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.2017 Nov 21;114(47):12442-12447.
doi: 10.1073/pnas.1703790114. Epub 2017 Oct 30.

Nasal airflow simulations suggest convergent adaptation in Neanderthals and modern humans

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Nasal airflow simulations suggest convergent adaptation in Neanderthals and modern humans

S de Azevedo et al. Proc Natl Acad Sci U S A..

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.

Keywords: Homo sapiens; Neanderthal; computational fluid dynamics; nasal morphology; quantitative genetics.

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Conflict of interest statement

The authors declare no conflict of interest.

Figures

Fig. 1.
Fig. 1.
Nasal morphological variation between MHs and Neanderthals as seen by principal component analysis and canonical variate analysis. (A) Scheme representing the anatomical landmarks placed on the external and internal osseous nasal structures (SI Appendix, Table S1). (B) First two PCs of shape change. NEA, blue dots; Neanderthals, red dots; SWE, green dots. SWE-93776 and NEA-2116236 specimens are indicated with empty dots. The arrow represents the displacement across the morphospace used to obtain the Neanderthal soft anatomy departing from the MH internal cavity, including the mucosa and turbinate soft structures. (C) Internal nasal cavity warped shape changes occurring across the first PC. The shape change defining the MH nose involve a general narrowing of the nose, both in their superior and inferior parts, along with an anterior-posterior alignment of the most anterior part of the concha with the external nasal border. The Neanderthal anatomy, conversely, is characterized by broader noses in general, along with a deflection of the anterior limit of the concha, which is placed on a more medial position in relation to the external border of the nose. In addition, an inspection on the sagittal plane of these shape changes indicate that MH noses present a more anterior projection of the medial part of the nasal border, whereas Neanderthals present, in general, a more flat nasal plane. (D) First and second canonical axes obtained from the first five PCs depicting shape changes that most differentiate the three groups (Neanderthals, SWE, NEA) in terms of nasal shape. The centroid shape of each group is presented as a warped internal nose. Discriminant functions among the three groups, withP values obtained after 10,000 permutations are as follows: SWE-Neanderthal Mahalanobis distance: 11.5 (P = 0.006). NEA-Neanderthal Mahalanobis distance: 55.3 (P = 0.029). SWE-NEA Mahalanobis distance: 2.48 (P = 0.005).
Fig. 2.
Fig. 2.
CFD model results. Temperature (°C) (A) and specific humidity [kgvap/kgda]) fields (B), at rest for forward (f: nasal vestibular zone) and backward (b: nasopharyngeal tract zone) planes when the pressure drop is maximum (t = 1.25 s;SI Appendix, Eq.S8) in cold-dry weather conditions for SWE, NEA, and Neanderthal. The temperature distribution in frontal planes f, when the breathing cycle reaches a maximum flow rate, shows that the mixture achieves the conditioning temperature faster for the NEA specimen, followed by Neanderthals showing an intermediate performance, especially in the superior part of the tract, and then by SWE, showing a relative worst performance. The temperature close to the oropharynx (plane b) is totally conditioned in NEA cavity and almost fully conditioned for the other two cavities. The moisture content or specific humidity at frontal planes follows the same behavior as the temperature field, being bigger in average for NEA nose, followed by Neanderthals and SWE. Specific humidity is in full saturation in plane b for NEA and almost saturated for Neanderthal and SWE noses. Averaged velocities at planes f and b are shown inC andD, respectively. It can be observed that the magnitude of the established velocities is 3.5–4 times bigger in the SWE and Neanderthal cavities than in NEA. Then, the residence time of a volume of mixture will be longer in NEA than in SWE and Neanderthals, enhancing the heat transfer from mucosa to the fluid and consequently the moist conditioning.E shows the volume-averaged specific thermal fluxq =uavrgρcp(Twall −Tmix)Anose/Vnose(in [W/m2]) needed for the conditioning of each specimen.uavrg is the average of the velocity field using data ofC andD, andAnose andVnose are the mucosa surface area and nose volume (SI Appendix), respectively. SeeSI Appendix, Figs. S9 and S10 for further details.
Fig. 3.
Fig. 3.
Phylogenetic framework and results for Lande’s genetic drift test. (Left) Cladograms depicting the position of cold-adapted species/populations (in terms of the ancestral climate condition, shown in yellow branches and boxes) in Macaca (Top), Hominidae (Middle), andHomo sapiens (Bottom) clades. Further details on samples characteristics can be found inSI Appendix, Table S5. See refs. , , and for further discussion on this topic. (Right Top) Whole skull configuration (all dots) and nasal configuration (blue dots). (Right Middle andRight Bottom) Lande’s results for the hierarchical groups studied here: all hominins,H. sapiens populations, fossil hominins,Macaca genus, fossilHomo species, Australopithecines,H. sapiens +H. neanderthalensis, whole skull configuration (Middle scheme) and nasal configuration (Bottom scheme). Blue boxes, Lande’s results compatible with stabilizing selection operating at the taxonomic level under study; gray boxes, Lande’s results compatible with genetic drift.
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References

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