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Evolutionary Lags in the Primate Brain Size/Body Size Relationship Revisited

PLOS One

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Reviewer #1: The paper “Evolutionary Lags in the Primate Brain Size/Body Size Relationship Revisited” provides thorough research on how brain size and body size are related in mammals. Author demonstrates a strong understanding of the topic and uses a clear, systematic approach. I have a few minor suggestions:

In the Methods section, it would help if the author explained better why RMA was chosen and what benefits it has compared to the more common OLS method.

In the Results section, Table 1 could be clearer if it included the standard errors and significance levels for the estimates.

Figure 1 is very interesting, but adding a legend to explain the symbols would make it easier to understand.

In the Discussion, the author should expand on how these findings relate to human evolution and what they mean for our understanding of brain development.

Overall, despite some small issues, this is a valuable piece of work that can be useful for other researchers studying evolution.

Reviewer #2: Dear Editors

This is my review of the manuscript Evolutionary Lags in the Primate Brain Size/Body Size Relationship Revisited.

The manuscript revisits the "brain lag hypothesis," which posits that during primate evolution, changes in brain size lagged behind changes in body size. Addressing a seminal 1999 analysis by Deaner & Nunn that found no evidence for this lag , the author re-analyzes their original dataset using updated molecular divergence dates and alternative statistical models (Reduced Major Axis regression and k-means clustering). The author concludes that a brain lag effect is indeed present. Furthermore, the study suggests that rather than merely catching up to a standard allometric baseline, certain primate lineages (and anthropoids in particular) overshot the regression line to occupy higher socio-cognitive end. The author attributes this to the cognitive demands of using large social groups as an anti-predator strategy, facilitated by energy savings from dietary shifts. The evolutionary trajectory of hominins is presented as a test case supporting this model.

Major Comments

The social brain is a fantastic hypothesis, but we know by now ECV is poor representation of the social brain circuitry, both in terms of functional neuroanatomy (Alcalá-López et al., 2018; Meshulam et al. 2025) and in evolutionary terms (Sansalone et al. 2023, Melchionna et al., 2025, Gutiérrez-Ibáñez). I feel the author should to the bare minimum, mention these studies and put a cautionary note about the use of brain volume to infer social cognition. This makes their arguments stronger, not weaker.

Suggested citations:

Meshulam, L., Angelaki, D., Benson, J., McRoberts, I., Noel, J.-P., Arlandis, J., Bonacchi, N., Bougrova, K., Catarino, J. A., Cazettes, F., Crombie, D., DeWitt, E. E., Freitas-Silva, L., Laranjeira, I. C., Mainen, Z. F., Meijer, G. T., Rai, P., Raiser, G., Rau, F., … Witten, I. B. (2025). A brain-wide map of neural activity during complex behaviour. Nature, 645(8079), 177–191. https://doi.org/10.1038/s41586-025-09235-0

Melchionna, M., Castiglione, S., Girardi, G., Profico, A., Mondanaro, A., Sansalone, G., Chatar, N., Pérez Ramos, A., Fernández-Monescillo, M., Serio, C., Pandolfi, L., Dembitzer, J., di Febbraro, M., Caliendo, M. M., di Costanzo, A., Morvillo, L., Esposito, A., & Raia, P. (2025). Cortical areas associated to higher cognition drove primate brain evolution. Communications Biology, 8(1), 80. https://doi.org/10.1038/s42003-025-07505-1

Gutiérrez-Ibáñez, C., Němec, P., Paré, M., Wylie, D. R., & Lefebvre, L. (2025). How do big brains evolve? Trends in Ecology & Evolution, 0(0). https://doi.org/10.1016/j.tree.2025.03.008

Alcalá-López, D., Smallwood, J., Jefferies, E., van Overwalle, F., Vogeley, K., Mars, R. B., Turetsky, B. I., Laird, A. R., Fox, P. T., Eickhoff, S. B., & Bzdok, D. (2018). Computing the Social Brain Connectome Across Systems and States. Cerebral Cortex (New York, N.Y. : 1991), 28(7), 2207–2232. https://doi.org/10.1093/cercor/bhx121

Sansalone, G., Profico, A., Wroe, S., Allen, K., Ledogar, J., Ledogar, S., Mitchell, D. R., Mondanaro, A., Melchionna, M., Castiglione, S., Serio, C., & Raia, P. (2023). Homo sapiens and Neanderthals share high cerebral cortex integration into adulthood. Nature Ecology & Evolution, 7(1), 42–50. https://doi.org/10.1038/s41559-022-01933-6

The author purposedly restricted their analysis to the Stephan et al. (1981) dataset to perfectly mirror Deaner & Nunn’s original methodology and isolate the impact of the statistical/dating changes. While this is methodologically sound for a direct rebuttal, relying exclusively on a 40-year-old dataset limits the broader applicability of the findings. I feel the manuscript would vastly benefit from the inclusion of a supplementary analysis using a modern, comprehensive primate brain/body size dataset (even if it requires using carefully corrected ECV data). This would demonstrate that the brain lag effect is a robust biological reality, rather than a mathematical artifact specific to the 1981 sample.

The author uses a path analysis of phylogenetic contrasts to conclude a strict causal sequence: group size selects for brain size, which then selects for body. While the Sobel tests of mediation provide statistical support for this sequence, inferring evolutionary causality and directional selection purely from cross-sectional contrast correlations remains inherently risky. The language surrounding this finding should be softened to acknowledge the limitations of the data structure, or further theoretical justification should be provided for why reverse causality (e.g., spare energy from body size permitting larger groups) is impossible.

Also, using k-means clustering on the residuals to define five statistical grades is a mathematically elegant way to handle data heterogeneity. However, the author later asserts that these grades map closely onto socio-cognitive grades. To avoid the appearance of statistical circularity, the manuscript should briefly detail how these specific k-means clusters align with independent biological or behavioral metrics of socio-cognitive complexity. Providing a concrete example of the taxa within these clusters and their corresponding social behaviors would ground the statistical grades in biological reality.

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Reviewer #2: No

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Evolutionary Lags in the Primate Brain Size/Body Size Relationship Revisited

PONE-D-25-66844R1

Dear Dr. Dunbar,

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Kind regards,

Federica Spani, Ph.D

Academic Editor

PLOS One

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