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Divergence-time estimates for hominins provide insight into encephalization and body mass trends in human evolution

Nature Ecology & Evolution volume 5, pages 808–819 (2021)Cite this article

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Matters Arising to this article was published on 04 July 2022

Abstract

Quantifying speciation times during human evolution is fundamental as it provides a timescale to test for the correlation between key evolutionary transitions and extrinsic factors such as climatic or environmental change. Here, we applied a total evidence dating approach to a hominin phylogeny to estimate divergence times under different topological hypotheses. The time-scaled phylogenies were subsequently used to perform ancestral state reconstructions of body mass and phylogenetic encephalization quotient (PEQ). Our divergence-time estimates are consistent with other recent studies that analysed extant species. We show that the origin of the genus Homo probably occurred between 4.30 and 2.56 million years ago. The ancestral state reconstructions show a general trend towards a smaller body mass before the emergence of Homo, followed by a trend towards a greater body mass. PEQ estimations display a general trend of gradual but accelerating encephalization evolution. The obtained results provide a rigorous temporal framework for human evolution.

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Fig. 1: Alternative topological hypotheses tested in the TED analyses.
Fig. 2: Summary diagram of important palaeoclimatic and hominin evolution events plotted next to the four obtained consensus phylogenies and time divergence estimates.
Fig. 3: Body mass ACSR for each species mapped onto the four consensus time-calibrated phylogenies.
Fig. 4: PEQ ACSR for each species mapped onto the four consensus time-calibrated phylogenies.
Fig. 5: Boxplots of body mass (kg) and PEQ ACSR per node on the basis of a sample of 9,002 time-calibrated posterior trees.

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Data availability

All data analysed in this study are available in Supplementary Tables 2 and 3 and in a permanent repository at https://doi.org/10.5281/zenodo.4537445. Additionally, the data are available in an open access repository at https://github.com/HansPueschel/Hominin-div-time-evolution.

Code availability

The code and input files are available in a permanent repository at https://doi.org/10.5281/zenodo.4537445. In addition, the code and input files are available in an open access repository at https://github.com/HansPueschel/Hominin-div-time-evolution.

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Acknowledgements

This research was funded by the National Agency for Research and Development (ANID)/PFCHA/Doctorado en el extranjero Becas Chile/2018-72190003 to H.P.P.; a Marie Skłodowska-Curie Actions Individual Fellowship (H2020-MSCA-IF-2018-2020; no. 792611) and the European Research Council (ERC) starting grant PalM, under the European Union’s Horizon 2020 Research and Innovation Programme (no. 756226) to O.C.B.; and the Leverhulme Trust Early Career Fellowship, ECF-2018-264 to T.A.P.

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Authors and Affiliations

  1. School of GeoSciences, University of Edinburgh, Grant Institute, Edinburgh, UK

    Hans P. Püschel & Ornella C. Bertrand

  2. MRC Human Genetics Unit, MRC Institute of Genetics & Molecular Medicine, University of Edinburgh, Western General Hospital, Edinburgh, UK

    Joseph E. O’Reilly

  3. Primate Models for Behavioural Evolution Lab, Institute of Cognitive and Evolutionary Anthropology, School of Anthropology and Museum Ethnography, University of Oxford, Oxford, UK

    René Bobe & Thomas A. Püschel

  4. Gorongosa National Park, Sofala, Mozambique

    René Bobe

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  1. Hans P. Püschel
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Contributions

H.P.P. and T.A.P. conceived and designed the study. O.C.B. compiled the body mass and ECV dataset. J.E.O. provided methodological support. H.P.P. and T.A.P. carried out all the mentioned analyses and wrote an initial draft. H.P.P., O.C.B., J.E.O., R.B. and T.A.P. interpreted the obtained results and contributed to the writing of the submitted version of this work.

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Correspondence to Hans P. Püschel or Thomas A. Püschel.

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Peer review information Nature Ecology & Evolution thanks Fredrik Ronquist and the other, anonymous, reviewer(s) for their contribution to the peer review of this work. Peer reviewer reports are available.

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Extended data

Extended Data Fig. 1 Consensus trees with Bayesian posterior probabilities showing the support for the nodes.

a, Dembo et al.17 hypothesis, b, Au. sediba hypothesis, c, H. naledi hypothesis and d, H. floresiensis hypothesis. Node numbers mentioned in text are within the red circles. We used soft constraints to allow the unconstrained taxa (that is, H. sapiens, H. neanderthalensis, H. heidelbergensis and Denisovans) to change position freely within the tree. For more details about the constraints used, see the Methods section.

Extended Data Fig. 2 Prior sensitivity analysis.

The dots indicate the mean and the lines the associated 95% highest posterior density interval (HPD) of the divergence-time estimations for each node. Different colours indicate the different priors that were tested. See the Methods for further details about each one of the priors that were tested.

Extended Data Fig. 3 Brain mass ACSR for each species mapped onto the four consensus time-calibrated phylogenies.

a, Dembo et al.17 hypothesis, b, Au. sediba hypothesis, c, H. naledi hypothesis and d, H. floresiensis hypothesis. The ACSR values were reconstructed using a ML ancestral character estimation method under a Brownian motion model.

Extended Data Fig. 4 Brain mass (g) ACSR traitgram for each species mapped onto the four consensus time-calibrated phylogenies.

a, Dembo et al.17 hypothesis, b, Au. sediba hypothesis, c, H. naledi hypothesis and d, H. floresiensis hypothesis.

Extended Data Fig. 5 Body mass (kg) ACSR traitgram for each species mapped onto the four consensus time-calibrated phylogenies.

a, Dembo et al.17 hypothesis, b, Au. sediba hypothesis, c, H. naledi hypothesis and d, H. floresiensis hypothesis.

Extended Data Fig. 6 PEQ ACSR traitgram for each species mapped onto the four consensus time-calibrated phylogenies.

a, Dembo et al.17 hypothesis, b, Au. sediba hypothesis, c, H. naledi hypothesis and d, H. floresiensis hypothesis.

Extended Data Fig. 7 Boxplots of brain mass (g) ACSR per node based on a sample of 9002 time-calibrated posterior trees for each one of the plots.

a, Dembo et al.17 hypothesis, b, Au. sediba hypothesis, c, H. naledi hypothesis and d, H. floresiensis hypothesis. The red dots indicate the brain mass (g) ACSR conducted using the consensus trees (as in Extended Data Fig. 3). The median is indicated by the horizontal black line, the interquartile range (IQR) is the white box and the whiskers indicate the minimum and the maximum (at 1.5 * IQR of the lower and upper hinge respectively). For details of each node, see Fig. 2.

Extended Data Fig. 8 PGLS models of ln(body mass) on ln(brain mass) based on the different consensus trees.

a, Dembo et al.17 hypothesis, b, Au. sediba hypothesis, c, H. naledi hypothesis and d, H. floresiensis hypothesis. We used a generalised least-squares fit by restricted maximum likelihood (REML), and a Brownian motion correlation structure. The resulting equations and R2 are in the plots next to the regression line in red.

Extended Data Fig. 9 Boxplots of expected brain mass (a–d) and PEQ (e–h) for all the tips based on a sample of 9002 time-calibrated posterior trees for each one of the hypotheses.

a,e, Dembo et al.17 hypothesis; b,f, Au. sediba hypothesis; c,g, H. naledi hypothesis and d,h, H. floresiensis hypothesis. The red dots indicate the expected brain mass (in g) for the tips of the consensus trees (a–d), or alternatively, the PEQ calculated for the tips of the consensus trees (e–h). The median is indicated by the horizontal black line, the interquartile range (IQR) is the white box and the whiskers indicate the minimum and the maximum (at 1.5 * IQR of the lower and upper hinge respectively). Further details about the hypotheses and how the expected brain mass and the PEQ were calculated are provided in the Methods section.

Extended Data Fig. 10 Brain mass ACSR versus body mass ACSR regressions from the consensus trees for each one of hypotheses.

a–d, Regressions considering nodes 1 to 24, e–h, regressions considering nodes 1 to 13 and i-l, regressions considering nodes 13 to 24. a,e,i, Dembo et al.17 hypothesis; b, f,j, Au. sediba hypothesis; c,g,k, H. naledi hypothesis and d,h,l, H. floresiensis hypothesis. The regression equations and the R2 values are given next to the regression’s lines in red. Colours dark purple, yellow and green indicate nodes 1 to 12, node 13 and nodes 14 to 24, respectively. In the case of the H. floresiensis hypothesis, node 14 was highlighted in yellow instead of node 13 due changes in the position of this node for this hypothesis. Nodes 7, 8 and 23 are not considered due the lack of body mass and/or brain mass estimations.

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Püschel, H.P., Bertrand, O.C., O’Reilly, J.E. et al. Divergence-time estimates for hominins provide insight into encephalization and body mass trends in human evolution. Nat Ecol Evol 5, 808–819 (2021). https://doi.org/10.1038/s41559-021-01431-1

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