Abstract
Uniquely, with respect to Middle Pleistocene hominins, anatomically modern humans do not possess marked browridges, and have a more vertical forehead with mobile eyebrows that play a key role in social signalling and communication. The presence and variability of browridges in archaic Homo species and their absence in ourselves have led to debate concerning their morphogenesis and function, with two main hypotheses being put forward: that browridge morphology is the result of the spatial relationship between the orbits and the brain case; and that browridge morphology is significantly impacted by biting mechanics. Here, we virtually manipulate the browridge morphology of an archaic hominin (Kabwe 1), showing that it is much larger than the minimum required to fulfil spatial demands and that browridge size has little impact on mechanical performance during biting. As browridge morphology in this fossil is not driven by spatial and mechanical requirements alone, the role of the supraorbital region in social communication is a potentially significant factor. We propose that conversion of the large browridges of our immediate ancestors to a more vertical frontal bone in modern humans allowed highly mobile eyebrows to display subtle affiliative emotions.
This is a preview of subscription content, access via your institution
Access options
Access Nature and 54 other Nature Portfolio journals
Get Nature+, our best-value online-access subscription
$29.99 / 30 days
cancel any time
Subscribe to this journal
Receive 12 digital issues and online access to articles
$119.00 per year
only $9.92 per issue
Buy this article
- Purchase on SpringerLink
- Instant access to full article PDF
Prices may be subject to local taxes which are calculated during checkout
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1038%2Fs41559-018-0528-0/MediaObjects/41559_2018_528_Fig1_HTML.jpg)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1038%2Fs41559-018-0528-0/MediaObjects/41559_2018_528_Fig2_HTML.jpg)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1038%2Fs41559-018-0528-0/MediaObjects/41559_2018_528_Fig3_HTML.jpg)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1038%2Fs41559-018-0528-0/MediaObjects/41559_2018_528_Fig4_HTML.jpg)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1038%2Fs41559-018-0528-0/MediaObjects/41559_2018_528_Fig5_HTML.jpg)
Similar content being viewed by others
References
Moss, M. L. & Young, R. W. A functional approach to craniology. Am. J. Phys. Anthropol. 18, 281–292 (1960).
Enlow, D. H. & Hans, M. G. Essentials of Facial Growth (W. B. Saunders Company, Philadelphia, 1996).
Bastir, M. & Rosas, A. Cranial base topology and basic trends in the facial evolution of Homo. J. Hum. Evol. 91, 26–35 (2016).
Bastir, M. et al. Effects of brain and facial size on basicranial form in human and primate evolution. J. Hum. Evol. 58, 424–431 (2010).
Shea, B. T. On aspects of skull form in African apes and orangutans, with implications for hominoid evolution. Am. J. Phys. Anthropol. 68, 329–342 (1985).
Ravosa, M. J. Browridge development in Cercopithecidae—a test of 2 models. Am. J. Phys. Anthropol. 76, 535–555 (1988).
Freidline, S. E., Gunz, P., Harvati, K. & Hublin, J. J. Middle Pleistocene human facial morphology in an evolutionary and developmental context. J. Hum. Evol. 63, 723–740 (2012).
Lieberman, D. E., McBratney, B. M. & Krovitz, G. The evolution and development of cranial form in Homo sapiens. Proc. Natl Acad. Sci. USA 99, 1134–1139 (2002).
Stringer, C. The Origin of Our Species (Penguin, London, 2012).
Cieri, R. L., Churchill, S. E., Franciscus, R. G., Tan, J. & Hare, B. Craniofacial feminization, social tolerance, and the origins of behavioral modernity. Curr. Anthropol. 55, 419–443 (2014).
Hare, B. Survival of the friendliest: Homo sapiens evolved via selection for prosociality. Annu. Rev. Psychol. 68, 155–186 (2017).
Hare, B., Wobber, V. & Wrangham, R. The self-domestication hypothesis: evolution of bonobo psychology is due to selection against aggression. Anim. Behav. 83, 573–585 (2012).
Shea, B. T. The Pygmy Chimpanzee: Evolutionary Biology and Behavior (ed. Susman, R. L.) 89–130 (Springer, New York, 1984).
Coolidge, H. J. Pan paniscus. Pigmy chimpanzee from south of the Congo River. Am. J. Phys. Anthropol. 18, 1–59 (1933).
Clay, Z. & de Waal, F. B. M. Development of socio-emotional competence in bonobos. Proc. Natl Acad. Sci. USA 110, 18121–18126 (2013).
Kano, F., Hirata, S. & Call, J. Social attention in the two species of Pan: bonobos make more eye contact than chimpanzees. PLoS ONE 10, e0129684 (2015).
Zink, K. D. & Lieberman, D. E. Impact of meat and Lower Palaeolithic food processing techniques on chewing in humans. Nature 531, 500–503 (2016).
Zink, K. D., Lieberman, D. E. & Lucas, P. W. Food material properties and early hominin processing techniques. J. Hum. Evol. 77, 155–166 (2014).
Carlson, D. S. Temporal variation in prehistoric Nubian crania. Am. J. Phys. Anthropol. 45, 467–484 (1976).
Carlson, D. S. & Van Gerven, D. P. Masticatory function and post-pleistocene evolution in Nubia. Am. J. Phys. Anthropol. 46, 495–506 (1977).
Russell, M. D. The supraorbital torus—a most remarkable peculiarity. Curr. Anthropol. 26, 337–360 (1985).
Oyen, O. J., Rice, R. W. & Cannon, M. S. Browridge structure and function in extant primates and Neanderthals. Am. J. Phys. Anthropol. 51, 83–96 (1979).
Endo, B. Analysis of stresses around the orbit due to masseter and temporalis muscles respectively. J. Anthropol. Soc. Nippon 78, 251–266 (1970).
Hilloowala, R. A. & Trent, R. B. Supraorbital ridge and masticatory apparatus II: humans (Eskimos). Hum. Evol. 3, 351–356 (1988).
Ravosa, M. J., Noble, V. E., Hylander, W. L., Johnson, K. R. & Kowalski, E. M. Masticatory stress, orbital orientation and the evolution of the primate postorbital bar. J. Human. Evol. 38, 667–693 (2000).
Hylander, W. L., Picq, P. G. & Johnson, K. R. Masticatory-stress hypotheses and the supraorbital region of primates. Am. J. Phys. Anthropol. 86, 1–36 (1991).
Kupczik, K. et al. Assessing mechanical function of the zygomatic region in macaques: validation and sensitivity testing of finite element models. J. Anat. 210, 41–53 (2007).
Tappen, N. C. The vermiculate surface pattern of brow ridges in Neandertal and modern crania. Am. J. Phys. Anthropol. 49, 1–10 (1978).
Tappen, N. C. Structure of bone in the skulls of Neanderthal fossils. Am. J. Phys. Anthropol. 38, 93–97 (1973).
Verhaegen, M. The aquatic ape evolves: common misconceptions and unproven assumptions about the so-called aquatic ape hypothesis. Hum. Evol. 28, 237–266 (2013).
Clark, G. A. & Willermet, C. M. Conceptual Issues in Modern Human Origins Research (Evolutionary Foundations for Human Behavior) (Walter de Gruyter, New York, 1997).
Krantz, G. S. Cranial hair and brow ridges. Mankind 9, 109–111 (1973).
Witzel, U. in Continuity and Discontinuity in the Peopling of Europe: One Hundred Fifty Years of Neanderthal Study (eds Condemi, S. & Weniger, G.-C.) 203–211 (Springer, Dordrecht, 2011).
Godinho, R. M. & O’Higgins, P. The biomechanical significance of the frontal sinus in Kabwe 1 (Homo heidelbergensis). J. Hum. Evol. 114, 141–153 (2018).
Lieberman, D. in Development, Growth and Evolution—Implications for the Study of the Hominid Skeleton Vol. 20 (eds O’Higgins, P. & Cohn, M.) 85–122 (Academic Press, London, 2000).
Strait, D. S. et al. Masticatory biomechanics and its relevance to early hominid phylogeny: an examination of palatal thickness using finite-element analysis. J. Hum. Evol. 52, 585–599 (2007).
O’Higgins, P. et al. Virtual functional morphology: novel approaches to the study of craniofacial form and function. Evol. Biol. 39, 521–535 (2012).
O’Higgins, P. & Milne, N. Applying geometric morphometrics to compare changes in size and shape arising from finite elements analyses. Hystrix Ital. J. Mammal. 24, 126–132 (2013).
Godinho, R. M. & O’Higgins, P. in Human Remains—Another Dimension: the Application of 3D Imaging in Funerary Context (eds Thompson, T. & Errickson, D.) 135–147 (Elsevier, London, 2017).
Frost, H. M. Bone’s mechanostat: a 2003 update. Anat. Rec. A Discov. Mol. Cell. Evol. Biol. 275A, 1081–1101 (2003).
Hylander, W. & Johnson, K. R. in Reconstructing Behavior in the Primate Fossil Record (eds Plavcan, J. M., Kay, R. F., Jungers, W. L. & Schaik, C. P.) 43–72 (Kluwer Academic/Plenum Publishers, New York, 2002).
Setchell, J. M. & Dixson, A. F. Changes in the secondary sexual adornments of male mandrills (Mandrillus sphinx) are associated with gain and loss of alpha status. Horm. Behav. 39, 177–184 (2001).
Wickings, E. J. & Dixson, A. F. Testicular function, secondary sexual development, and social status in male mandrills (Mandrillus sphinx). Physiol. Behav. 52, 909–916 (1992).
Elton, S. & Morgan, B. Muzzle size, paranasal swelling size and body mass in Mandrillus leucophaeus. Primates 47, 151–157 (2006).
Buikstra, J. & Ubelaker, D. Standards for Data Collection from Human Skeletal Remains: Proceedings of a Seminar at the Field Museum of Natural History (Arkansas Archeological Survey, Fayetteville, 1994).
Todorov, A., Baron, S. G. & Oosterhof, N. N. Evaluating face trustworthiness: a model based approach. Soc. Cogn. Affect. Neurosci. 3, 119–127 (2008).
Xu, F. et al. Similarities and differences in Chinese and Caucasian adults’ use of facial cues for trustworthiness judgments. PLoS ONE 7, e34859 (2012).
Thornhill, R. & MØller, A. P. Developmental stability, disease and medicine. Biol. Rev. 72, 497–548 (1997).
Amorim, A., Umbelino, C. & Matos, V. in V Jornadas Portuguesas de Paleopatologia: a Saúde e a Doença no Passado (eds Lopes, C. et al.) 15 (Centro de Investigação em Antropologia e Saúde, Coimbra, 2016).
Parr, L. A., Waller, B. M., Vick, S. J. & Bard, K. A. Classifying chimpanzee facial expressions using muscle action. Emotion 7, 172–181 (2007).
Tomasello, M., Hare, B., Lehmann, H. & Call, J. Reliance on head versus eyes in the gaze following of great apes and human infants: the cooperative eye hypothesis. J. Hum. Evol. 52, 314–320 (2007).
Kret, M. E. Emotional expressions beyond facial muscle actions. A call for studying autonomic signals and their impact on social perception. Front. Psychol. 6, 711 (2015).
Grammer, K., Schiefenhovel, W., Schleidt, M., Lorenz, B. & Eibl-Eibesfeldt, I. Patterns on the face—the eyebrow flash in crosscultural comparison. Ethology 77, 279–299 (1988).
Eibl-Eibesfeldt, I. Human Ethology (Aldine de Gruyter, New York, 1989).
Bavelas, J. B., Black, A., Lemery, C. R. & Mullett, J. “I show how you feel”: motor mimicry as a communicative act. J. Pers. Soc. Psychol. 50, 322–329 (1986).
Romero, T., Castellanos, M. A. & de Waal, F. B. M. Consolation as possible expression of sympathetic concern among chimpanzees. Proc. Natl Acad. Sci. USA 107, 12110–12115 (2010).
Hehman, E., Flake, J. K. & Freeman, J. B. Static and dynamic facial cues differentially affect the consistency of social evaluations. Pers. Soc. Psychol. Bull. 41, 1123–1134 (2015).
Neal, D. T. & Chartrand, T. L. Embodied emotion perception. Soc. Psychol. Pers. Sci. 2, 673–678 (2011).
Burrows, A. M., Waller, B. M., Parr, L. A. & Bonar, C. J. Muscles of facial expression in the chimpanzee (Pan troglodytes): descriptive, comparative and phylogenetic contexts. J. Anat. 208, 153–167 (2006).
Vick, S.-J., Waller, B. M., Parr, L. A., Smith Pasqualini, M. C. & Bard, K. A. A cross-species comparison of facial morphology and movement in humans and chimpanzees using the facial action coding system (FACS). J. Nonverbal Behav. 31, 1–20 (2007).
Parr, L. A., Waller, B. M., Burrows, A. M., Gothard, K. M. & Vick, S. J. Brief communication: MaqFACS: a muscle-based facial movement coding system for the rhesus macaque. Am. J. Phys. Anthropol. 143, 625–630 (2010).
Waller, B. M., Lembeck, M., Kuchenbuch, P., Burrows, A. M. & Liebal, K. GibbonFACS: a muscle-based facial movement coding system for hylobatids. Int. J. Primatol. 33, 809–821 (2012).
Caeiro, C. C., Waller, B. M., Zimmermann, E., Burrows, A. M. & Davila-Ross, M. OrangFACS: a muscle-based facial movement coding system for orangutans (Pongo spp.). Int. J. Primatol. 34, 115–129 (2013).
Manapat, M. L., Nowak, M. A. & Rand, D. G. Information, irrationality, and the evolution of trust. J. Econ. Behav. Organ. 90, S57–S75 (2013).
Apicella, C. L., Marlowe, F. W., Fowler, J. H. & Christakis, N. A. Social networks and cooperation in hunter-gatherers. Nature 481, 497–501 (2012).
Hublin, J.-J. et al. New fossils from Jebel Irhoud, Morocco and the pan-African origin of Homo sapiens. Nature 546, 289–292 (2017).
Fagan, M. J. et al. Voxel-based finite element analysis—working directly with microCT scan data. J. Morphol. 268, 1071 (2007).
Toro-Ibacache, V., Fitton, L. C., Fagan, M. J. & O’Higgins, P. Validity and sensitivity of a human cranial finite element model: implications for comparative studies of biting performance. J. Anat. 228, 70–84 (2016).
Fitton, L. C., Prôa, M., Rowland, C., Toro-Ibacache, V. & O’Higgins, P. The impact of simplifications on the performance of a finite element model of a Macaca fascicularis cranium. Anat. Rec. 298, 107–121 (2015).
Parr, W. C. H. et al. Toward integration of geometric morphometrics and computational biomechanics: new methods for 3D virtual reconstruction and quantitative analysis of finite element models. J. Theor. Biol. 301, 1–14 (2012).
Dechow, P. C., Nail, G. A., Schwartz-Dabney, C. L. & Ashman, R. B. Elastic properties of human supraorbital and mandibular bone. Am. J. Phys. Anthropol. 90, 291–306 (1993).
Schwartz-Dabney, C. L. & Dechow, P. C. Variations in cortical material properties throughout the human dentate mandible. Am. J. Phys. Anthropol. 120, 252–277 (2003).
O’Higgins, P. The study of morphological variation in the hominid fossil record: biology, landmarks and geometry. J. Anat. 197, 103–120 (2000).
Zelditch, M. L., Swiderski, D. L., Sheets, H. D. & Fink, W. L. Geometric Morphometrics for Biologists: A Primer (Elsevier, New York, 2004).
Acknowledgements
R.M.G. is funded by the Portuguese Foundation for Science and Technology (PhD funding reference: SFRH/BD/76375/2011). We are grateful to L. C. Fitton and S. Cobb at Hull York Medical School, C. Stringer at the Natural History Museum and B. Waller at the University of Portsmouth for discussion about this work. We thank R. Kruszynski at the Natural History Museum for facilitating access to the computed tomography scans and the original fossil of Kabwe 1. We also thank W. Sellers at the University of Manchester for access to software (Geomagic) in his laboratory. We are also grateful to the reviewers for helpful comments and suggestions.
Author information
Authors and Affiliations
Contributions
R.M.G., P.S. and P.O. designed the experiment. R.M.G. performed the simulations. R.M.G., P.S. and P.O. wrote the manuscript.
Corresponding author
Ethics declarations
Competing interests
The authors declare no competing interests.
Additional information
Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary information
Supplementary Information
Supplementary tables and figures
Rights and permissions
About this article
Cite this article
Godinho, R.M., Spikins, P. & O’Higgins, P. Supraorbital morphology and social dynamics in human evolution. Nat Ecol Evol 2, 956–961 (2018). https://doi.org/10.1038/s41559-018-0528-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1038/s41559-018-0528-0
This article is cited by
-
Mandibular morphology and the Mesolithic–Neolithic transition in Westernmost Iberia
Scientific Reports (2023)
-
Geometric morphometric investigation of craniofacial morphological change in domesticated silver foxes
Scientific Reports (2021)
-
The sociability spectrum: evidence from reciprocal genetic copy number variations
Molecular Autism (2020)
-
Assessing the Big Five personality traits using real-life static facial images
Scientific Reports (2020)
-
The evolutionary history of the human face
Nature Ecology & Evolution (2019)