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Impaired Air Conditioning within the Nasal Cavity in Flat-Faced Homo

Impaired Air Conditioning within the Nasal Cavity in Flat-Faced Homo

  • Takeshi Nishimura, 
  • Futoshi Mori, 
  • Sho Hanida, 
  • Kiyoshi Kumahata, 
  • Shigeru Ishikawa, 
  • Kaouthar Samarat, 
  • Takako Miyabe-Nishiwaki, 
  • Misato Hayashi, 
  • Masaki Tomonaga, 
  • Juri Suzuki
PLOS
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Abstract

We are flat-faced hominins with an external nose that protrudes from the face. This feature was derived in the genus Homo, along with facial flattening and reorientation to form a high nasal cavity. The nasal passage conditions the inhaled air in terms of temperature and humidity to match the conditions required in the lung, and its anatomical variation is believed to be evolutionarily sensitive to the ambient atmospheric conditions of a given habitat. In this study, we used computational fluid dynamics (CFD) with three-dimensional topology models of the nasal passage under the same simulation conditions, to investigate air-conditioning performance in humans, chimpanzees, and macaques. The CFD simulation showed a horizontal straight flow of inhaled air in chimpanzees and macaques, contrasting with the upward and curved flow in humans. The inhaled air is conditioned poorly in humans compared with nonhuman primates. Virtual modifications to the human external nose topology, in which the nasal vestibule and valve are modified to resemble those of chimpanzees, change the airflow to be horizontal, but have little influence on the air-conditioning performance in humans. These findings suggest that morphological variation of the nasal passage topology was only weakly sensitive to the ambient atmosphere conditions; rather, the high nasal cavity in humans was formed simply by evolutionary facial reorganization in the divergence of Homo from the other hominin lineages, impairing the air-conditioning performance. Even though the inhaled air is not adjusted well within the nasal cavity in humans, it can be fully conditioned subsequently in the pharyngeal cavity, which is lengthened in the flat-faced Homo. Thus, the air-conditioning faculty in the nasal passages was probably impaired in early Homo members, although they have survived successfully under the fluctuating climate of the Plio-Pleistocene, and then they moved “Out of Africa” to explore the more severe climates of Eurasia.

Author Summary

This is the first investigation of nasal air conditioning in nonhuman hominoids based on computational fluid dynamics with digital topological models of the nasal passage made using medical imaging. Our comparative results of humans, chimpanzees, and macaques show that the inhaled air is conditioned poorly in humans compared with nonhuman primates. We also show that our protruding external nose has little effect on improving air conditioning. The nasal anatomy in Homo was weakly sensitive to the ambient atmosphere conditions in evolution, but was formed passively by facial reorganization in this genus. Even though the inhaled air is not adjusted well within the nasal cavity in humans, it can be fully conditioned subsequently in the pharyngeal cavity, which is lengthened in flat-faced Homo. Thus, despite an impaired air-conditioning conformation in the nasal passages, Homo members must have survived successfully under the fluctuating climate of the Plio-Pleistocene, and then they moved “Out of Africa” in the Early Pleistocene to explore the more severe climates and ecological environments of Eurasia.

Introduction

A flat, short face is one of the legacies of the genus Homo [1, 2]. The facial component remains short and fully below the expanded forehead in this genus, and this contrasts with earlier and contemporary hominins such as the australopithecines, which possessed a long face that protruded away from the brain case in a manner analogous to nonhuman hominids, e.g., chimpanzees [13]. Consequently, the external nose protrudes from the face [4], the nasal cavity within the facial cranium is high and quadrangular in a lateral view, and the vertically oriented nasal vestibule is connected close to the floor of the tall nasal cavity in humans [2, 5]. This pattern contrasts with that found in nonhuman primates, which possess a long and triangular nasal cavity, and a horizontally oriented vestibule that is connected vertically with the middle of the cavity [2, 5]. However, the subsequent pharyngeal cavity is much longer in humans than in nonhuman primates [610]. The nasal passage, including the nasal vestibule and cavity, conditions the inhaled air, as well as performing other functions such as olfactory sensing, dust filtering, and voice resonance [11, 12]. The pharyngeal cavity also participates in conditioning the air that enters from the nasal cavity [11]. Insufficient conditioning can damage the mucosal tissues in the respiratory system and impair respiratory performance, thereby undermining health and increasing the likelihood of death [11, 12]. Thus, despite the evolutionary modifications in the nasal anatomy in the phyletic divergence of Homo from the other hominin lineages, adequate air conditioning must have been maintained, particularly to ensure their successful survival in the severely fluctuating climate of the Pleistocene and their subsequent spread from Africa to Eurasia [1, 13, 14].

In this study, we compared the principles and performance of air conditioning in humans, chimpanzees, and macaques by using a computational fluid dynamics (CFD) model [15] to simulate the airflow and heat and water exchanges over the mucosal surface in the nasal passage. The human CFD model used here simulates the predicted airflow and air-conditioning performance reliable for humans [15]. Three-dimensional models of the nasal passage topology were produced based on tomography scans of the three genera. The models include no paranasal sinuses. We compared the air-conditioning performance in the three genera using the same simulation conditions: heat and water exchange were predicted with a simulation model based on the histological compositions of the mucosal layers and the average surface temperature of the human nasal passage, i.e., 100% relative humidity (% RH) at 34°C (3.34% of the mass fraction of water; % MF) [15]. This means that this study examines the differences in performance that are caused by the anatomical differences of the nasal passage in the three genera, but does not simulate a real performance in nonhuman primates. Whereas similar CFD analyses performed in the same subjects of macaques showed a minor contribution of the maxillary sinus to air conditioning [16], here we examine them again to compare the air-conditioning performance of the three genera using the same simulation conditions. To evaluate the effects of the human external nose, we also produced two virtual topology models: a “no-valve” model where the nasal valve—a narrow slit-like channel between the nasal vestibule and cavity—was removed virtually; and a “horizontal” model where the vertically oriented vestibule was made horizontal, as seen in chimpanzees.

We evaluated the performance among the three species in varied ambient atmospheric conditions, and discuss the evolutionary modifications in air-conditioning performance in the divergence of Homo from the other hominin lineages lineage, using nonhuman primates as a model for the latter hominins.

Materials and Methods

Ethics statement

This study for animals was performed in strict accordance with the recommendations in the third edition of the Guidelines for the Care and Use of Laboratory Primates at the Primate Research Institute of the Kyoto University (KUPRI), Inuyama, Japan. The protocol was approved by the Animal Welfare and Animal Care Committee at KUPRI (Permit Numbers: 2009–075, 2010–027, 2011–067, and 2012–075). The chimpanzees were anesthetized intramuscularly with 3.5 mg ketamine hydrochloride (Sankyo-Parke-Davis & Co., Inc.) and 0.035 mg medetomidine hydrochloride (Meiji Seika Pharma Co., Ltd., Tokyo, Japan) per kilogram of body weight. The anesthesia was maintained with sevoflurane (Dainippon Sumitomo Pharma Co., Ltd., Osaka, Japan) delivered in oxygen through a precision vaporizer and a rebreathing circuit. The macaques were anesthetized intramuscularly with 2.5 mg ketamine hydrochloride and 0.1 mg medetomidine hydrochloride per kilogram of body weight. Every effort was made to minimize suffering. The daily care and housing facilities strictly conformed to the recommendations in the third edition of the Guidelines for the Care and Use of Laboratory Primates at the KUPRI. To ensure the animals' health and welfare, their general appearance was daily monitored and recorded, along with their daily food and fluid intake.

This study for humans was performed in strict accordance with the recommendations in the Declaration of Helsinki, Ethical Principle of Medical Research Involving Human Subjects prepared by the World Medical Association. All subjects gave an informed consent. The protocol was approved by the Human Research Ethics Committee of KUPRI (Permit Number: H2011-06).

Subjects and tomographic scanning

Ten non-human primates—four chimpanzees, Pan troglodytes [17], four Japanese macaques, Macaca fuscata, and two Rhesus macaques, M. mulatta—which were reared at KUPRI, Inuyama, Japan, were scanned using a computed tomography scanner (Asteion Premium 4, Toshiba Medical Systems Co., Otawara, Japan) at the KUPRI (S1 Table). The two species of macaques are here regarded as subjects of a same genus Macaca along with a genus Pan. All of the CT scans obtained in this study came from subjects without any history of surgery and had few abnormal traits in their heads, and few artifacts distorted the images of the nasal region. The scans were registered under PRICT # (S1 Table) and are availab