Multiple Components of Phylogenetic Non-stationarity in the Evolution of Brain Size in Fossil Hominins

  • José Alexandre Felizola Diniz-FilhoEmail author
  • Lucas Jardim
  • Alessandro Mondanaro
  • Pasquale Raia
Research Article


One outstanding phenotypic character in Homo is its brain evolution. Pagel (Morphology, shape and phylogeny, CRC Press, Boca Raton, 2002) performed a phylogenetic analysis of the evolution of cranial capacity (as a surrogate of brain size) in fossil hominins, finding evidence for gradual evolutionary change with accelerating rate. Since Pagel’s pioneering investigation, the hominin fossil record expanded backward in time, new species were added to our family tree, different phylogenetic hypotheses were advanced, and new phylogenetic comparative methods became available. Therefore, we feel it is timely to repeat and expand upon Pagel’s seminal paper by including such material and applying novel methodologies. We fitted several evolutionary models to the endocranial volume (ECV) for 21 fossil hominins (including Pagel’s original analyses) and estimated phylogenetic signal using different approaches, while accounting for phylogenetic uncertainty. We then applied the phylogenetic signal-representation curve to the data to look for non-stationarity (discontinuities, rate shifts, or presence of different evolutionary patterns in different parts of the phylogeny) in brain size evolution. Our analyses show that, in principle, Pagel’s findings are robust to the addition of new data and phylogenetic uncertainty and confirm both the strong phylogenetic signal in brain size and acceleration of ECV evolutionary rates towards the present. However, non-stationarity was also detected in about 11% of the simulations, with two significant evolutionary discontinuities occurring close to the origin of the H. sapiens lineage (H. sapiens, H. neanderthalensis, H. heidelbergensis and H. antecessor) and along the phyletic line leading to H. floresiensis. This study calls upon further investigation of these important moments in Homo evolution, in order to understand the processes underling each of these shifts in brain size evolutionary regimes.


Phylogenetic comparative methods Evolutionary models Endocranial volume Non-stationarity Adaptive evolution Hominins 



We thank three anonymous reviewers and Luis Mauricio Bini for constructive criticisms that greatly improved early versions of the manuscript. Work by JAFD.-F on macroecology and macroevolution have been continuously supported by CNPq Productivity Grants and is developed in the context of National Institutes for Science and Technology (INCT) in Ecology, Evolution and Biodiversity Conservation, supported by MCTIC/CNpq (proc. 465610/2014-5) and FAPEG (Grant No. 201810267000023). L.J. receives a DTI fellowship from INCT and during early phases of this work was supported by a CAPES Doctoral fellowship.

Supplementary material

11692_2019_9471_MOESM1_ESM.docx (61 kb)
Supplementary material 1 (DOCX 61 KB)


  1. Antón, S. C., Potts, R., & Aiello, L. C. (2014). Evolution of early Homo: An integrated biological perspective. Science, 345(6192), 1236828.Google Scholar
  2. Argue, D., Groves, C. P., Lee, M. S. Y., & Jungers, W. L. (2017). The affinities of Homo floresiensis based on phylogenetic analyses of cranial, dental, and postcranial characters. Journal of Human Evolution, 107, 107–133.Google Scholar
  3. Baab, K. L. (2016a). The role of neurocranial shape in defining the boundaries of an expanded Homo erectus hypodigm. Journal of Human Evolution, 92, 1–21.Google Scholar
  4. Baab, K. L. (2016b). The place of Homo floresiensis in human evolution. Journal of Anthropological Sciences, 94, 5–18.Google Scholar
  5. Bapst, D. W. (2012). Paleotree: An R package for paleontological and phylogenetic analyses of evolution. Methods in Ecology and Evolution, 3(5), 803–807.Google Scholar
  6. Beaulieu, J. M., Jhwueng, D.-C., Boettiger, C., & O’Meara, B. C. (2012). Modeling stabilizing selection: Expanding the Ornstein-Uhlenbeck model of adaptive evolution. Evolution, 66(8), 2369–2383.Google Scholar
  7. Berger, L. R., et al. (2015). Homo naledi, a new species of the genus Homo from the Dinaledi chamber, South Africa. eLife, 4, e09560.Google Scholar
  8. Blomberg, S. P., Garland Jr, T., & Ives, A. R. (2003). Testing for phylogenetic signal in comparative data: Behavioral traits are more labile. Evolution, 57, 717–745.Google Scholar
  9. Bruner, E., Grimaud-Hervé, D., Wu, X., Cuétara, J. M., & Holloway, R. (2015). A paleoneurological survey of Homo erectus endocranial metrics. Quaternary International, 368, 80–87.Google Scholar
  10. Burnham, K. P., & Anderson, D. R. (2002). Model selection and multimodel inference. New York: Springer-Verlag.Google Scholar
  11. Butler, M. A., & King, A. A. (2004). Phylogenetic comparative analysis: A modeling approach for adaptive evolution. The American Naturalist, 164(6), 683–695.Google Scholar
  12. Carotenuto, F., Tsikaridze, N., Rook, L., Lordkipanidze, D., Longo, L., Condemi, S., & Raia, P. (2016). Venturing out safely: The biogeography of Homo erectus dispersal out of Africa. Journal of Human Evolution, 95, 1–12.Google Scholar
  13. Castiglione, S., Tesone, G., Piccolo, M., Melchionna, M., Mondanaro, A., Serio, C., et al. (2018). A new method for testing evolutionary rate variation and shifts in phenotypic evolution. Methods in Ecology and Evolution, 9(4), 974–983.Google Scholar
  14. Charvet, C. J., Darlington, R. B., & Finlay, B. L. (2013). Variation in human brains may facilitate evolutionary change toward a limited range of phenotypes. Brain, Behavior and Evolution, 81(2), 74–85.Google Scholar
  15. Dembo, M., Matzke, N. J., Mooers, A. O., & Collard, M. (2015). Bayesian analysis of a morphological supermatrix sheds light on controversial fossil hominin relationships. Proceedings of the Royal Society B, 282(1812), 20150943.Google Scholar
  16. Dembo, M., Radovčić, D., Garvin, H. M., Laird, M. F., Schroeder, L., Scott, J. E., et al. (2016). The evolutionary relationships and age of Homo naledi: An assessment using dated Bayesian phylogenetic methods. Journal of Human Evolution, 97, 17–26.Google Scholar
  17. Desdevises, Y., Legendre, P., Azouzi, L., & Morand, S. (2003). Quantifying phylogenetically structured environmental variation. Evolution, 57, 2647–2652.Google Scholar
  18. Diniz-Filho, J. A. F., Alves, D. M. C. C., Villalobos, F., Sakamoto, M., Brusatte, S. L., & Bini, L. M. (2015). Phylogenetic eigenvectors and non-stationarity in the evolution of theropod dinosaur skulls. Journal of Evolutionary Biology, 28(7), 1410–1416.Google Scholar
  19. Diniz-Filho, J. A. F., Bini, L. M., Sakamoto, M., & Brusatte, S. L. (2014). Phylogenetic eigenvector regression in paleobiology. Revista Brasileira de Paleontologia, 17(2), 105–122.Google Scholar
  20. Diniz-Filho, J. A. F., & Raia, P. (2017). Island Rule, quantitative genetics and brain–body size evolution in Homo floresiensis. Proceedings of the Royal Society B: Biological Sciences, 284(1857), 20171065.Google Scholar
  21. Diniz-Filho, J. A. F., Rangel, T. F., Santos, T., & Bini, L. M. (2012). Exploring pattern of interspecific variation in quantitative traits using sequential phylogenetic eigenvector regressions. Evolution, 66(4), 1079–1090.Google Scholar
  22. Diniz-Filho, J. A. F., Sant’Ana, C. E. R., & Bini, L. M. (1998). An eigenvector method for estimating phylogenetic inertia. Evolution, 52(5), 1247–1262.Google Scholar
  23. Diniz-Filho, J. A. F., Terribile, L. C., Da Cruz, M. J., Vieira, L. C. G. (2010). Hidden patterns of phylogenetic non-stationarity overwhelm comparative analyses of niche conservatism and divergence. Global Ecology and Biogeography, 9, 916–926.Google Scholar
  24. Dirks, P. H. G. M., et al. (2017). The age of Homo naledi and associated sediments in the Rising Star cave, South Africa. eLife, 6, e24231.Google Scholar
  25. Du, A., Zipkin, A. M., Hatala, K. G., Renner, E., Baker, J. L., Bianchi, S., et al. (2018). Pattern and process in hominin brain size evolution are scale-dependent. Proceedings of the Royal Society B: Biological Sciences, 285(1873), 20172738.Google Scholar
  26. Eastman, J. M., Alfaro, M. E., Joyce, P., Hipp, A. L., & Harmon, L. J. (2011). A novel comparative method for identifying shifts in the rate of character evolution on trees. Evolution, 65(12), 3578–3589.Google Scholar
  27. Eckhardt, R. B., Henneberg, M., Weller, A. S., & Hsu, K. J. (2014). Rare events in earth history include the LB1 human skeleton from Flores, Indonesia, as a developmental singularity, not a unique taxon. Proceedings of the National Academy of Sciences, 111(33), 11961–11966.Google Scholar
  28. Falk, D., Redmond, J. C. Jr., Guyer, J., Conroy, C., Recheis, W., Weber, G. W., & Seidler, H. (2000). Early hominid brain evolution: A new look at old endocasts. Journal of Human Evolution, 38, 695–717.Google Scholar
  29. Fischer, B., & Mitteroecker, P. (2015). Covariation between human pelvis shape, stature, and head size alleviates the obstetric dilemma. Proceedings of the National Academy of Sciences, 112(18), 5655–5660.Google Scholar
  30. Foley, R. A., Martin, L., Lahr, M. M., & Stringer, C. (2016). Major transitions in human evolution. Philosophical Transactions of Royal Society B, 371, 20150229.Google Scholar
  31. Freckleton, R. P., Cooper, N., & Jetz, W. (2011). Comparative methods as a statistical fix: The dangers of ignoring an evolutionary model. The American Naturalist, 178(1), E10–E17.Google Scholar
  32. Freckleton, R. P., Harvey, P. H., & Pagel, M. (2002). Phylogenetic analysis and comparative data: A test and review of evidence. American Naturalist, 160, 712–726.Google Scholar
  33. Freckleton, R. P., Phillimore, A., & Pagel, M. (2008). Relating traits to diversification: A simple test. The American Naturalist, 172(1), 102–115.Google Scholar
  34. Gómez-Robles, A., Hopkins, W. D., & Sherwood, C. C. (2013). Increased morphological asymmetry, evolvability and plasticity in human brain evolution. Proceedings of the Royal Society B: Biological Sciences, 280(1761), 20130575.Google Scholar
  35. Gómez-Robles, A., Smaers, J. B., Holloway, R. L., Polly, P. D., & Wood, B. A. (2017). Brain enlargement and dental reduction were not linked in hominin evolution. Proceedings of the National Academy of Sciences, 114(3), 468–473.Google Scholar
  36. González-Forero, M., & Gardner, A. (2018). Inference of ecological and social drivers of human brain-size evolution. Nature, 557(7706), 554–557.Google Scholar
  37. Grabowski, M. (2016). Bigger brains led to bigger bodies?: The correlated evolution of human brain and body size. Current Anthropology, 57(2), 174–196.Google Scholar
  38. Grabowski, M. W., Hatala, K. G., Jungers, W. L., & Richmond, B. G. (2015). Body mass estimates of hominin fossils and the evolution of human body size. Journal of Human Evolution, 85, 75–93.Google Scholar
  39. Grabowski, M. W., Voje, K. L., & Hansen, T. F. (2016). Evolutionary modeling and correcting for observation error support a 3/5 brain-body allometry for primates. Journal of Human Evolution, 94, 106–116.Google Scholar
  40. Guénard, G., Legendre, P., & Peres-Neto, P. (2013). Phylogenetic eigenvector maps: A framework to model and predict species traits. Methods in Ecology and Evolution, 4(12), 1120–1131.Google Scholar
  41. Hansen, T. F., & Martins, E. P. (1996). Translating between microevolutionary process and macroevolutionary patterns: Correlation structure of interspecific data. Evolution, 50(4), 1404–1417.Google Scholar
  42. Hansen, T. F., Pienaar, J., & Orzack, S. H. (2008). A comparative method for studying adaptation to a evolving environment. Evolution, 62(8), 1965–1977.Google Scholar
  43. Harmon, L. J., Weir, J. T., Brock, C. D., Glor, R. E., & Challenger, W. (2008). Geiger: Investigating evolutionary radiations. Bioinformatics, 24(1), 129–131.Google Scholar
  44. Hawks, J., et al. (2017). New fossil remains of Homo naledi from the Lesedi Chamber, South Africa. eLife, 6, e24232.Google Scholar
  45. Herculano-Houzel, S. (2012). The remarkable, yet not extraordinary, human brain as a scaled-up primate brain and its associated cost. Proceedings of the National Academy of Sciences, 109(Supplement_1), 10661–10668.Google Scholar
  46. Holloway, R. L. (2015). The evolution of human brain. In W. Henke & I. Tattersall (Eds.), Handbook of Paleonthropology (pp. 1961–1987). New York: Springer.Google Scholar
  47. Holloway, R. L., Hurst, S. D., Garvin, H. M., Schoenemann, P. T., Vanti, W. B., Berger, L. R., & Hawks, J. (2018). Endocast morphology of Homo naledi from the Dinaledi Chamber, South Africa. Proceedngs of the National Academy of Sciences United States of America, 115, 5738–5743.Google Scholar
  48. Hublin, J.-J., et al. (2017). New fossils from Jebel Irhoud, Morocco and the pan-African origin of Homo sapiens. Nature, 546, 289–292.Google Scholar
  49. Hughes, J. K., & Smith, S. J. (2008). Simulating global patterns of Pleistocene hominid morphology. Journal of Archaeological Science, 35, 2240–2249.Google Scholar
  50. Jablonski, D. (2017a). Approaches to macroevolution: 1. General concepts and origin of variation. Evolutionary Biology, 44(4), 427–450.Google Scholar
  51. Jablonski, D. (2017b). Approaches to macroevolution: 2. Sorting of variation, some overarching issues, and general conclusions. Evolutionary Biology, 44(4), 451–475.Google Scholar
  52. Kaifu, Y., Baba, H., Sutikna, T., Morwood, M. J., Kubo, D., Saptomo, E. W., et al. (2011). Craniofacial morphology of Homo floresiensis: Description, taxonomic affinities, and evolutionary implication. Journal of Human Evolution, 61(6), 644–682.Google Scholar
  53. Khabbazian, M., Kriebel, R., Rohe, K., & Ané, C. (2016). Fast and accurate detection of evolutionary shifts in Ornstein–Uhlenbeck models. Methods in Ecology and Evolution, 7(7), 811–824.Google Scholar
  54. Kubo, D., Kono, R. T., & Kaifu, Y. (2013). Brain size of Homo floresiensis and its evolutionary implications. Proceedings of the Royal Society B: Biological Sciences, 280(1760), 20130338.Google Scholar
  55. Legendre, P., & Legendre, L. (2012). Numerical ecology. Amsterdam: Elsevier.Google Scholar
  56. Leonard, W. R., Robertson, M. L., Snodgrass, J. J., & Kuzawa, C. W. (2003). Metabolic correlates of hominid brain evolution. Comparative Biochemistry and Physiology - A Molecular and Integrative Physiology, 136(1), 5–15.Google Scholar
  57. Lordkipanidze, D., Ponce de Leon, M. S., Margvelashvili, A., Rak, Y., Rightmire, G. P., Vekua, A., & Zollikofer, C. P. E. (2013). A complete skull from Dmanisi, Georgia, and the evolutionary biology of early Homo. Science, 342(6156), 326–331.Google Scholar
  58. Maslin, M., Shultz, S., & Trauth, M. H. (2015). A synthesis of the theories and concepts of early human evolution. Philosophical transactions of the Royal Society of London. Series B, Biological sciences, 370, 1–12.Google Scholar
  59. Montgomery, S. H. (2018). Hominin brain evolution: The only way is up? Current Biology, 28, R784–R802.Google Scholar
  60. Montgomery, S. H., Capellini, I., Barton, R., & Mundy, N. I. (2010). Reconstructing the ups and downs of primate brain evolution: Implications for adaptive hypotheses and Homo floresiensis. BMC Biology, 8(1), 9.Google Scholar
  61. Montgomery, S. H., Mundy, N. I., & Barton, R. A. (2016). Brain evolution and development: Adaptation, allometry and constraint. Proceedings of the Royal Society B: Biological Sciences, 283(1838), 20160433.Google Scholar
  62. Navarrete, A., Van Schaik, C. P., & Isler, K. (2011). Energetics and the evolution of human brain size. Nature, 480(7375), 91–93.Google Scholar
  63. Neubauer, S., & Hublin, J.-J. (2012). The evolution of human brain development. Evolutionary Biology, 39(4), 568–586.Google Scholar
  64. Neubauer, S., Hublin, J.-J., & Gunz, P. (2018). The evolution of modern human brain shape. Science Advances, 4, eaao5961.Google Scholar
  65. O’Meara, B. C., Ané, C., Sanderson, M. J., & Wainwright, P. C. (2006). Testing for different rates of continuous trait evolution using likelihood. Evolution, 60(5), 922–933.Google Scholar
  66. Pagel, M. (1999). Inferring the historical patterns of biological evolution. Nature, 401, 877–884.Google Scholar
  67. Pagel, M. (2002). Modelling the evolution of continuously varying characters on phylogenetic trees. In N. MacLeod & P. L. Forey (Eds.), Morphology, shape and phylogeny (pp. 269–286). Boca Raton: CRC Press.Google Scholar
  68. Pennell, M. W., & Harmon, L. J. (2013). An integrative view of phylogenetic comparative methods: Connections to population genetics, community ecology, and paleobiology. Annals of the New York Academy of Sciences, 1289(1), 90–105.Google Scholar
  69. Pilbeam, D., & Gould, S. J. (1974). Size and scaling in human evolution. Science, 186(4167), 892–901.Google Scholar
  70. R Core Team. (2018). R: A language and environment for statistical computing. Vienna: R Foundation for Statistical Computing. See.
  71. Rabosky, D. L. (2014). Automatic detection of key innovations, rate shifts, and diversity-dependence on phylogenetic trees. PLoS ONE, 9(2), e89543.Google Scholar
  72. Rabosky, D. L., Grundler, M., Anderson, C., Title, P., Shi, J. J., Brown, J. W., et al. (2014). BAMMtools: An R package for the analysis of evolutionary dynamics on phylogenetic trees. Methods in Ecology and Evolution, 5(7), 701–707.Google Scholar
  73. Rightmire, G. P. (2013). Homo erectus and Middle Pleistocene hominins: Brain size, skull form and species recognition. Journal of Human Evolution, 65, 223–252.Google Scholar
  74. Rohlf, F. J. (2001). Comparative methods for the analysis of continuous variables: Geometric interpretations. Evolution, 55(1996), 2143–2160.Google Scholar
  75. Ruff, C. B., Trinkaus, E., & Holliday, T. W. (1997). Body mass and encephalization in Pleistocene Homo. Nature, 387(6629), 173–176.Google Scholar
  76. Schoenemann, P. T. (2013). Hominin brain evolution. In D. R. Begun (Ed.), A companion to paleoanthropology (pp. 136–164). Oxford: Wiley-Blackwell.Google Scholar
  77. Schroeder, L., et al. (2017). Skull diversity in the Homo lineage and the relative position of Homo naledi. Journal of Human Evolution, 104, 124–135.Google Scholar
  78. Schroeder, L., & Ackermann, R. R. (2017). Evolutionary processes shaping diversity across Homo lineages. Journal of Human Evolution, 111, 1–17.Google Scholar
  79. Schroeder, L., & von Cramon-Taubadel, N. (2017). The evolution of hominoid cranial diversity: A quantitative genetic approach. Evolution, 71(11), 2634–2649.Google Scholar
  80. Shultz, S., & Maslin, M. (2013). Early human speciation, brain expansion and dispersal influenced by African climate pulses. PLoS ONE, 8, e76750.Google Scholar
  81. Spoor, F., et al. (2015). Reconstructed Homo habilis type OH 7 suggests deep-rooted species diversity in early Homo. Nature, 519, 83–86.Google Scholar
  82. Trueman, J. W. H. (2010). A new cladistic analysis of Homo floresiensis. Journal of Human Evolution, 59(2), 223–226.Google Scholar
  83. Uyeda, J. C., & Harmon, L. J. (2014). A novel Bayesian method for inferring and interpreting the dynamics of adaptive landscapes from phylogenetic comparative data. Systematic Biology, 63(6), 902–918.Google Scholar
  84. van den Bergh, G. D., Kaifu, Y., Kurniawan, I., Kono, R. T., Brumm, A., Setiyabudi, E., et al. (2016). Homo floresiensis-like fossils from the early Middle Pleistocene of Flores. Nature, 534(7606), 245–248.Google Scholar
  85. von Cramon-Taubadel, N. (2014). The microevolution of modern human cranial variation: Implications for hominin and primate evolution. Annals of Human Biology, 41, 323–335.Google Scholar
  86. Wood, B. (2010). Reconstructing human evolution: Achievements, challenges and opportunities. Proceedings National Academy of Sciences United States of America, 107, 8902–8909.Google Scholar
  87. Wood, B., & Lonergan, N. (2008). The hominin fossil record: Taxa, grades and clades. Journal of Anatomy, 212, 354–376.Google Scholar
  88. Zeitoun, V., Barriel, V., & Widianto, H. (2016). Phylogenetic analysis of the calvaria of Homo floresiensis. Comptes rendus - Palevol, 15(5), 555–568.Google Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Departamento de Ecologia, Instituto de Ciências Biológicas (ICB)Universidade Federal de Goiás (UFG)GoiâniaBrazil
  2. 2.Programa de Pós-Graduação em Ecologia & Evolução, ICBUFGGoiâniaBrazil
  3. 3.Dipartimento di Scienze della Terra, dell’Ambiente e delle RisorseUniversità di Napoli Federico IINapoliItaly

Personalised recommendations