A study of the evolutionary history of cortical folding in mammals, its relationship to physiological and life-history traits and the underlying cortical progenitor behavior during embryogenesis, explains the diversity of folding we see across modern mammals. The diversity of neocortical folding among mammals can be explained by two distinct neurogenic programs, which give rise to mammals with a highly folded neocortex and mammals with slightly folded or unfolded neocortex, each occupying a distinct ecological niche.
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.
What are the key differences in the development and evolution of the cerebral cortex that underlie the differences in its size and degree of folding across mammals? Here, we present phylogenetic evidence that the Jurassic era mammalian ancestor may have been a relatively large-brained species with a folded neocortex. We then show that variation in the degree of cortical folding (gyrencephaly index [GI]) does not evolve linearly across species, as previously assumed, but that mammals fall into two principal groups associated with distinct ecological niches: low-GI mammals (such as mice and tarsiers) and high-GI mammals (such as dolphins and humans), which are found to generate on average 14-fold more brain weight per day of gestation. This greater daily brain weight production in mammals with a highly folded neocortex requires a specific class of progenitor cell-type to adopt a special mode of cell division, which is absent in mammals with slightly folded or unfolded neocortices. Differences among mammals within the same GI group (high or low) are not due to different programming, but rather the result of differences in the length of the neurogenic period. So, the impressively large and folded human neocortex, which is three times the size of the chimpanzee neocortex, can be explained by a modest evolutionary extension of the neurogenic period with respect to its closest primate ancestors.