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.