Evolutionary Biology

, Volume 39, Issue 4, pp 587–599 | Cite as

Brain Size Growth and Life History in Human Evolution

Synthesis Paper

Abstract

Increases in endocranial volume (a measure of brain size) play a major role in human evolution. Despite the importance of brain size increase, the developmental bases of human brain size evolution remain poorly characterized. Comparative analyses of endocranial volume size growth illustrate that distinctions between humans and other primates are consequences of differences in rates of brain size growth, with little evidence for differences in growth duration. Evaluation of available juvenile fossils shows that earliest hominins do not differ perceptibly from chimpanzees (Pan). However, rapid and human-like early brain growth apparently characterized Homo erectus at about 1 Ma before present. Neandertals show patterns of brain growth consistent with modern humans during infancy, but reach larger sizes than modern humans as a result of differences in later growth. Growth analyses reveal commonalities in patterns of early brain size growth during the last million years human evolution, despite major increases in adult size. This result implies consistency across hominins in terms of maternal metabolic costs of infancy. Continued size growth past infancy in Neandertals and modern humans, when compared to earlier hominins, may have cognitive implications. Differences between Neandertals and modern humans are implied, but difficult to define with certainty.

Keywords

Ontogeny Paleoanthropology Australopithecus Homo erectus Neandertals 

References

  1. Aiello, L. C., Bates, N., & Joffe, T. (2001). In defense of the expensive tissue hypothesis. In D. Falk & K. R. Gibson (Eds.), Evolutionary anatomy of the primate cerebral cortex (pp. 57–78). New York: Cambridge University Press.CrossRefGoogle Scholar
  2. Aiello, L. C., & Wheeler, P. (1995). The expensive tissue hypothesis. Current Anthropology, 36, 199–222.CrossRefGoogle Scholar
  3. Alemseged, Z., Spoor, F., Kimbel, W. H., Bobe, R., Geraads, D., Reed, D., et al. (2006). A juvenile early hominin skeleton from Dikika, Ethiopia. Nature, 443, 296–301.PubMedCrossRefGoogle Scholar
  4. Allman, J., & Hasenstaub, A. (1999). Brains, maturation times, and parenting. Neurobiology of Aging, 20, 447–454.PubMedCrossRefGoogle Scholar
  5. Allman, J. M., McLaughlin, T., & Hakeem, A. (1993). Brain structures and life-span in primate species. Proceedings of the National Academy of Sciences of the United States of America, 90, 3559–3563.PubMedCrossRefGoogle Scholar
  6. Antón, S. C. (1997). Developmental age and taxonomic affinity of the Mojokerto child, Java, Indonesia. American Journal of Physical Anthropology, 102, 497–514.PubMedCrossRefGoogle Scholar
  7. Armstrong, E. (1985). Relative brain size in monkeys and prosimians. American Journal of Physical Anthropology, 66, 263–273.CrossRefGoogle Scholar
  8. Barrickman, N. L., Bastian, M. L., Isler, K., & van Schaik, C. P. (2008). Life history costs and benefits of encephalization: A comparative test using data from long-term studies of primates in the wild. Journal of Human Evolution, 54, 568–590.PubMedCrossRefGoogle Scholar
  9. Berge, C., & Goularas, D. (2010). A new reconstruction of STS 14 pelvis (Australopithecus africanus) from computed tomography and three-dimensional modeling techniques. Journal of Human Evolution, 58, 262–272.PubMedCrossRefGoogle Scholar
  10. Black, J. E., Greenough, W. T., Anderson, B. J., & Isaacs, K. R. (1987). Environment and the aging brain. Canadian Journal of Psychology, 41, 111–130.PubMedGoogle Scholar
  11. Blomquist, G. E. (2009). Trade-off between age of first reproduction and survival in a female primate. Biology Letters, 5, 339–342.PubMedCrossRefGoogle Scholar
  12. Bruner, E., & Holloway, R. L. (2010). A bivariate approach to the widening of the frontal lobes in the genus Homo. Journal of Human Evolution, 58, 138–146.PubMedCrossRefGoogle Scholar
  13. Cleveland, W. S., & Devlin, S. J. (1988). Locally weighted regression: An approach to regression analysis by local fitting. Journal of the American Statistical Association, 83, 596–610.CrossRefGoogle Scholar
  14. Cleveland, W. S. (1979). Robust locally weighted regression and smoothing scatterplots. Journal of American Statistical Association, 74, 829–836.CrossRefGoogle Scholar
  15. Coqueugniot, H., Hublin, J.-J., Veillon, F., Houet, F., & Jacob, T. (2004). Early brain growth in Homo erectus and implications for cognitive ability. Nature, 431, 299–302.PubMedCrossRefGoogle Scholar
  16. Count, E. W. (1947). Brain and body weight in man: Their antecedents in growth and evolution. Annals of the New York Academy of Sciences, XLVI, 993–1122.CrossRefGoogle Scholar
  17. Dart, R. A. (1925). Australopithecus africanus: The man-ape of South Africa. Nature, 115, 195–199.CrossRefGoogle Scholar
  18. Darwin, C. (1859). On the Origin of the Species by Means of Natural Selection, or, the Preservation of Favoured Races in the Struggle for Life. London: J. Murray.Google Scholar
  19. d’Errico, F., Vanhaeren, M., Barton, N., Bouzouggar, A., Mienis, H., Richter, D., et al. (2009). Out of Africa: Modern human origins special feature: Additional evidence on the use of personal ornaments in the middle paleolithic of North Africa. Proceedings of the National Academy of Sciences of the United States of America, 106, 16051–16056.PubMedCrossRefGoogle Scholar
  20. DeSilva, J. M., & Lesnik, J. (2008). Brain size at birth throughout human evolution: A new method for estimating neonatal brain size in hominins. Journal of Human Evolution, 55, 1064–1074.PubMedCrossRefGoogle Scholar
  21. Dorus, S., Vallender, E. J., Evans, P. D., Anderson, J. R., Gilbert, S. L., Mahowald, M., et al. (2004). Accelerated evolution of nervous system genes in the origin of homo sapiens. Cell, 119, 1027–1040.PubMedCrossRefGoogle Scholar
  22. Dubois, E. (1897). Ueber die Abhängigkeit des Hirngewichtes von derKörpergrösse bei den Säugtieren. Archives of Anthropology, 25, 1–28.Google Scholar
  23. Evans, P. D., Vallender, E. J., & Lahn, B. T. (2006). Molecular evolution of the brain size regulator genes CDK5RAP2 and CENPJ. Gene, 375, 75–79.PubMedCrossRefGoogle Scholar
  24. Evans, P. D., Gilbert, S. L., Mekel-Bobrov, N., Vallender, E. J., Anderson, J. R., Vaez-Azizi, L. M., et al. (2005). Microcephalin, a gene regulating brain size, continues to evolve adaptively in humans. Science, 309, 1717–1720.PubMedCrossRefGoogle Scholar
  25. Evans, P. D., Anderson, J. R., Vallender, E. J., Choi, S. S., & Lahn, B. T. (2004a). Reconstructing the evolutionary history of microcephalin, a gene controlling human brain size. Human Molecular Genetics, 13, 1139–1145.PubMedCrossRefGoogle Scholar
  26. Evans, P. D., Anderson, J. R., Vallender, E. J., Gilbert, S. L., Malcom, C. M., Dorus, S., et al. (2004b). Adaptive evolution of ASPM, a major determinant of cerebral cortical size in humans. Human Molecular Genetics, 13, 489–494.PubMedCrossRefGoogle Scholar
  27. Falk, D., Hildebolt, C., Smith, K., Morwood, M. J., Sutikna, T., Jatmiko, et al. (2009). LB1’s virtual endocast, microcephaly, and hominin brain evolution. Journal of Human Evolution, 57, 597–607.PubMedCrossRefGoogle Scholar
  28. Falk, D., Hildebolt, C., Smith, K., Morwood, M. J., Sutikna, T., Brown, P., et al. (2005). The brain of LB1, Homo floresiensis. Science, 308, 242–245.PubMedCrossRefGoogle Scholar
  29. Garber, P. A., & Leigh, S. R. (1997). Ontogenetic variation in small-bodied new world primates: Implications for patterns of reproduction and infant care. Folia Primatologica, 68, 1–22.CrossRefGoogle Scholar
  30. Giedd, J. N., Snell, J. W., Lange, N., Rajapakse, J. C., Casey, B. J., Kozuch, P. L., et al. (1996). Quantitative magnetic resonance imaging of human brain development: Ages 4–18. Cerebral Cortex, 6, 551–560.PubMedCrossRefGoogle Scholar
  31. Gilbert, S. L., Dobyns, W. B., & Lahn, B. T. (2005). Genetic links between brain development and brain evolution. Nature Reviews Genetics, 6, 581–590.PubMedCrossRefGoogle Scholar
  32. Gould, S. J. (1981). The Mismeasure of Man. New York: Alfred R. Knopf.Google Scholar
  33. Gould, S. J., & Eldredge, N. (1977). Punctuated equilibria: The tempo and mode of evolution reconsidered. Paleobiology, 3, 115–151.Google Scholar
  34. Greenough, W. T., Black, J. E., & Wallace, C. S. (1987). Experience and brain development. Child Development, 58, 539–559.PubMedCrossRefGoogle Scholar
  35. Guatelli-Steinberg, D., Reid, D. J., & Bishop, T. A. (2007). Did the lateral enamel of Neandertal anterior teeth grow differently from that of modern humans? Journal of Human Evolution, 52, 72–84.PubMedCrossRefGoogle Scholar
  36. Gunz, P., Mitteroecker, P., Neubauer, S., Weber, G. W., & Bookstein, F. L. (2009). Principles for the virtual reconstruction of hominin crania. Journal of Human Evolution, 57, 48–62.PubMedCrossRefGoogle Scholar
  37. Gunz, P., Neubauer, S., Maureille, B., & Hublin, J.-J. (2010). Brain development after birth differs between Neanderthals and modern humans. Current Biology, 20(21), R921–R922.PubMedCrossRefGoogle Scholar
  38. Gunz, P., Neubauer, S., Golovanova, L., Doronichev, V., Maureille, B., & Hublin, J.-J. (2012). A uniquely human pattern of endocranial development. Insights from a new cranial reconstruction of the Neandertal newborn from Mesmaiskaya. Journal of Human Evolution. http://dx.doi.org/10.1016/j.jhevol.2011.11.013.
  39. Harvey, P. H., Martin, R. D., & Clutton-Brock, T. H. (1987). Life histories in a comparative perspective. In B. B. Smuts, D. L. Cheney, R. M. Seyfarth, R. W. Wrangham, & T. T. Struhsaker (Eds.), Primate Societies (pp. 181–196). Chicago: University of Chicago Press.Google Scholar
  40. Hawkes, K. (2004). Human longevity: The grandmother effect. Nature, 428, 128–129.PubMedCrossRefGoogle Scholar
  41. Hawkes, K. (2003). Grandmothers and the evolution of human longevity. American Journal of Human Biology, 15, 380–400.PubMedCrossRefGoogle Scholar
  42. Hawkes, K., O’Connell, J. F., Jones, N. G., Alvarez, H., & Charnov, E. L. (1998). Grandmothering, menopause, and the evolution of human life histories. Proceedings of the National Academy of Sciences of the United States of America, 95, 1336–1339.PubMedCrossRefGoogle Scholar
  43. Herndon, J. G., Tigges, J., Anderson, D. C., Klumpp, S. A, & McClure, H. M. (1999). Brain weight throughout the life span of the chimpanzee. Journal of Comparative Neurology, 409, 567–572.PubMedCrossRefGoogle Scholar
  44. Hill, K., & Hurtado, A. M. (1996). Ache Life History: The Ecology and Demography of a Foraging People. New York: Walter de Gruyter, Inc.Google Scholar
  45. Hofman, M. A. (1993). Encephalization and the evolution of longevity in mammals. Journal of Evolutionary Biology, 6, 209–627.CrossRefGoogle Scholar
  46. Holliday, M. A., Potter, D., Jarrah, A., & Bearg, S. (1967). The relation of metabolic rate to body weight and organ size. Pediatric Research, 1, 185–195.PubMedCrossRefGoogle Scholar
  47. Hublin, J.-J., & Coqueugniot, H. (2006). Absolute or proportional brain size: That is the question. A reply to comments. Journal of Human Evolution, 50, 109–113.CrossRefGoogle Scholar
  48. Humphrey, L. T. (2010). Weaning behaviour in human evolution. Seminars in Cell & Developmental Biology, 21, 453–461.CrossRefGoogle Scholar
  49. Isler, K., & van Schaik, C. P. (2009). The expensive brain: A framework for explaining evolutionary changes in brain size. Journal of Human Evolution, 57, 392–400.PubMedCrossRefGoogle Scholar
  50. Isler, K., Kirk, C. E., Miller, J. M., Albrecht, G. A., Gelvin, B. R., & Martin, R. D. (2008). Endocranial volumes of primate species: Scaling analyses using a comprehensive and reliable data set. Journal of Human Evolution, 55, 967–978.PubMedCrossRefGoogle Scholar
  51. Jolicoeur, P., Baron, G., & Cabana, T. (1988). Cross-sectional growth and decline of human stature and brain weight in 19th-century Germany. Growth, Development, and Aging, 52, 201–206.PubMedGoogle Scholar
  52. Kappelman, J., & Nachman, B. A. (2010). Temperate migrations: Climatically-mediated movements north (and south again?). American Journal of Physical Anthropology, 141, 139.Google Scholar
  53. Kramer, A. F., Bherer, L., Colcombe, S. J., Dong, W., & Greenough, W. T. (2004). Environmental influences on cognitive and brain plasticity during aging. The Journals of Gerontology: Series A: Biological Sciences and Medical Sciences, 59, M940–M957.CrossRefGoogle Scholar
  54. Leigh, S. R. (1992a). Cranial capacity evolution in Homo erectus and early Homo sapiens. American Journal of Physical Anthropology, 87, 1–13.PubMedCrossRefGoogle Scholar
  55. Leigh, S. R. (1992b). Patterns of variation in the ontogeny of primate body size dimorphism. Journal of Human Evolution, 23(1), 27–50.CrossRefGoogle Scholar
  56. Leigh, S. R. (1994). Ontogenetic correlates of diet in anthropoid primates. American Journal of Physical Anthropology, 94, 499–522.PubMedCrossRefGoogle Scholar
  57. Leigh, S. R. (2004). Brain growth, life history, and cognition in primate and human evolution. American Journal of Primatology, 62, 139–164.PubMedCrossRefGoogle Scholar
  58. Leigh, S. R. (2006a). Cranial ontogeny of Papio baboons (Papio hamadryas). American Journal of Physical Anthropology, 130, 71–84.PubMedCrossRefGoogle Scholar
  59. Leigh, S. R. (2006b). Brain ontogeny and life history in Homo erectus. Journal of Human Evolution, 50, 104–108.PubMedCrossRefGoogle Scholar
  60. Leigh, S. R., & Bernstein, R. M. (2006). Ontogeny, life history, and maternal investment in baboons. In L. Swedell & S. R. Leigh (Eds.), Reproduction and fitness in baboons: Behavioral, ecological, and life history perspectives (pp. 225–256). New York: Springer.CrossRefGoogle Scholar
  61. Leonard, W. R., Robertson, M. L., Snodgrass, J. J., & Kuzawa, C. W. (2003). Metabolic correlates of hominid brain evolution. Comparative Biochemistry and Physiology: Part A, Molecular & Integrative Physiology, 136, 5–15.CrossRefGoogle Scholar
  62. Leonard, W. R., & Robertson, M. L. (1997). Comparative primate energetics and hominid evolution. American Journal of Physical Anthropology, 102, 265–281.PubMedCrossRefGoogle Scholar
  63. Leigh, S. R., & Shea, B. T. (1996). Ontogeny of body size variation in apes. American Journal of Physical Anthropology, 99, 43–65.PubMedCrossRefGoogle Scholar
  64. Marchand, F. (1902). Ueber Das Hirngewicht Des Menschen. Leipzig: B.G. Teubner.Google Scholar
  65. Markham, J. A., & Greenough, W. T. (2004). Experience-driven brain plasticity: Beyond the synapse. Neuron Glia Biology, 1, 351–363.PubMedCrossRefGoogle Scholar
  66. Martin, R. D. (1981). Relative brain size and basal metabolic rate in terrestrial vertebrates. Nature, 293, 57–60.PubMedCrossRefGoogle Scholar
  67. Martin, R. D. (1983). Human brain evolution in an ecological context (James Arthur Lecture on the Evolution of the Human Brain, no. 52, 1982). New York: American Museum of Natural History.Google Scholar
  68. Martin, R. D. (1989). Evolution of the brain in early homininds. Ossa, 14, 49–62.Google Scholar
  69. McNulty, K. P., Frost, S. R., & Strait, D. S. (2006). Examining affinities of the Taung child by developmental simulation. Journal of Human Evolution, 51, 274–296.PubMedCrossRefGoogle Scholar
  70. Mekel-Bobrov, N., Posthuma, D., Gilbert, S. L., Lind, P., Gosso, M. F., Luciano, M., et al. (2007). The ongoing adaptive evolution of ASPM and microcephalin is not explained by increased intelligence. Human Molecular Genetics, 16, 600–608.PubMedCrossRefGoogle Scholar
  71. Mekel-Bobrov, N., Gilbert, S. L., Evans, P. D., Vallender, E. J., Anderson, J. R., Hudson, R. R., et al. (2005). Ongoing adaptive evolution of ASPM, a brain size determinant in homo sapiens. Science, 309, 1720–1722.PubMedCrossRefGoogle Scholar
  72. Montgomery, S. H., Capellini, I., Barton, R. A., & Mundy, N. I. (2010). Reconstructing the ups and downs of primate brain evolution: Implications for adaptive hypotheses and Homo floresiensis. BMC Biology, 8, 9.PubMedCrossRefGoogle Scholar
  73. Neubauer, S., & Hublin, J.-J. (2011). The evolution of human brain development. Evolutionary Biology. doi 10.1007/s11692-011-9156-1.
  74. Neubauer, S., Gunz, P., & Hublin, J.-J. (2010). Endocranial shape changes during growth in chimpanzees and humans: A morphometric analysis of unique and shared aspects. Journal of Human Evolution, 59, 555–556.PubMedCrossRefGoogle Scholar
  75. Pilbeam, D., & Gould, S. J. (1974). Size and scaling in human evolution. Science, 186, 892–901.PubMedCrossRefGoogle Scholar
  76. Ponce de Leon, M. S., Golovanova, L., Doronichev, V., Romanova, G., Akazawa, T., Kondo, O., et al. (2008). Neanderthal brain size at birth provides insights into the evolution of human life history. Proceedings of the National Academy of Sciences of the United States of America, 105, 13764–13768.PubMedCrossRefGoogle Scholar
  77. Rightmire, G. P. (1981). Patterns in the evolution of Homo erectus. Paleobiology, 7, 241–246.Google Scholar
  78. Rightmire, G. P. (2004). Brain size and encephalization in early to mid-pleistocene Homo. American Journal of Physical Anthropology, 124, 109–123.PubMedCrossRefGoogle Scholar
  79. Rosenberg, K. R., & Trevathan, W. R. (2001). The evolution of human birth. Scientific American, 285, 72–77.PubMedCrossRefGoogle Scholar
  80. Ruff, C. (2010). Body size and body shape in early hominins—implications of the Gona pelvis. Journal of Human Evolution, 58, 166–178.PubMedCrossRefGoogle Scholar
  81. Sacher, G. A. (1959). Relationship of lifespan to brain weight and body weight in mammals. In G. E. W. Wolstenholme & M. O’Connor (Eds.), C.I.B.A. foundation Colloquia on aging volume 5: The lifespan of animals (pp. 115–133). London: Churchill.Google Scholar
  82. Sacher, G. A., & Stafffeldt, E. F. (1974). Relation of gestation time to brain weight for placental mammals. American Naturalist, 108, 593–615.CrossRefGoogle Scholar
  83. Sakai, T., Mikami, A., Matsui, M., Suzuki, J., Hamada, Y., Tanaka, M., et al. (2011). Differential prefrontal white matter development in chimpanzees and humans. Current Biology, 21, 1397–1402.PubMedCrossRefGoogle Scholar
  84. Schwartz, J. H., Holloway, R. L., Broadfield, D. C., Tattersall, I., & Yuan, M. S. (2004). The Human Fossil Record Volume 3, Brain Endocasts - the Paleoneurological Evidence. Hoboken, NJ: John Wiley and Sons.Google Scholar
  85. Shattuck, M. R., & Williams, S. A. (2010). Arboreality has allowed for the evolution of increased longevity in mammals. Proceedings of the National Academy of Sciences of the United States of America, 107, 4635–4639.PubMedCrossRefGoogle Scholar
  86. Simpson, S. W., Quade, J., Levin, N. E., Butler, R., Dupont-Nivet, G., Everett, M., et al. (2008). A female Homo erectus pelvis from Gona, Ethiopia. Science, 322, 1089–1092.PubMedCrossRefGoogle Scholar
  87. Smith, T. M., Toussaint, M., Reid, D. J., Olejniczak, A. J., & Hublin, J. J. (2007). Rapid dental development in a middle paleolithic Belgian Neanderthal. Proceedings of the National Academy of Sciences of the United States of America, 104, 20220–20225.PubMedCrossRefGoogle Scholar
  88. Swisher, C. C., 3rd, Rink, W. J., Antón, S. C., Schwarcz, H. P., Curtis, G. H., Suprijo, A., et al. (1996). Latest Homoerectus of Java: Potential contemporaneity with Homo sapiens in Southeast Asia. Science, 274, 1870–1874.PubMedCrossRefGoogle Scholar
  89. Tobias, P. V. (1970). Brain-size, grey matter and race–fact or fiction? American Journal of Physical Anthropology, 32, 3–25.PubMedCrossRefGoogle Scholar
  90. Trevathan, W. R. (1996). The evolution of bipedalism and assisted birth. Medical Anthropology Quarterly, 10, 287–290.PubMedCrossRefGoogle Scholar
  91. Vallender, E. J., & Lahn, B. T. (2006). A primate-specific acceleration in the evolution of the caspase-dependent apoptosis pathway. Human Molecular Genetics, 15, 3034–3040.PubMedCrossRefGoogle Scholar
  92. Vrba, E. S. (1998). Multiphasic growth models and the prolonged growth exemplified by human brain evolution. Journal of Theoretical Biology, 190, 227–239.PubMedCrossRefGoogle Scholar
  93. Walker, A., & Ruff, C. B. (1993). Reconstruction of the pelvis. In A. Walker & R. Leakey (Eds.), The Nariokotome Homo erectus Skeleton (pp. 221–233). Cambridge: Harvard Univ. Press.Google Scholar
  94. Weaver, T. D., & Hublin, J. J. (2009). Neandertal birth canal shape and the evolution of human childbirth. Proceedings of the National Academy of Sciences of the United States of America, 106, 8151–8156.PubMedCrossRefGoogle Scholar
  95. Weidenreich, F. (1941). The brain and its rôle in the phylogenetic transformation of the human skull. Transactions of the American Philosophical Society, 31, 320–442.CrossRefGoogle Scholar
  96. White, T. D., Asfaw, B., DeGusta, D., Gilbert, H., Richards, G. D., Suwa, G., et al. (2003). Pleistocene Homo sapiens from Middle Awash, Ethiopia. Nature, 423, 724–747.CrossRefGoogle Scholar
  97. Williams, G. C. (1957). Pleiotropy, natural selection, and the evolution of senescence. Evolution, 11, 398–4111.CrossRefGoogle Scholar
  98. Wolpoff, M. H. (1986). Stasis in the interpretation of evolution in Homo erectus: A reply to Rightmire. Paleobiology, 12, 325–328.Google Scholar
  99. Wood, J., Milner, G. R., Harpending, H. C., & Weiss, K. M. (1992). The osteological paradox: Problems of inferring prehistoric health from skeletal samples. Current Anthropology, 33, 343–370.CrossRefGoogle Scholar

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© Springer Science+Business Media, LLC 2012

Authors and Affiliations

  1. 1.Department of Anthropology, Institute for Genomic Biology, College of MedicineUniversity of IllinoisUrbanaUSA

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