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Research Article

Nasal airflow simulations suggest convergent adaptation in Neanderthals and modern humans

S. de Azevedo, M. F. González, C. Cintas, V. Ramallo, M. Quinto-Sánchez, F. Márquez, T. Hünemeier, C. Paschetta, A. Ruderman, P. Navarro, B. A. Pazos, C. C. Silva de Cerqueira, O. Velan, F. Ramírez-Rozzi, N. Calvo, H. G. Castro, View ORCID ProfileR. R. Paz, and R. González-José
PNAS November 21, 2017 114 (47) 12442-12447; first published October 30, 2017; https://doi.org/10.1073/pnas.1703790114
S. de Azevedo
aInstituto Patagónico de Ciencias Sociales y Humanas, Centro Nacional Patagónico, Consejo Nacional de Investigaciones Científicas y Técnicas, U9120ACD, Puerto Madryn, Argentina;
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M. F. González
aInstituto Patagónico de Ciencias Sociales y Humanas, Centro Nacional Patagónico, Consejo Nacional de Investigaciones Científicas y Técnicas, U9120ACD, Puerto Madryn, Argentina;
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C. Cintas
aInstituto Patagónico de Ciencias Sociales y Humanas, Centro Nacional Patagónico, Consejo Nacional de Investigaciones Científicas y Técnicas, U9120ACD, Puerto Madryn, Argentina;
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V. Ramallo
aInstituto Patagónico de Ciencias Sociales y Humanas, Centro Nacional Patagónico, Consejo Nacional de Investigaciones Científicas y Técnicas, U9120ACD, Puerto Madryn, Argentina;
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M. Quinto-Sánchez
bCiencia Forense, Facultad de Medicina, Circuito de la Investigación Científica s/n, Ciudad Universitaria, Universidad Nacional Autónoma de México, Del. Coyoacán, CP 04510, Mexico;
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F. Márquez
cInstituto de Biología de Organismos Marinos, Centro Nacional Patagónico, Consejo Nacional de Investigaciones Científicas y Técnicas, U9120ACD, Puerto Madryn, Argentina;
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T. Hünemeier
dDepartamento de Genética e Biologia Evolutiva, Cidade Universitária, University of São Paulo, 05508-900, São Paulo, Brazil;
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C. Paschetta
aInstituto Patagónico de Ciencias Sociales y Humanas, Centro Nacional Patagónico, Consejo Nacional de Investigaciones Científicas y Técnicas, U9120ACD, Puerto Madryn, Argentina;
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A. Ruderman
aInstituto Patagónico de Ciencias Sociales y Humanas, Centro Nacional Patagónico, Consejo Nacional de Investigaciones Científicas y Técnicas, U9120ACD, Puerto Madryn, Argentina;
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P. Navarro
aInstituto Patagónico de Ciencias Sociales y Humanas, Centro Nacional Patagónico, Consejo Nacional de Investigaciones Científicas y Técnicas, U9120ACD, Puerto Madryn, Argentina;
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B. A. Pazos
aInstituto Patagónico de Ciencias Sociales y Humanas, Centro Nacional Patagónico, Consejo Nacional de Investigaciones Científicas y Técnicas, U9120ACD, Puerto Madryn, Argentina;
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C. C. Silva de Cerqueira
eSuperintendência da Polícia Técnico-Científica do Estado de São Paulo, Equipe de Perícias Criminalísticas de Ourinhos, 19901-560, São Paulo, Brazil;
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O. Velan
fDepartamento Académico de Ciencias Morfológicas, Hospital Italiano, C1199ABB, Buenos Aires, Argentina;
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F. Ramírez-Rozzi
gUMR 5288 Anthropologie Moléculaire et Imagerie de Synthèse, CNRS, 92120 Montrouge, France;
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N. Calvo
hDepartment of Computing, Universidad Nacional del Litoral, S3000, Santa Fe, Argentina;
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H. G. Castro
iInstituto de Modelado e Innovación Tecnológica, Universidad Nacional del Nordeste, CP W3404AAS, Corrientes, Argentina;
jConsejo Nacional de Investigaciones Científicas y Técnicas, C1425FQB, Buenos Aires, Argentina;
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R. R. Paz
jConsejo Nacional de Investigaciones Científicas y Técnicas, C1425FQB, Buenos Aires, Argentina;
kLivermore Software Technology Corporation, Livermore, CA 94551
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  • ORCID record for R. R. Paz
  • For correspondence: rodrigo.r.paz@gmail.com rolando@cenpat-conicet.gob.ar
R. González-José
aInstituto Patagónico de Ciencias Sociales y Humanas, Centro Nacional Patagónico, Consejo Nacional de Investigaciones Científicas y Técnicas, U9120ACD, Puerto Madryn, Argentina;
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  • For correspondence: rodrigo.r.paz@gmail.com rolando@cenpat-conicet.gob.ar
  1. Edited by Cynthia M. Beall, Case Western Reserve University, Cleveland, OH, and approved July 31, 2017 (received for review March 13, 2017)

This article has a Letter. Please see:

  • Impact of sampling strategies and reconstruction protocols in nasal airflow simulations in fossil hominins - May 04, 2018

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  • Reply to Evteev and Heuzé: How to overcome the problem of modeling respiration departing from bony structures
    - May 04, 2018
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Significance

Due to its role in humidifying and warming the air before it reaches the lungs, adaptations in the internal nasal anatomy are suspected to have been essential for modern humans and Neanderthals during the settlement of Eurasian harsh landscapes. Unfortunately, the lack of soft-tissue evidence in the fossil record precludes any study of Neanderthal respiratory performance. Here, we use warping techniques to reconstruct a generic Neanderthal nose, computational fluid dynamics simulations to compare the respiratory performance on both species, and evolutionary analyses to detect signals of selection. We report striking differences on fluid residence times under cold/dry climatic conditions. Different from previously suggested, our results indicate that both species would have achieved an advantageous species-specific respiratory performance in cold climates.

Abstract

Both modern humans (MHs) and Neanderthals successfully settled across western Eurasian cold-climate landscapes. Among the many adaptations considered as essential to survival in such landscapes, changes in the nasal morphology and/or function aimed to humidify and warm the air before it reaches the lungs are of key importance. Unfortunately, the lack of soft-tissue evidence in the fossil record turns difficult any comparative study of respiratory performance. Here, we reconstruct the internal nasal cavity of a Neanderthal plus two representatives of climatically divergent MH populations (southwestern Europeans and northeastern Asians). The reconstruction includes mucosa distribution enabling a realistic simulation of the breathing cycle in different climatic conditions via computational fluid dynamics. Striking across-specimens differences in fluid residence times affecting humidification and warming performance at the anterior tract were found under cold/dry climate simulations. Specifically, the Asian model achieves a rapid air conditioning, followed by the Neanderthals, whereas the European model attains a proper conditioning only around the medium-posterior tract. In addition, quantitative-genetic evolutionary analyses of nasal morphology provided signals of stabilizing selection for MH populations, with the removal of Arctic populations turning covariation patterns compatible with evolution by genetic drift. Both results indicate that, departing from important craniofacial differences existing among Neanderthals and MHs, an advantageous species-specific respiratory performance in cold climates may have occurred in both species. Fluid dynamics and evolutionary biology independently provided evidence of nasal evolution, suggesting that adaptive explanations regarding complex functional phenotypes require interdisciplinary approaches aimed to quantify both performance and evolutionary signals on covariation patterns.

  • nasal morphology
  • computational fluid dynamics
  • quantitative genetics
  • Neanderthal
  • Homo sapiens

Footnotes

  • ↵1S.d.A., M.F.G., and C.C. contributed equally to this work.

  • ↵2To whom correspondence may be addressed. Email: rodrigo.r.paz{at}gmail.com or rolando{at}cenpat-conicet.gob.ar.
  • Author contributions: S.d.A., M.F.G., C.C., O.V., R.R.P., and R.G.-J. designed research; S.d.A., M.F.G., C.C., V.R., M.Q.-S., F.M., T.H., C.P., A.R., P.N., B.A.P., C.C.S.d.C., O.V., F.R.-R., N.C., H.G.C., R.R.P., and R.G.-J. performed research; O.V., F.R.-R., H.G.C., R.R.P., and R.G.-J. contributed new reagents/analytic tools; S.d.A., M.F.G., C.C., V.R., M.Q.-S., F.M., T.H., C.P., A.R., P.N., B.A.P., C.C.S.d.C., O.V., F.R.-R., N.C., H.G.C., R.R.P., and R.G.-J. analyzed data; and S.d.A., C.C., F.R.-R., R.R.P., and R.G.-J. wrote the paper.

  • The authors declare no conflict of interest.

  • This article is a PNAS Direct Submission.

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1703790114/-/DCSupplemental.

Published under the PNAS license.

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Nasal adaptation in Neanderthals and modern humans
S. de Azevedo, M. F. González, C. Cintas, V. Ramallo, M. Quinto-Sánchez, F. Márquez, T. Hünemeier, C. Paschetta, A. Ruderman, P. Navarro, B. A. Pazos, C. C. Silva de Cerqueira, O. Velan, F. Ramírez-Rozzi, N. Calvo, H. G. Castro, R. R. Paz, R. González-José
Proceedings of the National Academy of Sciences Nov 2017, 114 (47) 12442-12447; DOI: 10.1073/pnas.1703790114

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Nasal adaptation in Neanderthals and modern humans
S. de Azevedo, M. F. González, C. Cintas, V. Ramallo, M. Quinto-Sánchez, F. Márquez, T. Hünemeier, C. Paschetta, A. Ruderman, P. Navarro, B. A. Pazos, C. C. Silva de Cerqueira, O. Velan, F. Ramírez-Rozzi, N. Calvo, H. G. Castro, R. R. Paz, R. González-José
Proceedings of the National Academy of Sciences Nov 2017, 114 (47) 12442-12447; DOI: 10.1073/pnas.1703790114
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