How the unique configuration of the human head may enhance flavor perception capabilities: an evolutionary perspective
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Harvard University, Human Evolutionary Biology, United States
Since flavor derives from the synthesis of taste, somatosensation and smell, one of the most important factors in the ability to perceive flavor is retronasal olfaction in which volatile compounds pass from the oral cavity through the pharynx to the olfactory epithelium. Retronasal olfaction has been documented in both humans and rodents, but appears less effective in rodents than orthonasal olfaction because expired air does not come into as much contact with the sensory neurons in the olfactory epithelium as inspired air [1,2]. Detailed comparisons of retronasal airflow patterns among different species have not been conducted, but several lines of evidence lead to the hypothesis that retronasal airflow may be specially enhanced in humans because of four derived features of the human head and neck that evolved at different stages because of selection for functions other than olfaction [3]. If so, then human flavor perception capabilities may be more derived than is commonly appreciated, and perhaps played a role in selecting for the evolution of cooking.
The first derived adaptation that aids human retronasal olfaction is the absence of the transverse lamina, a horizontal shelf of bone that partitions the olfactory chamber of the nasal fossa from the more inferior respiratory passage. This lamina, which is present in most mammals, was lost during the evolution of monkeys (haplorhines) from more primitive primates (strepsirhines) as part of a reorganization of the nasal cavity. The function of the transverse lamina has not been tested but it probably aids orthonasal olfaction by trapping inspired air in the olfactory region. Loss of the transverse lamina is commonly interpreted to be one of several trade-offs in primate evolution that favored vision over olfaction [4], but it likely benefits retronasal olfaction by permitting a direct pathway for expired air to flow towards the olfactory epithelium.
A second derived adaptation present in humans is the 90° orientation of the neck relative to the long axes of the nasal and oral cavities (Figure 1). This shift in the orientation was almost certainly selected for because of the evolution of bipedalism, which appears to be the key derived feature that distinguishes early hominins from other apes. Although bipedalism likely evolved as an adaption for hominins to locomote and forage efficiently, a vertically oriented neck requires expired air to turn approximately 90° to get from the nasopharynx to the external nares [reviewed in 3]. Consequently, a larger percentage of expired air in bipedal hominins is directed toward the superior margin of the nasal cavity, hence to the olfactory epithelium.
The third derived adaptation of humans that may aid retronasal olfaction is enhanced turbulence in the nasal cavity. Turbulent flow generates more resistance than laminar flow but likely increases the ability for odorants to bind to olfactory neurons by slowing airflow rates, causing a higher percentage of odorants to circulate repeatedly in vortices along the margins of the olfactory epithelium, and by eliminating the boundary zone of inert air that occurs during pure laminar flow [2]. Retronasal airflow turbulence in humans is likely increased by the 90° turn that expired air must take to enter the nasal cavity, by shortening of the nasal cavity from the loss of a snout, and by valve-like discontinuities in cross sectional area between the nasal cavity, the internal nares, and the nasopharynx. Some of these features evolved in the first bipedal hominins, but others such as midfacial shortening evolved in the genus Homo. Although enhanced turbulence in the nose may benefit olfaction, it most likely evolved as an adaptation to enhance the ability to control the humidity and temperature of both inspired and expired air during vigorous physical activity in hot, arid conditions [reviewed in 3].
The final adaptation that may improve retronasal olfaction is the unique configuration of the human pharynx (Figure 1). Unlike other mammals, humans have a relatively short and retracted face, which results in a short oral cavity with a rounded tongue whose inferior margin lies well below the margin of the mandible. Because the hyoid and larynx are suspended from the base of the tongue, the human larynx becomes separated early in postnatal life relative to the oral cavity, causing humans to be the only species with a non-intranarial epiglottis in which the epiglottis does not contact the soft palate [3]. As a result, humans have no separation between the airway and foodway in the oropharynx. The non-intranarial epiglottis makes humans more likely to choke on food than other mammals, but helps humans produce more perceptible speech by setting up a two-tube vocal tract whose horizontal and vertical portions are equal in length and whose cross sectional areas can be modified independently by approximately 10-fold by the tongue [5]. Although this configuration almost certainly evolved for speech, it likely has beneficial consequences for retronasal olfaction. Whereas all other mammals, including chimpanzees, store a bolus of food prior to swallowing anterior to the epiglottis and thus removed from the airway, humans must store the bolus superior to the epiglottis in the pathway of expired air. Thus as humans breathe while chewing between swallows, expired air may be more likely to pick up volatile compounds from foods, which are then transported retronasally to the olfactory epithelium.
The hypothesis that derived features of the human head and neck enhance retronasal olfaction needs to be tested. Comparative data are especially needed on retronasal airflow in a variety of mammals including other primates. In addition, more data are needed on retronasal olfactory perception in great apes such as chimpanzees. However, if true, then it is possible that humans may have uniquely enhanced abilities to detect flavor from food, raising several evolutionary hypotheses. Given that bipedalism, speech and thermoregulation were probably strong selective forces in human evolution, it is likely that enhanced retronasal olfaction in humans is a byproduct of selection for other adaptations. However, it is reasonable to hypothesize that the ability to perceive flavor from food may, in turn, have played an important role in the evolution of cooking, which creates more odorants that enhance flavor. Perhaps humans who enjoyed the enhanced flavors of cooked food were more likely to cook their food, leading to selection for greater reliance on cooked food, which has many energetic and nutritional benefits [6].
References
1. Scott JW, Acevedo HP, Sherrill L, Phan M (2007) J Neurophysiol 97:1941–1950.
2. Zhao K, Scherer PW, Hajiloo SA, Dalton P (2004) Chem Senses 29:365–379.
3. Lieberman DE (2011) The Evolution of the Human Head. Cambridge, MA: Harvard University Press.
4. Martin RB (1990) Primate Origins and Evolution: A Phylogenetic Reconstruction. Princeton University Press
5. Lieberman P (1984) The Biology and Evolution of Language. Cambridge, MA: Harvard University Press
6. Wrangham RW (2009) Catching Fire: How Cooking Made us Human. New York: Basic Books
Keywords:
Cooking,
flavor,
Hominins,
Human head,
Nasopharynx,
Retronasal Olfaction
Conference:
Science of Human Flavor Perception, New York, United States, 9 May - 9 May, 2014.
Presentation Type:
Abstract
Topic:
Science of Human Flavor Perception
Citation:
Lieberman
DE
(2015). How the unique configuration of the human head may enhance flavor perception capabilities: an evolutionary perspective.
Front. Integr. Neurosci.
Conference Abstract:
Science of Human Flavor Perception.
doi: 10.3389/conf.fnint.2015.03.00003
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Received:
28 Jul 2014;
Published Online:
30 Jan 2015.
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Correspondence:
Prof. Daniel E Lieberman, Harvard University, Human Evolutionary Biology, Cambridge, MA, United States, danlieb@fas.harvard.edu