There is controversy around the mechanisms that guided the change in brain shape during the evolution of modern humans. It has long been held that different cortical areas evolved independently from each other to develop their unique functional specializations. However, some recent studies suggest that high integration between different cortical areas could facilitate the emergence of equally extreme, highly specialized brain functions. Here, we analyse the evolution of brain shape in primates using three-dimensional geometric morphometrics of endocasts. We aim to determine, firstly, whether modern humans present unique developmental patterns of covariation between brain cortical areas; and secondly, whether hominins experienced unusually high rates of evolution in brain covariation as compared to other primates. On the basis of analyses including modern humans and other extant great apes at different developmental stages, we first demonstrate that, unlike our closest living relatives, Homo sapiens retain high levels of covariation between cortical areas into adulthood. Among the other great apes, high levels of covariation are only found in immature individuals. Secondly, at the macro-evolutionary level, our analysis of 400 endocasts, representing 148 extant primate species and 6 fossil hominins, shows that strong covariation between different areas of the brain in H. sapiens and Homo neanderthalensis evolved under distinctly higher evolutionary rates than in any other primate, suggesting that natural selection favoured a greatly integrated brain in both species. These results hold when extinct species are excluded and allometric effects are accounted for. Our findings demonstrate that high covariation in the brain may have played a critical role in the evolution of unique cognitive capacities and complex behaviours in both modern humans and Neanderthals.
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