An Adaptive Threshold in Mammalian Neocortical Evolution

Abstract

Expansion of the neocortex is a hallmark of human evolution. However, determining which adaptive mechanisms facilitated its expansion remains an open question. Here we show, using the gyrencephaly index (GI) and other physiological and life-history data for 102 mammalian species, that gyrencephaly is an ancestral mammalian trait. We find that variation in GI does not evolve linearly across species, but that mammals constitute two principal groups above and below a GI threshold value of 1.5, approximately equal to 109 neurons, which may be characterized by distinct constellations of physiological and life-history traits. By integrating data on neurogenic period, neuroepithelial founder pool size, cell-cycle length, progenitor-type abundances, and cortical neuron number into discrete mathematical models, we identify symmetric proliferative divisions of basal progenitors in the subventricular zone of the developing neocortex as evolutionarily necessary for generating a 14-fold increase in daily prenatal neuron production, traversal of the GI threshold, and thus establishment of two principal groups. We conclude that, despite considerable neuroanatomical differences, changes in the length of the neurogenic period alone, rather than any novel neurogenic progenitor lineage, are sufficient to explain differences in neuron number and neocortical size between species within the same principal group.

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Cited by papers we hold 5

• Evolution and cell-type specificity of human-specific genes preferentially expressed in progenitors of fetal neocortex · 2018
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• Dishing out mini-brains: Current progress and future prospects in brain organoid research · 2016
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• The hominoid-specific gene TBC1D3 promotes generation of basal neural progenitors and induces cortical folding in mice · 2016
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• Differences and similarities between human and chimpanzee neural progenitors during cerebral cortex development · 2016
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• Comparative genomics of brain size evolution · 2014
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