No known hominin species matches the expected dental morphology of the last common ancestor of Neanderthals and modern humans

Edited by Jukka Jernvall, University of Helsinki, Helsinki, Finland, and accepted by the Editorial Board September 19, 2013 (received for review February 9, 2013)
October 21, 2013
110 (45) 18196-18201

Significance

The identity of the last common ancestor of Neanderthals and modern humans is a controversial issue. This debate has been often addressed by means of descriptive analyses that are difficult to test. Our primary aim is to put questions about human evolution into a testable quantitative framework and to offer an objective means to sort out apparently unsolvable debates about hominin phylogeny. Our paper shows that no known hominin species matches the expected morphology of this common ancestor. Furthermore, we found that European representatives of potential ancestral species have had affinities with Neanderthals for almost 1 My, thus supporting a model of early divergence between Neanderthals and modern humans.

Abstract

A central problem in paleoanthropology is the identity of the last common ancestor of Neanderthals and modern humans ([N-MH]LCA). Recently developed analytical techniques now allow this problem to be addressed using a probabilistic morphological framework. This study provides a quantitative reconstruction of the expected dental morphology of the [N-MH]LCA and an assessment of whether known fossil species are compatible with this ancestral position. We show that no known fossil species is a suitable candidate for being the [N-MH]LCA and that all late Early and Middle Pleistocene taxa from Europe have Neanderthal dental affinities, pointing to the existence of a European clade originated around 1 Ma. These results are incongruent with younger molecular divergence estimates and suggest at least one of the following must be true: (i) European fossils and the [N-MH]LCA selectively retained primitive dental traits; (ii) molecular estimates of the divergence between Neanderthals and modern humans are underestimated; or (iii) phenotypic divergence and speciation between both species were decoupled such that phenotypic differentiation, at least in dental morphology, predated speciation.

Continue Reading

Acknowledgments

We thank Emília Martins, James Rohlf, Michelle Lawing, Bernard Wood, Asier Gómez-Olivencia, and David Sánchez-Martín for discussion on several aspects of the manuscript. We also thank the editor and three anonymous reviewers for their help in improving our manuscript. Access to fossil specimens was made possible by O. Kullmer, B. Denkel, and F. Schrenk (Senckenberg Institute); D. Lordkipanidze, A. Vekua, and G. Kiladze (Georgian National Museum); H. de Lumley, M. A. de Lumley, and A. Vialet (Institut de Paléontologie Humaine); P. Mennecier (Musée de l'Homme); I. Tattersall, G. Sawyer, and G. García (American Museum of Natural History); L. Jellema and J. Haile-Selassie (Cleveland Museum of Natural History); and M. Botella (Laboratory of Physical Anthropology, University of Granada). This work was partially supported by funding by the Spanish Ministry of Science and Innovation (Project CGL2009-12703-C03-01-02-03). Fieldwork at Atapuerca is supported by the Consejería de Cultura y Turismo (Junta de Castilla y León) and the Fundación Atapuerca.

Supporting Information

Supporting Information (PDF)
Supporting Information
sd01.txt

References

1
JJ Hublin, Out of Africa: Modern human origins special feature: The origin of Neandertals. Proc Natl Acad Sci USA 106, 16022–16027 (2009).
2
JH Schwartz, I Tattersall, Fossil evidence for the origin of Homo sapiens. Am J Phys Anthropol 143, 94–121 (2010).
3
C Stringer, The status of Homo heidelbergensis (Schoetensack 1908). Evol Anthropol 21, 101–107 (2012).
4
R González-José, I Escapa, WA Neves, R Cúneo, HM Pucciarelli, Cladistic analysis of continuous modularized traits provides phylogenetic signals in Homo evolution. Nature 453, 775–778 (2008).
5
DC Adams, A Cardini, LR Monteiro, P O’Higgins, FJ Rohlf, Morphometrics and phylogenetics: Principal components of shape from cranial modules are neither appropriate nor effective cladistic characters. J Hum Evol 60, 240–243 (2011).
6
EP Martins, TF Hansen, Phylogenies and the comparative method: A general approach to incorporating phylogenetic information into the analysis of interspecific data. Am Nat 149, 646–667 (1997).
7
DS Strait, Human systematics. A Companion to Paleoanthropology, ed DR Begun (Blackwell Publishing, Oxford), pp. 35–54 (2013).
8
B Wood, N Lonergan, The hominin fossil record: Taxa, grades and clades. J Anat 212, 354–376 (2008).
9
I Tattersall, Neanderthals, Homo sapiens, and the question of species in paleoanthropology. J Anthropol Sci 85, 139–146 (2007).
10
JL Arsuaga, I Martínez, A Gracia, C Lorenzo, The Sima de los Huesos crania (Sierra de Atapuerca, Spain). A comparative study. J Hum Evol 33, 219–281 (1997).
11
P Endicott, SY Ho, C Stringer, Using genetic evidence to evaluate four palaeoanthropological hypotheses for the timing of Neanderthal and modern human origins. J Hum Evol 59, 87–95 (2010).
12
A Gómez-Robles, JM Bermúdez de Castro, M Martinón-Torres, L Prado-Simón, JL Arsuaga, A geometric morphometric analysis of hominin upper second and third molars, with particular emphasis on European Pleistocene populations. J Hum Evol 63, 512–526 (2012).
13
JL Bischoff, et al., The Sima de los Huesos hominids date to beyond U/Th equilibrium (>350 kyr) and perhaps to 400-500 kyr: New radiometric dates. J Archaeol Sci 30, 275–280 (2003).
14
JL Bischoff, et al., High-resolution U-series dates from the Sima de los Huesos hominids yields 600 kyrs: Implications for the evolution of the early Neanderthal lineage. J Archaeol Sci 34, 763–770 (2007).
15
RE Green, et al., A draft sequence of the Neandertal genome. Science 328, 710–722 (2010).
16
SC Antón, Natural history of Homo erectus. Am J Phys Anthropol 46, 126–170 (2003).
17
G Shen, X Gao, B Gao, DE Granger, Age of Zhoukoudian Homo erectus determined with (26)Al/(10)Be burial dating. Nature 458, 198–200 (2009).
18
GP Rightmire, Homo in the Middle Pleistocene: Hypodigms, variation, and species recognition. Evol Anthropol 17, 8–21 (2008).
19
JM Parés, et al., Reassessing the age of Atapuerca-TD6 (Spain): New paleomagnetic results. J Archaeol Sci 40, 4586–4595 (2013).
20
B Wood, M Collard, The human genus. Science 284, 65–71 (1999).
21
PD Polly, Paleontology and the comparative method: Ancestral node reconstructions versus observed node values. Am Nat 157, 596–609 (2001).
22
G Bräuer, The origin of modern anatomy: By speciation or intraspecific evolution? Evol Anthropol 17, 22–37 (2008).
23
GP Rightmire, Human evolution in the Middle Pleistocene: The role of Homo heidelbergensis. Evol Anthropol 6, 218–227 (1998).
24
C Stringer, Modern human origins: Progress and prospects. Philos Trans R Soc Lond B Biol Sci 357, 563–579 (2002).
25
A Gómez-Robles, PD Polly, Morphological integration in the hominin dentition: evolutionary, developmental, and functional factors. Evolution 66, 1024–1043 (2012).
26
E Trinkaus, Modern human versus Neandertal evolutionary distinctiveness. Curr Anthropol 47, 597–620 (2006).
27
TD Weaver, CC Roseman, CB Stringer, Were neandertal and modern human cranial differences produced by natural selection or genetic drift? J Hum Evol 53, 135–145 (2007).
28
SE Bailey, A morphometric analysis of maxillary molar crowns of Middle-Late Pleistocene hominins. J Hum Evol 47, 183–198 (2004).
29
A Gómez-Robles, et al., A geometric morphometric analysis of hominin upper first molar shape. J Hum Evol 53, 272–285 (2007).
30
M Martinón-Torres, et al., Gran Dolina-TD6 and Sima de los Huesos dental samples: Preliminary approach to some dental characters of interest for phylogenetic studies. Dental Perspectives on Human Evolution, eds SE Bailey, J-J Hublin (Springer, Berlin), pp. 65–79 (2007).
31
A Gómez-Robles, JM de Castro, M Martinón-Torres, L Prado-Simón, Crown size and cusp proportions in Homo antecessor upper first molars. A comment on Quam et al. 2009. J Anat 218, 258–262 (2011).
32
K MacDonald, M Martinón-Torres, RW Dennell, JM Bermúdez de Castro, Discontinuity in the record for hominin occupation in South-Western Europe: Implications for occupation of the middle latitudes of Europe. Quat Int 271, 84–97 (2012).
33
RW Dennell, M Martinón-Torres, JM Bermúdez de Castro, Hominin variability, climatic instability and population demography in Middle Pleistocene Europe. Quat Sci Rev 30, 1511–1524 (2011).
34
CJ Jolly, A proper study for mankind: Analogies from the Papionin monkeys and their implications for human evolution. Am J Phys Anthropol 116, 177–204 (2001).
35
TD Weaver, CC Roseman, CB Stringer, Close correspondence between quantitative- and molecular-genetic divergence times for Neandertals and modern humans. Proc Natl Acad Sci USA 105, 4645–4649 (2008).
36
J Hawks, Longer time scale for human evolution. Proc Natl Acad Sci USA 109, 15531–15532 (2012).
37
KE Langergraber, et al., Generation times in wild chimpanzees and gorillas suggest earlier divergence times in great ape and human evolution. Proc Natl Acad Sci USA 109, 15716–15721 (2012).
38
A Scally, R Durbin, Revising the human mutation rate: Implications for understanding human evolution. Nat Rev Genet 13, 745–753 (2012).
39
Q Fu, et al., A revised timescale for human evolution based on ancient mitochondrial genomes. Curr Biol 23, 553–559 (2013).
40
RE Green, B Shapiro, Human evolution: Turning back the clock. Curr Biol 23, R286–R288 (2013).
41
JM Bermúdez de Castro, et al., A hominid from the lower Pleistocene of Atapuerca, Spain: Possible ancestor to Neandertals and modern humans. Science 276, 1392–1395 (1997).
42
J-L Arsuaga, et al., The human cranial remains from Gran Dolina Lower Pleistocene site (Sierra de Atapuerca, Spain). J Hum Evol 37, 431–457 (1999).
43
R García-González, et al., Étude analytique d’une clavicule complète de subadulte d’Homo antecessor (site de Gran Dolina, Sierra d’Atapuerca, Burgos, Espagne). Anthropologie 113, 222–232, French. (2009).
44
SI Pérez, V Bernal, PN González, M Sardi, GG Politis, Discrepancy between cranial and DNA data of early Americans: Implications for American peopling. PLoS ONE 4, e5746 (2009).
45
FL Bookstein, Applying landmark methods to biological outline data. Image Fusion and Shape Variability Techniques, eds KV Mardia, CA Gill, IL Dryden (Leeds Univ Press, Leeds, UK), pp. 79–87 (1996).
46
Rohlf FJ (2005) tpsDig2 software. (State Univ of New York, Stony Brook, NY).
47
FJ Rohlf, D Slice, Extensions of the Procrustes method for the optimal superimposition of landmarks. Syst Zool 39, 40–59 (1990).
48
IL Dryden, KV Mardia Statistical Shape Analysis (Wiley, New York, 1998).
49
PD Polly, Adaptive zones and the pinniped ankle: A three-dimensional quantitative analysis of carnivoran tarsal evolution. Mammalian Evolutionary Morphology, a Tribute to Frederick S. Szalay, eds E Sargis, M Dagosto (Springer, Dordrecht, The Netherlands), pp. 167–196 (2008).
50
FJ Rohlf, Comparative methods for the analysis of continuous variables: Geometric interpretations. Evolution 55, 2143–2160 (2001).
51
Polly PD (2012) Geometric morphometrics for Mathematica. Version 9.0. (Indiana University ScholarWorks). Available at http://hdl.handle.net/2022/14613. June 1, 2013.
52
M Pagel, Modelling the evolution of continuously varying characters on phylogenetic trees: The case of hominid cranial capacity. Morphology, Shape and Phylogeny, eds N MacLeod, PL Forey (Taylor & Francis, London), pp. 269–286 (2002).
53
TH Oakley, CW Cunningham, Independent contrasts succeed where ancestor reconstruction fails in a known bacteriophage phylogeny. Evolution 54, 397–405 (2000).
54
J Felsenstein Inferring Phylogenies (Sinauer, Sunderland, MA, 2004).
55
PD Polly, On the simulation of the evolution of morphological shape: Multivariate shape under selection and drift. Palaeontol Electronica 7, 1–28 (2004).
56
G Hunt, Phenotypic variation in fossil samples: Modeling the consequences of time-averaging. Paleobiology 30, 426–443 (2004).

Information & Authors

Information

Published in

Go to Proceedings of the National Academy of Sciences
Go to Proceedings of the National Academy of Sciences
Proceedings of the National Academy of Sciences
Vol. 110 | No. 45
November 5, 2013
PubMed: 24145426

Classifications

Submission history

Published online: October 21, 2013
Published in issue: November 5, 2013

Keywords

  1. phylogeny
  2. node reconstruction
  3. geometric morphometrics
  4. morphospace
  5. European Pleistocene

Acknowledgments

We thank Emília Martins, James Rohlf, Michelle Lawing, Bernard Wood, Asier Gómez-Olivencia, and David Sánchez-Martín for discussion on several aspects of the manuscript. We also thank the editor and three anonymous reviewers for their help in improving our manuscript. Access to fossil specimens was made possible by O. Kullmer, B. Denkel, and F. Schrenk (Senckenberg Institute); D. Lordkipanidze, A. Vekua, and G. Kiladze (Georgian National Museum); H. de Lumley, M. A. de Lumley, and A. Vialet (Institut de Paléontologie Humaine); P. Mennecier (Musée de l'Homme); I. Tattersall, G. Sawyer, and G. García (American Museum of Natural History); L. Jellema and J. Haile-Selassie (Cleveland Museum of Natural History); and M. Botella (Laboratory of Physical Anthropology, University of Granada). This work was partially supported by funding by the Spanish Ministry of Science and Innovation (Project CGL2009-12703-C03-01-02-03). Fieldwork at Atapuerca is supported by the Consejería de Cultura y Turismo (Junta de Castilla y León) and the Fundación Atapuerca.

Notes

This article is a PNAS Direct Submission. J.J. is a guest editor invited by the Editorial Board.

Authors

Affiliations

Aida Gómez-Robles1 [email protected]
Department of Anthropology, The George Washington University, Washington, DC 20052;
Konrad Lorenz Institute for Evolution and Cognition Research, A-3422 Altenberg, Austria;
José María Bermúdez de Castro
Centro Nacional de Investigación sobre la Evolución Humana, 09002 Burgos, Spain;
Juan-Luis Arsuaga
Centro de Investigación Sobre la Evolución y Comportamiento Humanos, Universidad Complutense de Madrid–Instituto de Salud Carlos III, 28029 Madrid, Spain;
Eudald Carbonell
Institut Català de Paleoecologia Humana i Evolució Social, Universitat Rovira i Virgili, 43007 Tarragona, Spain; and
P. David Polly
Departments of Geological Sciences, Biology, and Anthropology, Indiana University, Bloomington,IN 47405

Notes

1
To whom correspondence should be addressed. E-mail: [email protected].
Author contributions: A.G.-R. and P.D.P. designed research; A.G.-R., J.M.B.d.C., J.-L.A., E.C., and P.D.P. performed research; P.D.P. contributed new reagents/analytic tools; A.G.-R. analyzed data; and A.G.-R. and P.D.P. wrote the paper.

Competing Interests

The authors declare no conflict of interest.

Metrics & Citations

Metrics

Note: The article usage is presented with a three- to four-day delay and will update daily once available. Due to ths delay, usage data will not appear immediately following publication. Citation information is sourced from Crossref Cited-by service.


Citation statements

Altmetrics

Citations

If you have the appropriate software installed, you can download article citation data to the citation manager of your choice. Simply select your manager software from the list below and click Download.

Cited by

    Loading...

    View Options

    View options

    PDF format

    Download this article as a PDF file

    DOWNLOAD PDF

    Get Access

    Login options

    Check if you have access through your login credentials or your institution to get full access on this article.

    Personal login Institutional Login

    Recommend to a librarian

    Recommend PNAS to a Librarian

    Purchase options

    Purchase this article to get full access to it.

    Single Article Purchase

    No known hominin species matches the expected dental morphology of the last common ancestor of Neanderthals and modern humans
    Proceedings of the National Academy of Sciences
    • Vol. 110
    • No. 45
    • pp. 18025-18339

    Media

    Figures

    Tables

    Other

    Share

    Share

    Share article link

    Share on social media