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Homo sapiens and Neanderthals share high cerebral cortex integration into adulthood

Nature Ecology & Evolution volume 7, pages 42–50 (2023)Cite this article

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Abstract

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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Fig. 1: Patterns of postnatal integration in modern humans and chimpanzees.
Fig. 2: Macro-evolution of primate brain morphology and covariation.
Fig. 3: Evolutionary rates of integration within Hominoidea.

Data availability

All data required to replicate this study are available at https://doi.org/10.6084/m9.figshare.21202775. Source data are provided with this paper.

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The code required to replicate this study is available at https://doi.org/10.6084/m9.figshare.21202775.

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Acknowledgements

We are grateful to M. White, P. Piras and C. Fruciano for their useful comments during manuscript preparation.

Author information

Author notes

  1. These authors contributed equally: Gabriele Sansalone, Antonio Profico.

Authors and Affiliations

  1. Function, Evolution & Anatomy Research Lab, Zoology Division, School of Environmental and Rural Science, University of New England, Armidale, New South Wales, Australia

    Gabriele Sansalone, Stephen Wroe & Sarah Ledogar

  2. Institute for Marine Biological Resources and Biotechnology (IRBIM), National Research Council, Messina, Italy

    Gabriele Sansalone

  3. Department of Biology, University of Pisa, Pisa, Italy

    Antonio Profico

  4. Department of Neuroscience, Washington University School of Medicine, St. Louis, MO, USA

    Kari Allen

  5. Department of Health Sciences, East Tennessee State University, Johnson City, TN, USA

    Justin Ledogar

  6. Department of Archaeology & Palaeoanthropology, School of Humanities, University of New England, Armidale, New South Wales, Australia

    Sarah Ledogar

  7. College of Science and Engineering, Flinders University, Adelaide, South Australia, Australia

    Dave Rex Mitchell

  8. Department of Earth Sciences, Università degli Studi di Firenze, Florence, Italy

    Alessandro Mondanaro

  9. Department of Earth Sciences, Environment and Resources, Università degli Studi di Napoli Federico II, Monte Sant’Angelo, Naples, Italy

    Marina Melchionna, Silvia Castiglione & Pasquale Raia

  10. Research Centre in Evolutionary Anthropology and Palaeoecology, School of Biological and Environmental Sciences, Liverpool John Moores University, Liverpool, UK

    Carmela Serio

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Contributions

The study was conceived by G.S., A.P., S.W. and P.R. D.R.M., S.L., A.P., J.L., M.M. and K.A. processed the endocasts. S.L. and G.S. digitized the landmarks. G.S., P.R., A.P., C.S., S.C., M.M. and A.M. analysed the data. G.S., P.R., A.P. and S.W. wrote the manuscript with substantial contributions from all the other authors.

Corresponding authors

Correspondence to Gabriele Sansalone or Antonio Profico.

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The authors declare no competing interests.

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Nature Ecology & Evolution thanks Amelie Beaudet, Stephen Montgomery and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

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Extended data

Extended Data Fig. 1 Endocast local integration assessment.

The set of each semilandmark (a) and its 9 closest semilandmarks define the N-Core (b). The remaining semilandmarks define the C-Core (c). The N-Core and R-Core are subjected to two independent GPAs and the covariation between the two blocks is calculated by PLS (d). With CR the GPA is computed the entire set (e). The values from PLS and CR analyses are used to create a colour map of integration (f) and modularity (g).

Extended Data Fig. 2 Evolutionary rates of CR values within the Cercopithecinae clade.

Evolutionary rates of CR values within the Cercopithecinae clade.

Source data

Extended Data Fig. 3 Evolutionary rates of CR values within the Strepsirrhini.

Evolutionary rates of CR values within the Strepsirrhini.

Source data

Extended Data Fig. 4 Evolutionary rates of CR values within the family Cebidae.

Evolutionary rates of CR values within the family Cebidae.

Source data

Extended Data Table 1 R-PLS values
Full size table
Extended Data Table 2 Effect sizes of separate PLS analyses
Full size table
Extended Data Table 3 CR values measured after size and phylogenetic correction
Full size table

Supplementary information

Supplementary Information

Supplementary Figs. 1–4, Tables 1–3, specimens institutional codes and tree in Newick format.

Reporting Summary

Source data

Source Data Fig. 1

Statistical test results and display.

Source Data Fig. 2

Statistical test results and display.

Source Data Fig. 3

Statistical test results and display.

Source Data Extended Data Table 1

Statistical test results.

Source Data Extended Data Table 2

Statistical test results.

Source Data Extended Data Fig. 2

Statistical test results and display.

Source Data Extended Data Fig. 3

Statistical test results and display.

Source Data Extended Data Fig. 4

Statistical test results and display.

Source Data Extended Data Table 3

Statistical test results.

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Sansalone, G., Profico, A., Wroe, S. et al. Homo sapiens and Neanderthals share high cerebral cortex integration into adulthood. Nat Ecol Evol 7, 42–50 (2023). https://doi.org/10.1038/s41559-022-01933-6

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