Restricted access
Review article
Review articleHominin cognitive evolution: identifying patterns and processes in the fossil and archaeological record
Published:05 August 2012https://doi.org/10.1098/rstb.2012.0115
Abstract
As only limited insight into behaviour is available from the archaeological record, much of our understanding of historical changes in human cognition is restricted to identifying changes in brain size and architecture. Using both absolute and residual brain size estimates, we show that hominin brain evolution was likely to be the result of a mix of processes; punctuated changes at approximately 100 kya, 1 Mya and 1.8 Mya are supplemented by gradual within-lineage changes in Homo erectus and Homo sapiens sensu lato. While brain size increase in Homo in Africa is a gradual process, migration of hominins into Eurasia is associated with step changes at approximately 400 kya and approximately 100 kya. We then demonstrate that periods of rapid change in hominin brain size are not temporally associated with changes in environmental unpredictability or with long-term palaeoclimate trends. Thus, we argue that commonly used global sea level or Indian Ocean dust palaeoclimate records provide little evidence for either the variability selection or aridity hypotheses explaining changes in hominin brain size. Brain size change at approximately 100 kya is coincident with demographic change and the appearance of fully modern language. However, gaps remain in our understanding of the external pressures driving encephalization, which will only be filled by novel applications of the fossil, palaeoclimatic and archaeological records.
Footnotes
References
- 1
Robson S. L.& Wood B. . 2008Hominin life history: reconstruction and evolution. J. Anat. 212, 394–425. doi:10.1111/j.1469-7580.2008.00867.x (doi:10.1111/j.1469-7580.2008.00867.x). Crossref, PubMed, ISI, Google Scholar - 2
Leonard W. R.& Robertson M. L. . 1992Nutritional requirements and human evolution: a bioenergetics model. Am. J. Hum. Biol. 4, 179–195. doi:10.1002/ajhb.1310040204 (doi:10.1002/ajhb.1310040204). Crossref, PubMed, ISI, Google Scholar - 3
Aiello L. C.& Wells J. C. K. . 2002Energetics and the evolution of the genus Homo. Annu. Rev. Anthropol. 31, 323–338. doi:10.1146/annurev.anthro.31.040402.085403 (doi:10.1146/annurev.anthro.31.040402.085403). Crossref, ISI, Google Scholar - 4
Steudel-Numbers K. L. . 2006Energetics in Homo erectus and other early hominins: the consequences of increased lower-limb length. J. Hum. Evol. 51, 445–453. doi:10.1016/j.jhevol.2006.05.001 (doi:10.1016/j.jhevol.2006.05.001). Crossref, PubMed, ISI, Google Scholar - 5
- 6
Vrba E. S., Denton G. H., Partridge T. C.& Burckle L. H. E. . 1995Paleoclimate and evolution, with emphasis on human origins.New Haven, CT: Yale University Press. Google Scholar - 7
Potts R. . 1998Variability selection in hominid evolution. Evol. Anthropol. Issues News Rev. 7, 81–96. doi:10.1002/(SICI)1520-6505(1998)7:3<81::AID-EVAN3>3.0.CO;2-A (doi:10.1002/(SICI)1520-6505(1998)7:3<81::AID-EVAN3>3.0.CO;2-A). Crossref, ISI, Google Scholar - 8
Potts R. . 1998Environmental hypotheses of hominin evolution. Am. J. Phys. Anthropol. 41, 93–136. doi:10.1002/(SICI)1096-8644(1998)107:27+<93::AID-AJPA5>3.0.CO;2-X (doi:10.1002/(SICI)1096-8644(1998)107:27+<93::AID-AJPA5>3.0.CO;2-X). Crossref, Google Scholar - 9
Trauth M. H., 2010Human evolution in a variable environment: the amplifier lakes of Eastern Africa. Quat. Sci. Rev. 29, 2981–2988. doi:10.1016/j.quascirev.2010.07.007 (doi:10.1016/j.quascirev.2010.07.007). Crossref, ISI, Google Scholar - 10
Ungar P. S., Grine F. E.& Teaford M. F. . 2006Diet in early Homo: a review of the evidence and a new model of adaptive versatility. Annu. Rev. Anthropol. 35, 209–228. doi:10.1146/annurev.anthro.35.081705.123153 (doi:10.1146/annurev.anthro.35.081705.123153). Crossref, ISI, Google Scholar - 11
Kaplan H., Hill K., Lancaster J.& Hurtado A. M. . 2000A theory of human life history evolution: diet, intelligence, and longevity. Evol. Anthropol. Issues News Rev. 9, 156–185. doi:10.1002/1520-6505(2000)9:4<156::AID-EVAN5>3.0.CO;2-7 (doi:10.1002/1520-6505(2000)9:4<156::AID-EVAN5>3.0.CO;2-7). Crossref, ISI, Google Scholar - 12
Gamble C., Gowlett J.& Dunbar R. . 2011The social brain and the shape of the Palaeolithic. Camb. Archaeol. J. 21, 115–136. doi:10.1017/S0959774311000072 (doi:10.1017/S0959774311000072). Crossref, ISI, Google Scholar - 13
Ash J.& Gallup G. . 2007Paleoclimatic variation and brain expansion during human evolution. Hum. Nat. 18, 109–124. doi:10.1007/s12110-007-9015-z (doi:10.1007/s12110-007-9015-z). Crossref, PubMed, ISI, Google Scholar - 14
Bailey D. H.& Geary D. H. . 2009Hominid brain evolution: testing climatic, ecological, and social competition models. Hum. Nat. 20, 67–79. doi:10.1007/s12110-008-9054-0 (doi:10.1007/s12110-008-9054-0). Crossref, ISI, Google Scholar - 15
Cowlishaw G. . 1997Trade-offs between foraging and predation risk determine habitat use in a desert baboon population. Anim. Behav. 53, 667–686. doi:10.1006/anbe.1996.0298 (doi:10.1006/anbe.1996.0298). Crossref, ISI, Google Scholar - 16
Hill R. A.& Lee P. C. . 1998Predation risk as an influence on group size in cercopithecoid primates: implications for social structure. J. Zool. 245, 447–456. doi:10.1111/j.1469-7998.1998.tb00119.x (doi:10.1111/j.1469-7998.1998.tb00119.x). Crossref, ISI, Google Scholar - 17
Pickering T. R., Clarke R. J.& Moggi-Cecchi J. . 2004Role of carnivores in the accumulation of the Sterkfontein Member 4 hominid assemblage: a taphonomic reassessment of the complete hominid fossil sample (1936–1999). Am. J. Phys. Anthropol. 125, 1–15. doi:10.1002/ajpa.10278 (doi:10.1002/ajpa.10278). Crossref, PubMed, ISI, Google Scholar - 18
Gilbert C. C., McGraw W. S.& Delson E. . 2009Brief communication: Plio-Pleistocene eagle predation on fossil cercopithecids from the Humpata Plateau, southern Angola. Am. J. Phys. Anthropol. 139, 421–429. doi:10.1002/ajpa.21004 (doi:10.1002/ajpa.21004). Crossref, PubMed, ISI, Google Scholar - 19
Wood B.& Collard M. . 1999The human genus. Science 284, 65–71. doi:10.1126/science.284.5411.65 (doi:10.1126/science.284.5411.65). Crossref, PubMed, ISI, Google Scholar - 20
Reed K. E. . 1997Early hominid evolution and ecological change through the African Plio-Pleistocene. J. Hum. Evol. 32, 289–322. doi:10.1006/jhev.1996.0106 (doi:10.1006/jhev.1996.0106). Crossref, PubMed, ISI, Google Scholar - 21
Shultz S.& Dunbar R. I. M. . 2006Chimpanzee and felid diet composition is influenced by prey brain size. Biol. Lett. 2, 505–508. doi:10.1098/rsbl.2006.0519 (doi:10.1098/rsbl.2006.0519). Link, ISI, Google Scholar - 22
Shultz S.& Finlayson L. V. . 2010Large body and small brain and group sizes are associated with predator preferences for mammalian prey. Behav. Ecol. 21, 1073–1079. doi:10.1093/beheco/arq108 (doi:10.1093/beheco/arq108). Crossref, ISI, Google Scholar - 23
van Schaik C. P. . 1983Why Are diurnal primates living in groups?Behaviour 87, 120–144. doi:10.1163/156853983X00147 (doi:10.1163/156853983X00147). Crossref, ISI, Google Scholar - 24
Shultz S., Noe R., McGraw W. S.& Dunbar R. I. . 2004A community-level evaluation of the impact of prey behavioural and ecological characteristics on predator diet composition. Proc. R. Soc. B 271, 725–32. doi:10.1098/rspb.2003.2626 (doi:10.1098/rspb.2003.2626). Link, ISI, Google Scholar - 25
Dunbar R. I. M.& Shultz S. . 2007Evolution in the social brain. Science 317, 1344–1347. doi:10.1126/science.1145463 (doi:10.1126/science.1145463). Crossref, PubMed, ISI, Google Scholar - 26
Jolly A. . 1966Lemur social behavior and primate intelligence. Science 153, 501–506. doi:10.1126/science.153.3735.501 (doi:10.1126/science.153.3735.501). Crossref, PubMed, ISI, Google Scholar - 27
Humphrey N. K. . 1976The social function of intellect. Growing points in ethology (eds, Bateson P. P. G.& Hinde R. A. ), pp. 303–317. Cambridge, UK: Cambridge University Press. Google Scholar - 28
Dunbar R. I. M. . 2011Evolutionary basis of the social brain. The Oxford handbook of social neuroscience (eds, Decety J.& Cacioppo J. T. ), pp. 28–38. Oxford, UK: Oxford University Press. Google Scholar - 29
Shultz S.& Dunbar R. I. M. . 2012Social cognition and cortical function: an evolutionary perspective. Action, perception and the brain: adaptation and cephalic expression (ed.& Schulkin J. ). Basingstoke, UK: Palgrave Macmillian. Google Scholar - 30
Barton R. A. . 1996Neocortex size and behavioural ecology in primates. Proc. R. Soc. B 263, 173–177. doi:10.1098/rspb.1996.0028 (doi:10.1098/rspb.1996.0028). Link, ISI, Google Scholar - 31
Dunbar R. I. M. . 1998The social brain hypothesis. Evol. Anthropol. Issues News Rev. 6, 178–190. doi:10.1002/(SICI)1520-6505(1998)6:5<178::AID-EVAN5>3.0.CO;2-8 (doi:10.1002/(SICI)1520-6505(1998)6:5<178::AID-EVAN5>3.0.CO;2-8). Crossref, ISI, Google Scholar - 32
Aiello L. C.& Dunbar R. I. M. . 1993Neocortex size, group-size, and the evolution of language. Curr. Anthropol. 34, 184–193. doi:10.1086/204160 (doi:10.1086/204160). Crossref, ISI, Google Scholar - 33
Dunbar R. I. M. . 2009The social brain hypothesis and its implications for social evolution. Ann. Hum. Biol. 36, 562–572. doi:10.1080/03014460902960289 (doi:10.1080/03014460902960289). Crossref, PubMed, ISI, Google Scholar - 34
- 35
Deacon T. W. . 1997The symbolic species: the co-evolution of language and the brain. New York, NY: W. W. Norton and Co. Google Scholar - 36
Powell J. L., Lewis P. A., Dunbar R. I. M., García-Fiñana M.& Roberts N. . 2010Orbital prefrontal cortex volume correlates with social cognitive competence. Neuropsychologia 48, 3554–3562. doi:10.1016/j.neuropsychologia.2010.08.004 (doi:10.1016/j.neuropsychologia.2010.08.004). Crossref, PubMed, ISI, Google Scholar - 37
Lewis P. A., Rezaie R., Brown R., Roberts N.& Dunbar R. I. M. . 2011Ventromedial prefrontal volume predicts understanding of others and social network size. NeuroImage 57, 1624–1629. doi:10.1016/j.neuroimage.2011.05.030 (doi:10.1016/j.neuroimage.2011.05.030). Crossref, PubMed, ISI, Google Scholar - 38
Bogin B. . 1997Evolutionary hypotheses for human childhood. Am. J. Phys. Anthropol. 104, 63–89. doi:10.1002/(SICI)1096-8644(1997)25+<63::AID-AJPA3>3.0.CO;2-8 (doi:10.1002/(SICI)1096-8644(1997)25+<63::AID-AJPA3>3.0.CO;2-8). Crossref, Google Scholar - 39
Dunbar R. I. M.& Shultz S. . 2007Understanding primate brain evolution. Phil. Trans. R. Soc. B 362, 649–658. doi:10.1098/rstb.2006.2001 (doi:10.1098/rstb.2006.2001). Link, ISI, Google Scholar - 40
Shultz S.& Dunbar R. I. M. . 2010Encephalization is not a universal macroevolutionary phenomenon in mammals but is associated with sociality. Proc. Natl Acad. Sci. USA 107, 21 582–21 586. doi:10.1073/pnas.1005246107 (doi:10.1073/pnas.1005246107). Crossref, ISI, Google Scholar - 41
Isler K.& van Schaik C. P. . 2009Why are there so few smart mammals (but so many smart birds)?Biol. Lett. 5, 125–129. doi:10.1098/rsbl.2008.0469 (doi:10.1098/rsbl.2008.0469). Link, ISI, Google Scholar - 42
Martin R. D. . 1981Relative brain size and basal metabolic rate in terrestrial vertebrates. Nature 293, 57–60. doi:10.1038/293057a0 (doi:10.1038/293057a0). Crossref, PubMed, ISI, Google Scholar - 43
Milton K. . 1999A hypothesis to explain the role of meat-eating in human evolution. Evol. Anthropol. Issues News Rev. 8, 11–21. doi:10.1002/(SICI)1520-6505(1999)8:1<11::AID-EVAN6>3.0.CO;2-M (doi:10.1002/(SICI)1520-6505(1999)8:1<11::AID-EVAN6>3.0.CO;2-M). Crossref, ISI, Google Scholar - 44
Leonard W. R.& Robertson M. L. . 1996On diet, energy metabolism, and brain size in human evolution. Curr. Anthropol. 37, 125–129. doi:10.1086/204476 (doi:10.1086/204476). Crossref, ISI, Google Scholar - 45
Wrangham R. W., Jones Holland J., Laden G., Pilbeam D.& Conklin-Brittain N. . 1999The raw and the stolen: cooking and the ecology of human origins. Curr. Anthropol. 40, 567–594. doi:10.1086/300083 (doi:10.1086/300083). Crossref, PubMed, ISI, Google Scholar - 46
Foley R.& Gamble C. . 2009The ecology of social transitions in human evolution. Phil. Trans. R. Soc. B 364, 3267–3279. doi:10.1098/rstb.2009.0136 (doi:10.1098/rstb.2009.0136). Link, ISI, Google Scholar - 47
Gould S. J.& Eldredge N. . 1977Punctuated equilibria: the tempo and mode of evolution reconsidered. Paleobiology 3, 115–151. Crossref, Google Scholar - 48
Cronin J. E., Boaz N. T., Stringer C. B.& Rak Y. . 1981Tempo and mode in hominid evolution. Nature 292, 113–122. doi:10.1038/292113a0 (doi:10.1038/292113a0). Crossref, PubMed, ISI, Google Scholar - 49
Lee S.-H.& Wolpoff M. H. . 2003The pattern of evolution in Pleistocene human brain size. Paleobiology 29, 186–196. doi:10.1666/0094-8373(2003)029<0186:TPOEIP>2.0.CO;2 (doi:10.1666/0094-8373(2003)029<0186:TPOEIP>2.0.CO;2). Crossref, ISI, Google Scholar - 50
Rightmire G. P. . 1981Patterns in the evolution of Homo erectus. Paleobiology 7, 241–246. Crossref, ISI, Google Scholar - 51
Ruff C. B., Trinkaus E.& Holliday T. W. . 1997Body mass and encephalization in Pleistocene Homo. Nature 387, 173–176. doi:10.1038/387173a0 (doi:10.1038/387173a0). Crossref, PubMed, ISI, Google Scholar - 52
Rightmire G. P. . 2004Brain size and encephalization in early to Mid-Pleistocene Homo. Am. J. Phys. Anthropol. 124, 109–123. doi:10.1002/ajpa.10346 (doi:10.1002/ajpa.10346). Crossref, PubMed, ISI, Google Scholar - 53
Beals K. L., Smith C. L.& Dodd S. M. . 1984Brain size, cranial morphology, climate, and time machines. Curr. Anthropol. 25, 301–330. doi:10.1086/203138 (doi:10.1086/203138). Crossref, ISI, Google Scholar - 54
Leigh S. R. . 1992Cranial capacity evolution in Homo erectus and early Homo sapiens. Am. J. Phys. Anthropol. 87, 1–13. doi:10.1002/ajpa.1330870102 (doi:10.1002/ajpa.1330870102). Crossref, PubMed, ISI, Google Scholar - 55
Lestrel P. E.& Read D. W. . 1973Hominid cranial capacity versus time: a regression approach. J. Hum. Evol. 2, 405–411. doi:10.1016/0047-2484(73)90020-1 (doi:10.1016/0047-2484(73)90020-1). Crossref, ISI, Google Scholar - 56
Lestrel P. E. . 1976Hominid brain size versus time: revised regression estimates. J. Hum. Evol. 5, 207–212. doi:10.1016/0047-2484(76)90022-1 (doi:10.1016/0047-2484(76)90022-1). Crossref, ISI, Google Scholar - 57
Godfrey L.& Jacobs K. H. . 1981Gradual, autocatalytic and punctuational models of hominid brain evolution: a cautionary tale. J. Hum. Evol. 10, 255–272. doi:10.1016/S0047-2484(81)80063-2 (doi:10.1016/S0047-2484(81)80063-2). Crossref, ISI, Google Scholar - 58
Rightmire G. P. . 1986Statis in Homo erectus defended. Paleobiology 12, 324–325. Crossref, ISI, Google Scholar - 59
Green R. E., 2010A draft sequence of the Neandertal genome. Science 328, 710–722. doi:10.1126/science.1188021 (doi:10.1126/science.1188021). Crossref, PubMed, ISI, Google Scholar - 60
Krause J., Fu Q., Good J. M., Viola B., Shunkov M. V., Derevianko A. P.& Paabo S. . 2010The complete mitochondrial DNA genome of an unknown hominin from southern Siberia. Nature 464, 894–897. doi:10.1038/nature08976 (doi:10.1038/nature08976). Crossref, PubMed, ISI, Google Scholar - 61
Strait D. S.& Grine F. E. . 2004Inferring hominoid and early hominid phylogeny using craniodental characters: the role of fossil taxa. J. Hum. Evol. 47, 399–452. doi:10.1016/j.jhevol.2004.08.008 (doi:10.1016/j.jhevol.2004.08.008). Crossref, PubMed, ISI, Google Scholar - 62
Shultz S.& Dunbar R. I. M. . 2010Species differences in executive function correlate with hippocampus volume and neocortex ratio across nonhuman primates. J. Comput. Psychol. 124, 252–260. doi:10.1037/a0018894 (doi:10.1037/a0018894). Crossref, PubMed, ISI, Google Scholar - 63
Deaner R. O., Isler K., Burkart J.& van Schaik C. . 2007Overall brain size, and not encephalization quotient, best predicts cognitive ability across non-human primates. Brain Behav. Evol. 70, 115–124. doi:10.1159/000102973 (doi:10.1159/000102973). Crossref, PubMed, ISI, Google Scholar - 64
Wolpoff M. H. . 1984Evolution in Homo erectus: the question of statis. Paleobiology 10, 389–406. Crossref, ISI, Google Scholar - 65
McHenry H. M. . 1994Behavioral ecological implications of early hominid body size. J. Hum. Evol. 27, 77–87. doi:10.1006/jhev.1994.1036 (doi:10.1006/jhev.1994.1036). Crossref, ISI, Google Scholar - 66
Hublin J. J. . 2009The origin of Neandertals. Proc. Natl Acad. Sci. USA 106, 16 022–16 027. Crossref, ISI, Google Scholar - 67
Endicott P., Ho S. Y. W.& Stringer C. B. . 2010Using genetic evidence to evaluate four palaeoanthropological hypotheses for the timing of Neanderthal and modern human origins. J. Hum. Evol. 59, 87–95. doi:10.1016/j.jhevol.2010.04.005 (doi:10.1016/j.jhevol.2010.04.005). Crossref, PubMed, ISI, Google Scholar - 68
Pearce E.& Dunbar R. Latitudinal variation in light levels drives human visual system size. Biol. Lett. 8, 90–93. Link, ISI, Google Scholar - 69
Miller K. G., 2005The Phanerozoic record of global sea-level change. Science 310, 1293–1298. doi:10.1126/science.1116412 (doi:10.1126/science.1116412). Crossref, PubMed, ISI, Google Scholar - 70
deMenocal P. B. . 1995Plio-Pleistocene African climate. Science 270, 53–59. doi:10.1126/science.270.5233.53 (doi:10.1126/science.270.5233.53). Crossref, PubMed, ISI, Google Scholar - 71
Trauth H. H., Larrasoaña J. C.& Mudelsee M. . 2009Trends, rhythms and events in Plio-Pleistocene African climate. Quat. Sci. Rev. 28, 399–411. doi:10.1016/j.quascirev.2008.11.003 (doi:10.1016/j.quascirev.2008.11.003). Crossref, ISI, Google Scholar - 72
Bobe R.& Behrensmeyer A. K. . 2004The expansion of grassland ecosystems in Africa in relation to mammalian evolution and the origin of the genus Homo. Palaeogeogr. Palaeoclimatol. Palaeoecol. 207, 399–420. doi:10.1016/S0031-0182(04)00049-5 (doi:10.1016/S0031-0182(04)00049-5). Crossref, ISI, Google Scholar - 73
Donges J. F., Donner R. V., Trauth M. H., Marwan N., Schellnhuber H.-J.& Kurths J. . 2011Nonlinear detection of paleoclimate-variability transitions possibly related to human evolution. Proc. Natl Acad. Sci. USA 108, 20 422–20 427. doi:10.1073/pnas.1117052108 (doi:10.1073/pnas.1117052108). Crossref, ISI, Google Scholar - 74
Tobias P. V. . 2006Longevity, death and encephalisation among Plio-Pleistocene hominins. Int. Congress Ser. 1296, 1–15. doi:10.1016/j.ics.2006.03.034 (doi:10.1016/j.ics.2006.03.034). Crossref, Google Scholar - 75
Aiello L. C.& Key C. . 2002Energetic consequences of being a Homo erectus female. Am. J. Hum. Biol. 14, 551–565. doi:10.1002/ajhb.10069 (doi:10.1002/ajhb.10069). Crossref, PubMed, ISI, Google Scholar - 76
Buchsbaum D., Bridgers S., Weisberg D. S.& Gopnik A. . 2012The power of possibility: causal learning, counterfactual reasoning, and pretend play. Phil. Trans. R. Soc. B 367, 2202–2212. doi:10.1098/rstb.2012.0122 (doi:10.1098/rstb.2012.0122). Link, ISI, Google Scholar - 77
Joffe T. H. . 1997Social pressures have selected for an extended juvenile period in primates. J. Hum. Evol. 32, 593–605. doi:10.1006/jhev.1997.0140 (doi:10.1006/jhev.1997.0140). Crossref, PubMed, ISI, Google Scholar - 78
Smith T. M., Tafforeau P., Reid D. J., Grün R., Eggins S., Boutakiout M.& Hublin J.-J. . 2007Earliest evidence of modern human life history in North African early Homo sapiens. Proc. Natl Acad. Sci. USA 104, 6128–6133. doi:10.1073/pnas.0700747104 (doi:10.1073/pnas.0700747104). Crossref, PubMed, ISI, Google Scholar - 79
Brothers L. . 1990The social brain: a project for integrating primate behavior and neurophysiology in a new domain. Concepts Neurosci. 1, 27–51. Google Scholar - 80
Behrens T. E. J., Hunt L. T.& Rushworth M. F. S. . 2009The computation of social behavior. Science 324, 1160–1164. doi:10.1126/science.1169694 (doi:10.1126/science.1169694). Crossref, PubMed, ISI, Google Scholar - 81
Mithen S. . 1999Imitation and cultural change: a view from the Stone Age, with specific reference to the manufacture of handaxes. Mammalian social learning: comparative and ecological perspectives (eds, Box H. O.& Gibson K. R. ), pp. 389–400. Cambridge, UK: Cambridge University Press. Google Scholar - 82
Goren-Inbar N., Alperson N., Kislev M. E., Simchoni O., Melamed Y., Ben-Nun A.& Werker E. . 2004Evidence of hominin control of fire at Gesher Benot Ya`aqov, Israel. Science 304, 725–727. doi:10.1126/science.1095443 (doi:10.1126/science.1095443). Crossref, PubMed, ISI, Google Scholar - 83
d'Errico F.& Stringer C. B. . 2011Evolution, revolution or saltation scenario for the emergence of modern cultures?Phil. Trans. R. Soc. B 366, 1060–1069. doi:10.1098/rstb.2010.0340 (doi:10.1098/rstb.2010.0340). Link, ISI, Google Scholar - 84
Mellars P. . 2006Why did modern human populations disperse from Africa ca. 60,000 years ago? A new model. Proc. Natl Acad. Sci. USA 103, 9381–9386. doi:10.1073/pnas.0510792103 (doi:10.1073/pnas.0510792103). Crossref, PubMed, ISI, Google Scholar - 85
Powell A., Shennan S.& Thomas M. G. . 2009Late Pleistocene demography and the appearance of modern human behavior. Science 324, 1298–1301. doi:10.1126/science.1170165 (doi:10.1126/science.1170165). Crossref, PubMed, ISI, Google Scholar - 86
Klein R. G. . 1995Anatomy, behavior, and modern human origins. J. World Prehistory 9, 167–198. doi:10.1007/BF02221838 (doi:10.1007/BF02221838). Crossref, ISI, Google Scholar - 87
Klein R. G. . 2000Archeology and the evolution of human behavior. Evol. Anthropol. Issues News Rev. 9, 17–36. doi:10.1002/(SICI)1520-6505(2000)9:1<17::AID-EVAN3>3.0.CO;2-A (doi:10.1002/(SICI)1520-6505(2000)9:1<17::AID-EVAN3>3.0.CO;2-A). Crossref, ISI, Google Scholar - 88
Holloway R. L. . 1996Evolution of the human brain. Handbook of human symbolic evolution (eds, Lock A.& Peters C. R. ), pp. 74–116. Oxford, UK: Blackwell. Google Scholar - 89
Holloway R. L., Broadfield D. C.& Yuan M. S. . 2004Brain endocasts: the paleoneurological evidence. The Human Fossil Record. New York, NY: Wiley. Crossref, Google Scholar - 90
Lieberman P. . 2007The evolution of human speech: its anatomical and neural bases. Curr. Anthropol. 48, 39–66. doi:10.1086/509092 (doi:10.1086/509092). Crossref, ISI, Google Scholar - 91
Schwartz J. H.& Tattersall I. . 2010Fossil evidence for the origin of Homo sapiens. Am. J. Phys. Anthropol. 143, 94–121. doi:10.1002/ajpa.21443 (doi:10.1002/ajpa.21443). Crossref, PubMed, ISI, Google Scholar - 92
Dunbar R. I. M. . 2009Why only humans have language. The prehistory of language (eds, Botha R.& Knight C. ), pp. 12–35. Oxford, UK: Oxford University Press. Crossref, Google Scholar - 93
Sterelny K. . 2012Language, gesture, skill: the coevolutionary foundations of language.Phil. Trans. R. Soc. B 367, 2141–2151. doi:10.1098/rstb.2012.0116 (doi:10.1098/rstb.2012.0116). Link, ISI, Google Scholar - 94
Maclarnon A.& Hewitt G. . 2004Increased breathing control: another factor in the evolution of human language. Evol. Anthropol. Issues News Rev. 13, 181–197. doi:10.1002/evan.20032 (doi:10.1002/evan.20032). Crossref, ISI, Google Scholar - 95
Kay R. F., Cartmill M.& Balow M. . 1998The hypoglossal canal and the origin of human vocal behavior. Proc. Natl Acad. Sci. USA 95, 5417–5419. doi:10.1073/pnas.95.9.5417 (doi:10.1073/pnas.95.9.5417). Crossref, PubMed, ISI, Google Scholar - 96
- 97
- 98
Atkinson Q. D. . 2011Phonemic diversity supports a serial founder effect model of language expansion from Africa. Science 332, 346–349. doi:10.1126/science.1199295 (doi:10.1126/science.1199295). Crossref, PubMed, ISI, Google Scholar
