the largest dataset of its kind and including essential data on reptiles. We show that reptiles have not only small brains relative to body size but also low neuronal densities, resulting in average neuron numbers over 20 times lower than those in birds and mammals of similar body size. Amniote brain evolution is characterized by the following four major shifts in neuron–brain scaling. The most dramatic increases in brain neurons occurred independently with the appearance of birds and mammals, resulting in convergent neuron scaling in the two endotherm lineages. The other two major increases in the number of neurons happened in core land birds and anthropoid primates, which are two groups known for their cognitive prowess. Interestingly, relative brain size is associated with relative neuronal cell density in reptiles, birds, and primates but not in other mammals. This has important implications for studies using relative brain size as a proxy when looking for evolutionary drivers of animal cognition.

The evolution of cognitive capacity or “intelligence” and its underlying neural substrate has been of long-standing interest to biologists. Great strides have been made in understanding the evolution of brain size in vertebrates, with studies analyzing data on thousands of species (1–3). Since larger animals have larger brains but are not necessarily smarter, most studies of cognitive evolution use relative brain size (corrected for body size), which is thought to reflect extra neurons beyond those needed for controlling the body (4). We now have a good idea where major changes in brain–body scaling happened within birds (2) and mammals (3), and it is also clear that both mammals and birds have relatively larger brains than nonavian sauropsids (hereafter referred to as reptiles), although this has been rarely formally quantified because data on reptilian brain sizes are scarce (5).However, we still lack a clear picture of the evolution of actual brain processing capacity. This is because the same increase in relative brain size can be reached by different evolutionary paths, not always involving actual brain enlargement, and might often result from selection on body size (3). Moreover, similarly sized brains of distantly related species can harbor substantially different numbers of neurons overall and in major brain parts (6, 7). These two caveats invalidate the very idea that we can estimate extra neurons and glean information about cognitive capacity from absolute or relative brain size alone.This capacity is better determined by the number of neurons in the brain or specific brain parts (although their relative importance is still debated), their connections, interneuronal distance, and axonal conduction velocity (8, 9). Unlike brain size, though, these measures are not readily available for a sufficient number of species to be of practical use. Nevertheless, thanks to methodological advances (10), neuronal scaling rules (the allometric relationship between brain mass and neuron numbers) have now been determined for eight high-level mammalian clades (6, 11–13) as well as for a limited sampling of birds (14, 15).To get the big picture of amniote brain evolution, we have to include data on nonavian reptiles. The deepest split in amniote evolution occurred between the synapsid lineage, leading to mammals, and the sauropsid lineage, including reptiles and birds. We cannot tell if similarities between birds and mammals are due to shared ancestry or convergent evolution without considering reptiles. Yet, the dearth of quantitative data on reptile brains is striking—brain mass is available for 183 species (5, 16), compared to thousands for birds and mammals, and neuron numbers are known for a mere 4 reptile species (17–19).Taken together, to understand the evolution of brain processing capacity in amniotes, we need to include nonavian reptiles, consider changes in both brain–body and neuron–brain scaling, and examine the allocation of neurons to different brain parts. In this study, we provide these much needed data and reconstruct the big picture of brain evolution in amniotes in terms of neuron numbers.