The human nose could have evolved to separate olfactory inputs to enhance stereo olfaction; as humans became more sedentary in the Neolithic, maybe other functions appeared (detecting disease in newly dense human settlements)

The navigational nose: a new hypothesis for the function of the human external pyramid. Lucia F. Jacobs. Journal of Experimental Biology 2019 222: jeb186924. February 6 2019, doi: 10.1242/jeb.186924

ABSTRACT: One of the outstanding questions in evolution is why Homo erectus became the first primate species to evolve the external pyramid, i.e. an external nose. The accepted hypothesis for this trait has been its role in respiration, to warm and humidify air as it is inspired. However, new studies testing the key assumptions of the conditioning hypothesis, such as the importance of turbulence to enhance heat and moisture exchange, have called this hypothesis into question. The human nose has two functions, however, respiration and olfaction. It is thus also possible that the external nose evolved in response to selection for olfaction. The genus Homo had many adaptations for long-distance locomotion, which allowed Homo erectus to greatly expand its species range, from Africa to Asia. Long-distance navigation in birds and other species is often accomplished by orientation to environmental odors. Such olfactory navigation, in turn, is enhanced by stereo olfaction, made possible by the separation of the olfactory sensors. By these principles, the human external nose could have evolved to separate olfactory inputs to enhance stereo olfaction. This could also explain why nose shape later became so variable: as humans became more sedentary in the Neolithic, a decreasing need for long-distance movements could have been replaced by selection for other olfactory functions, such as detecting disease, that would have been critical to survival in newly dense human settlements.


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Human olfactory navigation

Olfaction is often underestimated as a sensory basis for navigation (Jacobs, 2012). This neglect is particularly acute in the study of human navigation (Jacobs et al., 2015). This is partly because primates, and particularly humans, have erroneously been assumed to have exceptionally poor olfactory abilities (Laska et al., 2000; McGann, 2017; Shepherd, 2004). Yet, in many species, including humans, the largest gene superfamilies are those for olfactory receptors (Hasin-Brumshtein et al., 2009). And while primates are indeed highly visual (Smith et al., 2007, 2014), visual acuity does not preclude the use of olfaction for long-distance movements in other highly visual animals such as birds (Wallraff, 2005).

Descriptive reports of humans using odors to navigate have a long history (Porteous, 1985; Gatty, 1983), especially in the visually impaired (Koutsoklenis and Papadopoulos, 2011), although there are to date only two experimental studies of olfactory navigation in humans. In the first study, humans were shown to accurately follow an odor trail of chocolate across a grassy field, and their accuracy was enhanced by stereo olfaction (Porter et al., 2007). In another study, humans were able to learn and map an arbitrary location in a room using only odor gradients (Jacobs et al., 2015).

Clearly, the human ability to orient to odors is not as highly developed as that of olfactory specialists, such as the domestic dog. First, the human internal nasal chamber is smaller than expected for a mammal of its body size (Zwicker et al., 2018). Its chamber lacks an olfactory recess, a feature found in the domestic dog that separates the olfactory air stream from the respiratory air stream. The recess is thought to retard and enhance the processing of air to extract odors (Craven et al., 2010, 2007).

But to make the analogy with birds once again: just because human olfaction is inferior does not mean it is not functional. Modern birds also have a reduced olfactory system in comparison to their archosaur ancestors (Zelenitsky et al., 2011). Yet, bird olfactory bulb size may be adapted to different ecological niches (Corfield et al., 2015), including long-distance travel: diverse bird species rely primarily on olfaction for orientation during migration and experimental displacement (Wallraff, 2005; Gagliardo, 2013; Holland et al., 2009; Wikelski et al., 2015). Air-borne odors can be stable across time and hence may offer unique value to navigators, as a long-distance sensory highway (Safi et al., 2016). This property of air-borne odors could lead to selection for olfactory navigation skills, even in highly visual and auditory species, such as birds and bipedal apes.

Stereo olfaction

Comparative studies can offer clues as to what properties of the human nose would support such olfactory navigation. A primary function would be stereo olfaction, or the spatial separation of paired sensors to increase the accuracy of directional orientation, similar to stereo audition (von Békésy, 1964). von Békésy's (1964) hypothesis has been supported by studies from a wide range of invertebrate and vertebrate species: honey bee (Apis mellifera) (Martin, 1965), desert ant (Cataglyphis fortis) (Steck et al., 2010), fruit fly (Drosophila melanogaster) (Borst and Heisenberg, 1982), terrestrial snail (Achatina fulica) (Chase and Croll, 1981), giant garden slug (Limax maximus) (Gelperin, 1974), blacktip shark (Carcharhinus limbatus) (Gardiner et al., 2015) and sharks in general (Gardiner and Atema, 2010), brown bullhead catfish (Ictalurus nebulosus) (Bardach et al., 1967; Johnsen and Teeter, 1980), the bifurcated tongue of snakes (Schwenk, 1994), laboratory rat (Rattus norvegicus) (Rajan et al., 2006; Khan et al., 2012), eastern American mole (Scalopus aquaticus) (Catania, 2013), domestic dog (Canis lupus familiaris) (Craven et al., 2010) and human (Porter et al., 2007). The manipulation of crossing the inputs also eliminates the ability to orient in space to odors, both in animals with antennae (Martin, 1965) and in those with nares (Catania, 2013).

The critical variable in stereo olfaction is the physical separation of the catchment areas in the fluid, whether air or water, in which odorants are suspended. Sensor mobility will be critical in determining the volume of fluid sampled and the separation of the catchment areas, with greater separation allowing for greater accuracy in orientation. For example, a honey bee with two fixed antennae oriented less accurately to an odor source than a bee with two mobile antennae (Martin, 1965). For vertebrates with nares, Stoddart (1979) proposed that the key variable may instead be the length and flexibility of the neck, suggesting this could explain why vertebrates with less flexible necks, such as salamanders, have more widely spaced nares. This increased nasal breadth would theoretically increase the separation of the samples and hence compensate for the lack of head mobility seen in vertebrates with less flexible necks (Stoddart, 1979). The same reasoning has been used to study the separation of nostrils in sharks such as the hammerhead shark, where computational models predict that this separation increases the shark's accuracy in directional orientation (Rygg et al., 2013; Gardiner and Atema, 2010).

A third principle that has been proposed to enhance stereo olfaction, in addition to using the movement of antenniform structures or increasing the spatial separation of the nares, is the addition of a tube-like vestibule to the nares. The use of tube noses to increase the accuracy of stereo olfaction was first proposed by Stoddart (1979) to explain the distribution of tube noses in several bat families (Vespertilionidae subfamilies Nyctimeninae and Murininae; also in Pteropodidae). A recent study of the physics of siphons offers direct support for Stoddart's (1979) hypothesis. When fluids are siphoned into a simple vertical tube, the size and separation of the catchment area are determined by the velocity of movement of the fluid and the height of the tube entrance from the bed on which it stands. The greater the distance between the bed and the siphon opening, the greater the spatial separation between the siphon and the catchment area from which the siphon draws in fluids. There is a further additive effect of fluid velocity, such that a tall tube, pulling in fluid at a higher velocity, will be sampling from areas that are farther apart than a siphon that is flush with the bed's surface or is pulling in fluids at a lower velocity (True and Crimaldi, 2017).

This result has important implications for understanding the adaptive significance of tube noses. A longer tube would therefore increase the spatial separation of odor samples, effectively increasing the distance between the sensors. Additionally, the further separation of these samples could be controlled by varying the intensity of the inhalation, which would increase the velocity of the fluid, further separate the catchment areas and thus further enhance stereo olfaction.

The hypothesis that a tube nose enhances stereo olfaction may explain the presence of this trait not only in bats but in birds. Tube-nosed seabirds (Procellariiformes), which include shearwaters and albatrosses, are well known for their ability to orient to odors, such as the krill metabolites that are odor proxies for the presence of prey (Nevitt, 2008). Tube-nosed seabirds are also thought to use olfaction to orient during long-distance movements over water, in the absence of proximal visual landmarks (Reynolds et al., 2015; Safi et al., 2016; Dell'Ariccia et al., 2014). In addition, the relative size of the olfactory bulbs is also larger in aquatic bird species (Corfield et al., 2015). It is therefore possible that the demands faced by these seabirds have led to the evolution of tube-like appendages to further separate catchment areas and thus enhance olfactory navigation accuracy.

It is interesting that tube noses have evolved in vertebrate taxa that have evolved powered flight; relatively larger olfactory bulbs are associated with increased space use in homing pigeons (Mehlhorn and Rehkämper, 2009), which navigate using odors (Wallraff, 2005). Mapping an odor gradient may be done more accurately with the greater number of samples possible over larger distances and hence may be more valuable in species using long-distance movements, such as flying insects and vertebrates (Jacobs and Menzel, 2014). But this logic might also apply to terrestrial vertebrates that cover large distances, e.g. cursorial vertebrates, such as carnivores and humans; relatively larger olfactory bulbs are also found in terrestrial carnivores that range over longer distances (Gittleman, 1991). If increases in space use are associated with an increased use of olfactory navigation, then this constraint may be relevant to the genus Homo, the first hominid to significantly increase space use and leave Africa (Antón et al., 2014). To answer this, we must first consider the question of the hominid nose in the context of other primates.

Olfaction in Homo

Perhaps external nose morphologies in primates, including Homo, can also be explained by the olfactory spatial hypothesis (Jacobs, 2012). As a catarrhine, the genus Homo is one of the least olfactory primates, yet it is the only primate to have evolved a large external nose. The only exception to this is the catarrhine proboscis monkey (Nasalis larvatus), but in this case the external nose is used by males in audiovisual communication and does not appear to be specialized for olfaction (Koda et al., 2018).

The human external nose shows several unique features (Figs 1 and 2). The external pyramid encloses generally inferior-orienting nares, a trait not found in other great apes. The pyramid encloses the nares within the alae nasi, the cartilaginous structures surrounding each naris, separated by a third structure, the columella, a protrusion between the two alae. No current hypothesis posits a respiratory function for the alae nasi or columella.

Yet, such structures could theoretically enhance olfaction, specifically stereo olfaction. It is a testable hypothesis that the alae nasi could act as tube noses, where a greater length of nasal vestibule would correspond with greater separation of the catchment areas of inspired air. The unique inferior orientation of the human nares, separated by the columella, might also further separate the geometry of the catchment areas during inspiration. Finally, the external pyramid itself could increase the distance between the nares and, to a greater extent than that seen in platyrrhine monkeys, could also enhance stereo olfaction. These predictions could be tested by measuring the effect of nasal metrics on a human's accuracy in orienting to an odor gradient. Using standard methods, it should be possible to measure the effect of nasal breadth on orientation accuracy to odors distributed in plumes. If supported, then the navigational nose hypothesis could then be used to address the remaining questions about the human external nose: why did it appear when it did and why did nasal breadth and height subsequently become so variable in modern humans?

Why did it evolve?

The external pyramid first appeared in Homo erectus (Franciscus and Trinkaus, 1988) (Fig. 6). Early Homo evolved in an increasingly unpredictable climate, with periods of great aridity, and forest habitats changing to grasslands (Antón et al., 2014). This change in climate and habitat structure led to selection in Homo for a suite of traits to increase bipedal locomotory efficiency, such as increased lower limb length, which allowed archaic humans to forage more economically for widely dispersed resources (Steudel-Numbers, 2006; Bramble and Lieberman, 2004; Kuhn et al., 2016; Antón et al., 2014; Antón, 2012; Lieberman, 2011).

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Fig. 6.

A reconstruction of Homo erectus. An early African Homo erectus, based on the skull KNM-ER 3733. Reproduced with permission from Gurche (2013).

Another major behavioral shift in Homo at this time was an increase in carnivory, a shift that brought the genus into direct competition with other mammalian carnivores (Churchill et al., 2016). Given this interspecific competition between humans and other African carnivores, it may be most fruitful to ask not what species humans are most closely related to but to which species they are most ecologically similar (Schaller and Lowther, 1969). Humans were competing not only with cursorial carnivores but also with olfactory specialists, species that used olfaction both to detect prey and to orient in space. Carnivory, space use and olfactory bulb size may be generally associated, as they are in terrestrial carnivores (Gittleman, 1986) and theropod dinosaurs (Zelenitsky et al., 2011, 2009); a similar association between carnivory, space use and olfaction may be seen in piscivorous birds (Wikelski et al., 2015) and sharks (Nosal et al., 2016).

Many African carnivores, such African lions (Panthera leo), wild dogs (Lycaon pictus) and spotted hyenas (Crocuta crocuta), are also highly social and hunt cooperatively (Smith et al., 2012). To compete in this environment, Homo sapiens also became, like their competitors, increasingly social, both hunting and breeding cooperatively (Hrdy, 2007). The ability to hunt cooperatively, even before the development of weaponry, changed many aspects of human socio-ecology. One behavior that may have evolved at this time is the use of endurance pursuit to capture large game (Carrier et al., 1984; Bramble and Lieberman, 2004). Endurance pursuit requires accurate spatial orientation, while tracking and returning to camp (Liebenberg, 2008). Such long-distance travel could also have selected for new navigational skills, such as olfactory navigation.

There are additional navigational costs of carnivory beyond prey search and handling. Carnivory carries with it a higher risk of foraging with zero return than does foraging for non-meat foods. Hence, a primary mechanism that has been shown to insure against such risk is to maintain large social networks for food sharing (Grove, 2009). In models of hunter–gatherer food sharing, greater cooperation and the elimination of free riders is supported primarily by increased mobility (Lewis et al., 2014). One of the true costs of carnivory may therefore be the need for cooperative hunting and a widely dispersed social network for food sharing, a behavior that would be made efficient with more accurate spatial navigation.

Thus, olfactory navigation in Homo could have represented an important new technical skill to increase the efficiency of space use. This, in turn, would have selected for mechanisms of stereo olfaction. It has also been proposed that it was these adaptations for increased mobility that allowed archaic humans to subsequently expand their species distribution (Kuhn et al., 2016); by 1.8 million years ago, Homo erectus had expanded out of Africa and become established in Georgia, Indonesia and possibly China (Antón et al., 2014).

Implications for sex differences

Both the conditioning hypothesis and the navigational hypothesis posit that the human external nose evolved as an adaptation for long-distance movement. Thus, both hypotheses are predicated on the same ecological demand: increased space use in an arid environment, necessitating efficient conditioning and efficient navigation. Individual differences in long-distance travel should therefore be reflected in nasal structure.

Although men generally have larger range sizes than women (Gaulin, 1992), women may also forage over long distances (Jones et al., 1994). Both may orient using odor and hence both could benefit from stereo olfaction. The advantage of stereo olfaction may operate at different spatial scales. In a landscape defined both by arrays of local landmarks and distant cues that supply compass directions, females weight proximal landmark cues more heavily than do males (Jacobs and Schenk, 2003; Chai and Jacobs, 2010; Bettis and Jacobs, 2013). But it is not clear at what scale stereo olfaction is most effective when tracking an odor plume; stereo olfaction is clearly important in close-range orientation to odors (Catania, 2013; Porter et al., 2007). Unlike a distant visual object that provides direction, plumes are not contiguous in space but are a collection of discrete filaments (Murlis et al., 1992). Thus, the local structure must be analyzed to deduce the global structure. In this light, stereo olfaction might be valuable for the analysis of both close and distant resources. The key factor is the added value of a second sensor, as has been recently demonstrated in an information theoretical model of optimal sampling for spatial orientation in an empirically measured odor plume (Boie et al., 2018). In short, the evolution of the external pyramid could have been equally adaptive for women building high-resolution maps of resources near the home base or men building low-resolution maps of distant resources.

The use of long-distance foraging by men, in particular endurance pursuit, may also explain sex differences in the relative size of the external and internal nose. In a sample of European-descent Americans, men had larger external noses, both absolutely and relative to body size, than did women (Holton et al., 2014). In a study using crania from diverse worldwide populations, males also had a relatively larger nasal chamber volume than women, including relative larger choanae, i.e. the posterior opening leading to the lungs (Bastir et al., 2011). The authors conclude that the larger internal chamber and choanae in males would allow a greater volume of air to be conditioned during exercise (Bastir et al., 2011). A similar sex difference in internal nose dimensions has been documented in imaging studies of German and Chinese adults, with men showing a relatively larger nasal aperture than women (Schlager and Rüdell, 2015).

Such sex differences in nose morphology could have arisen via sexual selection in males for enhanced respiration during long-distance travel. The choanae, for example, which are relatively larger in males, have a purely respiratory function (Bastir et al., 2011). Thus, while the original appearance of the external nose in Homo erectus may have been due to natural selection for increased space use in both sexes of the species, other nasal structures could have been shaped by sexual selection to enhance a male's ability to compete with other men, such as in endurance pursuit. Male hunting skill in hunter-gatherer societies can often be interpreted as a trait driven by female choice and may be the product of both natural selection for foraging and sexual selection for male–male competition (Hawkes and Bird, 2002).

Sexual selection for navigation might also explain patterns in olfactory bulb size. In a German sample, both absolute olfactory bulb size and olfactory function developed gradually between the ages of 6 and 17 (Hummel et al., 2011). It increased throughout adulthood to peak around age 40 and then declined in both women and men, although the absolute size of the olfactory bulb was consistently larger in men (Buschhüter et al., 2008). Forty is also the age at which mortality begins to increase in hunter–gatherers, peaking at a model adult death of 70 years (Gurven and Kaplan, 2007). Finally, olfactory bulb size is positively correlated with olfactory function (discrimination and threshold) in humans (Buschhüter et al., 2008; Hummel et al., 2011, 2013; Mazal et al., 2016; Seubert et al., 2013). This suite of characters in human males could be an adaptation for efficient foraging, a difference that might emerge at puberty and extend over the peak hunting years, where accurate spatial orientation to odors might be enhanced by a larger external nose, while the capacity for oxygen exchange would be increased by a larger internal nasal chamber and choanae.

In contrast, women might have evolved a different suite of olfactory specializations, in addition to the stereo olfaction afforded by an external nose. Women consistently outperform men on measures of odor identification, for both social and non-social odors (Doty and Cameron, 2009). In a cross-cultural study of Japanese, Italian and German participants, women more accurately identified the sex and individual identity of an axillary odor (Schleidt et al., 1981); in a study of American college students, women could more accurately identify their own axillary odor than could men (Platek et al., 2001). Thus, in social encounters, women may have access to more accurate olfactory information than men.

These sex differences could arise from sex differences in olfactory system plasticity. The olfactory system changes rapidly (e.g. within months) if given repeated exposures to an odor, even in humans that are initially anosmic to the odorant (e.g. androsterone) (Wysocki et al., 1989). Repeated exposures both decreased the threshold of detection and increased absolute olfactory bulb size in the subject (Haehner et al., 2008). Even when only one nostril is exposed to the odor, both olfactory bulbs increased 11–13% in volume after 4 months (Negoias et al., 2017). This effect of repeated exposure decreasing the threshold of detection for an odor is significantly stronger in women than in men (Dalton et al., 2002).

Therefore, experience-dependent sex differences in social experiences and hence olfactory exposure could lead to the observed female advantage in olfactory identification. These female advantages might also arise via sexual selection, in this case selection for enhanced social intelligence. This form of neural plasticity could also support related skills, such as tracking and mapping the distribution of other resources, e.g. food and medicinal plants, that could be identified most accurately by odor. Relevant to this, a new study has demonstrated that a human's ability to identify odors co-varies with their ability to learn landmark locations in a virtual environment. These cognitive skills also co-varied with the size and integrity of brain structures involved in both spatial navigation (right hippocampus) and olfaction (left orbitofrontal cortex) (Dahmani et al., 2018), in accordance with the olfactory spatial hypothesis (Jacobs, 2012). This tight relationship between olfaction and spatial memory could have evolved via selection for mapping resources via chemical cues.

The predictions of these proposed sex-specific specializations, whether long-distance travel in men or resource tracking in women, are amenable to empirical testing. Re-framing the human external nose as an olfactory structure could lead to new insights into human perception and brain plasticity and their modulation by natural and sexual selection.