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

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Abstract

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.

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References

  • Antón, S. C., Potts, R., & Aiello, L. C. (2014). Evolution of early Homo: An integrated biological perspective. Science, 345(6192), 1236828.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Baab, K. L. (2016b). The place of Homo floresiensis in human evolution. Journal of Anthropological Sciences, 94, 5–18.

    PubMed  Google Scholar 

  • Bapst, D. W. (2012). Paleotree: An R package for paleontological and phylogenetic analyses of evolution. Methods in Ecology and Evolution, 3(5), 803–807.

    Article  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Berger, L. R., et al. (2015). Homo naledi, a new species of the genus Homo from the Dinaledi chamber, South Africa. eLife, 4, e09560.

    Article  PubMed Central  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Burnham, K. P., & Anderson, D. R. (2002). Model selection and multimodel inference. New York: Springer-Verlag.

    Google Scholar 

  • Butler, M. A., & King, A. A. (2004). Phylogenetic comparative analysis: A modeling approach for adaptive evolution. The American Naturalist, 164(6), 683–695.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Desdevises, Y., Legendre, P., Azouzi, L., & Morand, S. (2003). Quantifying phylogenetically structured environmental variation. Evolution, 57, 2647–2652.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Foley, R. A., Martin, L., Lahr, M. M., & Stringer, C. (2016). Major transitions in human evolution. Philosophical Transactions of Royal Society B, 371, 20150229.

    Article  CAS  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Freckleton, R. P., Phillimore, A., & Pagel, M. (2008). Relating traits to diversification: A simple test. The American Naturalist, 172(1), 102–115.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • González-Forero, M., & Gardner, A. (2018). Inference of ecological and social drivers of human brain-size evolution. Nature, 557(7706), 554–557.

    Article  PubMed  CAS  Google Scholar 

  • Grabowski, M. (2016). Bigger brains led to bigger bodies?: The correlated evolution of human brain and body size. Current Anthropology, 57(2), 174–196.

    Article  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Hansen, T. F., & Martins, E. P. (1996). Translating between microevolutionary process and macroevolutionary patterns: Correlation structure of interspecific data. Evolution, 50(4), 1404–1417.

    Article  PubMed  Google Scholar 

  • Hansen, T. F., Pienaar, J., & Orzack, S. H. (2008). A comparative method for studying adaptation to a evolving environment. Evolution, 62(8), 1965–1977.

    PubMed  Google Scholar 

  • Harmon, L. J., Weir, J. T., Brock, C. D., Glor, R. E., & Challenger, W. (2008). Geiger: Investigating evolutionary radiations. Bioinformatics, 24(1), 129–131.

    Article  PubMed  CAS  Google Scholar 

  • Hawks, J., et al. (2017). New fossil remains of Homo naledi from the Lesedi Chamber, South Africa. eLife, 6, e24232.

    Article  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Holloway, R. L. (2015). The evolution of human brain. In W. Henke & I. Tattersall (Eds.), Handbook of Paleonthropology (pp. 1961–1987). New York: Springer.

    Chapter  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Hublin, J.-J., et al. (2017). New fossils from Jebel Irhoud, Morocco and the pan-African origin of Homo sapiens. Nature, 546, 289–292.

    Article  PubMed  CAS  Google Scholar 

  • Hughes, J. K., & Smith, S. J. (2008). Simulating global patterns of Pleistocene hominid morphology. Journal of Archaeological Science, 35, 2240–2249.

    Article  Google Scholar 

  • Jablonski, D. (2017a). Approaches to macroevolution: 1. General concepts and origin of variation. Evolutionary Biology, 44(4), 427–450.

    Article  PubMed  Google Scholar 

  • Jablonski, D. (2017b). Approaches to macroevolution: 2. Sorting of variation, some overarching issues, and general conclusions. Evolutionary Biology, 44(4), 451–475.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  PubMed  PubMed Central  Google Scholar 

  • Legendre, P., & Legendre, L. (2012). Numerical ecology. Amsterdam: Elsevier.

    Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Montgomery, S. H. (2018). Hominin brain evolution: The only way is up? Current Biology, 28, R784–R802.

    Article  CAS  Google Scholar 

  • 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.

    Article  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  PubMed  PubMed Central  Google Scholar 

  • Navarrete, A., Van Schaik, C. P., & Isler, K. (2011). Energetics and the evolution of human brain size. Nature, 480(7375), 91–93.

    Article  PubMed  CAS  Google Scholar 

  • Neubauer, S., & Hublin, J.-J. (2012). The evolution of human brain development. Evolutionary Biology, 39(4), 568–586.

    Article  Google Scholar 

  • Neubauer, S., Hublin, J.-J., & Gunz, P. (2018). The evolution of modern human brain shape. Science Advances, 4, eaao5961.

    Article  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Pagel, M. (1999). Inferring the historical patterns of biological evolution. Nature, 401, 877–884.

    Article  CAS  Google Scholar 

  • 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.

    Chapter  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Pilbeam, D., & Gould, S. J. (1974). Size and scaling in human evolution. Science, 186(4167), 892–901.

    Article  PubMed  CAS  Google Scholar 

  • R Core Team. (2018). R: A language and environment for statistical computing. Vienna: R Foundation for Statistical Computing. http://www.R-project.org. See.

  • Rabosky, D. L. (2014). Automatic detection of key innovations, rate shifts, and diversity-dependence on phylogenetic trees. PLoS ONE, 9(2), e89543.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Rightmire, G. P. (2013). Homo erectus and Middle Pleistocene hominins: Brain size, skull form and species recognition. Journal of Human Evolution, 65, 223–252.

    Article  PubMed  Google Scholar 

  • Rohlf, F. J. (2001). Comparative methods for the analysis of continuous variables: Geometric interpretations. Evolution, 55(1996), 2143–2160.

    Article  PubMed  CAS  Google Scholar 

  • Ruff, C. B., Trinkaus, E., & Holliday, T. W. (1997). Body mass and encephalization in Pleistocene Homo. Nature, 387(6629), 173–176.

    Article  PubMed  CAS  Google Scholar 

  • Schoenemann, P. T. (2013). Hominin brain evolution. In D. R. Begun (Ed.), A companion to paleoanthropology (pp. 136–164). Oxford: Wiley-Blackwell.

    Chapter  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Schroeder, L., & Ackermann, R. R. (2017). Evolutionary processes shaping diversity across Homo lineages. Journal of Human Evolution, 111, 1–17.

    Article  PubMed  Google Scholar 

  • Schroeder, L., & von Cramon-Taubadel, N. (2017). The evolution of hominoid cranial diversity: A quantitative genetic approach. Evolution, 71(11), 2634–2649.

    Article  PubMed  Google Scholar 

  • Shultz, S., & Maslin, M. (2013). Early human speciation, brain expansion and dispersal influenced by African climate pulses. PLoS ONE, 8, e76750.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Spoor, F., et al. (2015). Reconstructed Homo habilis type OH 7 suggests deep-rooted species diversity in early Homo. Nature, 519, 83–86.

    Article  PubMed  CAS  Google Scholar 

  • Trueman, J. W. H. (2010). A new cladistic analysis of Homo floresiensis. Journal of Human Evolution, 59(2), 223–226.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Wood, B. (2010). Reconstructing human evolution: Achievements, challenges and opportunities. Proceedings National Academy of Sciences United States of America, 107, 8902–8909.

    Article  Google Scholar 

  • Wood, B., & Lonergan, N. (2008). The hominin fossil record: Taxa, grades and clades. Journal of Anatomy, 212, 354–376.

    Article  PubMed  PubMed Central  Google Scholar 

  • Zeitoun, V., Barriel, V., & Widianto, H. (2016). Phylogenetic analysis of the calvaria of Homo floresiensis. Comptes rendus - Palevol, 15(5), 555–568.

    Article  Google Scholar 

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Acknowledgements

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.

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Diniz-Filho, J.A.F., Jardim, L., Mondanaro, A. et al. Multiple Components of Phylogenetic Non-stationarity in the Evolution of Brain Size in Fossil Hominins. Evol Biol 46, 47–59 (2019). https://doi.org/10.1007/s11692-019-09471-z

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