Smell With Inspiration: The Evolutionary Significance of Olfaction
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YEARBOOK OF PHYSICAL ANTHROPOLOGY 53:63–74 (2010)
Smell With Inspiration: The Evolutionary
Significance of Olfaction
Kara C. Hoover*
Anthropology Department, University of Alaska Fairbanks, Fairbanks, AK 99775
KEY WORDS olfaction; evolutionary biology; evolutionary genetics; human variation;
genotype–phenotype
ABSTRACT The olfactory receptor gene family is the depression and quality of life issues, neurodegenerative
largest in the mammalian genome (and larger than any disorders, adult and childhood obesity, and decreased
other gene family in any other species), comprising 1% of nutrition in elderly females. Human pheromones, a con-
genes. Beginning with a genetic radiation in reptiles troversial subject, seem to be a natural phenomenon, with
roughly 200 million years ago, terrestrial vertebrates can a small number identified in clinical studies. The con-
detect millions of odorants. Each species has an olfactory sumer product industry (perfumes, food and beverage,
repertoire unique to the genetic makeup of that species. and pesticides) devotes billions of dollars each year sup-
The human olfactory repertoire is quite diverse. Contrary porting olfactory research in an effort to enhance product
to erroneously reported estimates, humans can detect mil- design and marketing. With so many intersecting areas of
lions of airborne odorants (volatiles) in quite small concen- research, anthropology has a tremendous contribution to
trations. We exhibit tremendous variation in our genes make to this growing body of work that crosses traditional
that control the receptors in our olfactory epithelium, and disciplinary lines and has a clear applied component.
this may relate to variation in cross-cultural perception of Also, anthropology could benefit from considering the
and preference for odors. With age, humans experience power of the olfactory system in memory, behavioral
differential olfactory dysfunction, with some odors and social cues, evolutionary history, mate choice, food
remaining strong and others becoming increasingly faint. decisions, and overall health. Yrbk Phys Anthropol 53:63–
Olfactory dysfunction has been pathologically linked to 74, 2010. V 2010 Wiley-Liss, Inc.
C
Smell is an involuntary ubiquitous sensation. Waking mean to humans? These are questions that are at the
or sleeping, eyes shut or open, we cannot help but smell heart of our discipline, and yet biological anthropologists
with inspiration. The other senses can be stopped man- have not engaged fully with the vastly expanding inter-
ually (closing the eyes or plugging the ears), but we can- disciplinary body of olfactory research.
not stop breathing; even mouth-breathing will impart a
weak sense of smell.
For most primates, smell certainly does not seem as CHEMOSENSING AND OLFACTION
evolutionarily significant as vision. Trichromatic vision
Chemosensing is phylogenetically the oldest sensory
is a derived trait, the result of retro-fitting duplicated
system, the first means of communication between
parts of the ancestral mammalian opsin gene family
organisms. The chemical senses include olfaction (smell),
into a third one to increase the richness of the color
field. Although not as rich a visual field as four-coned gustation (taste), and chemesthesis (pain, touch, and
therapsids (Cretaceous era mammalian ancestors), pri- thermal dermal sensations) (Finger et al., 2000). Terres-
mate trichromatic vision certainly had an impact on trial vertebrate animals distinguish between taste and
our evolutionary trajectory (Jacobs, 2009). The evolu- smell via different physical mediums and biological
tionary significance of vision (compared to olfaction) is structures. Odorants are airborne and detected via the
visible in a brief review of major anthropology journals nose. Tastes are water soluble and detected via the
(Table 1). mouth. In fishes, all chemosensing occurs in the water
Perhaps our discomfort with our longest serving verte- and is thus limited to water-soluble chemical stimuli,
brate sense stems from the pungency of odors generated eliminating a distinction between smell and taste. In all
by a mass of humans living in close quarters or the false animals, however, there is overlap in cerebral processing
notion that humans are microsmic (poor smellers able to of these chemosenses (Caprio and Derby, 2008).
perceive a limited number of odors). Nevertheless, our Even the most minimal chemosensing toolkit directs
fascination with odor and need to participate in the ol- an organism toward food and mates but away from
factory environment is as old as civilization, if not older threats (toxins and other organisms) (Van Houten,
(see Gilbert, 2008 for an excellent overview of human
olfaction). Beginning in the middle of the 18th Century,
however, westerners began to alter their smellscapes *Correspondence to: Kara C. Hoover, Anthropology Department,
University of Alaska Fairbanks, Fairbanks, Alaska 99775.
(Kleinschmidt, 1999), a trend that has continued today.
E-mail: kara.hoover@alaska.edu
On the one hand, modern humans take pleasure in
smelling, but on the other hand reject olfaction as DOI 10.1002/ajpa.21441
having an evolutionarily significant role. What is the Published online in Wiley Online Library
evolutionary significance of olfaction and what it might (wileyonlinelibrary.com).
C 2010
V WILEY-LISS, INC.64 K.C. HOOVER
TABLE 1. Brief review of key words in major anthropology journals
Journal of American American
Human Journal of Physical Journal of Human Current American
Key word Evolution Anthropology Biology Anthropology Anthropologist Total
Vision 111 16 14 8 102 251
Olfaction/smell 49 5 0 61 2 117
2000). Differential adaptation to environmental chal- cortex are connected directly via the first cranial nerve
lenges is reflected in the variation of olfactory strategies (the olfactory nerve), which runs through the lateral ol-
across phylogenetically diverse species. Each species is factory tract. The lateral olfactory tract is exposed to the
fine-tuned to recognize a range of chemical signals rela- environment via the nasal passages and interacts
tive to its own evolutionary ecology. Despite this adapt- directly with inhaled air (Langdon, 2005). Olfaction truly
ive variation, basic olfactory anatomy has been con- is an environmental probe; a direct link between the
served across 500 million years of vertebrate evolution brain and the environment without intermediate proc-
(Stoddart, 1980; Dahanukar et al., 2005; Menashe and essing (e.g., unlike the skin linked to the brain via the
Lancet, 2006) and consists of two independent compo- intermediary of the spinal cord or the sense of taste gen-
nents: the main olfactory system for detecting chemical erated in taste buds, which are not neural sensory cells).
compounds (odorants) and the accessory olfactory system Mammalian olfaction is processed in the limbic area of
for detecting chemical communications from other ani- the brain where emotion and memory are stored. This
mals (often referred to as pheromones) (Zufall and creates a unique interplay among the three. Perhaps the
Leinders-Zufall, 2008). In a recent review, Munger and most interesting part of this arrangement is that mam-
coworkers (2009) argue that each olfactory subsystem mals react to an odor before thinking about it. So, to
(main and accessory) is not exclusively devoted to a spe- revisit the orange example, the individual will be experi-
cific stimulus (respectively, odorants and pheromones). encing negative emotions because of the past association
of being sick and smelling orange before the frontal lobe
Main olfactory system perceives the scent as ‘‘orange.’’ For humans, our com-
plex cultural context adds perhaps a third layer of odor
There are two parts to the main olfactory system. First, processing, abstract contemplation of scent, or sensation.
the main olfactory system detects odorants in the nasal Sensation is part of the lived cultural experience, a com-
cavity and sends those data to the brain. Odor detection is plex web of individual experience mediated by and nego-
simply the process of chemical compounds being ‘‘recog- tiated through culture (but that is beyond the scope of
nized’’ by specific receptor cells in the nasal cavity. Second, this review and for cultural anthropologists to contem-
the cerebrum perceives the odorant. Perception is much plate).
more complex than detection because it involves memory
and emotion in the identification of an odor (e.g., orange Accessory olfactory system
odor is detected, memories of orange-flavored medicine
are retrieved, and negative emotional state is awakened). The accessory olfactory system detects chemical com-
munication between animals (pheromones). A rigorous
Odor detection. The first part of the process, odor definition of pheromones would be a chemical signal
detection, begins in the nasal cavity. The nasal cavity is between organisms of the same species that communi-
lined with olfactory epithelium containing olfactory sen- cates mutually beneficial information on the state of one
sory neuron cells that produce receptor proteins. Embed- individual to another (e.g., a female in estrus or men-
ded in the cellular plasma membrane, these receptors arche) (Meredith, 2001). A less-rigorous definition would
await the arrival of appropriate ligands (in this case, an be a chemical signal released by one organism to another
odorant) capable of binding to the receptor. The attrac- that evokes a reaction (e.g., behavioral response or infor-
tion between receptor and ligand is based on molecular mation receipt). This simpler definition would allow
shape (though some argument [Turin, 1996] has been inclusion of female menstrual cycling and cross-species
made for molecular vibration). Once the ligand has communication (Wysocki and Preti, 2004). Most verte-
attached, the biochemical pathway is initiated. The olfac- brate pheromone detection takes place primarily in the
tory receptor response spreads through the cell, initiat- vomeronasal organ (Buck, 2000). The vomeronasal organ
ing impulses in the olfactory neuron. Olfactory neuronal houses sensory neurons and the accessory olfactory bulb
axons converge in the olfactory bulb (paired structures that processes input (similar to the olfactory bulb)
the size of a pea). In humans, the olfactory bulb is (Zufall and Leinders-Zufall, 2008).
located underneath the frontal lobe and directly above
the olfactory epithelium. In most non-human verte-
EARLY VERTEBRATES AND FISH
brates, the olfactory bulb is located in the foremost part
of the brain. Initial signal organization and processing Biology
take place in the olfactory bulb before information is
transmitted to the olfactory cortex of the cerebrum, Vertebrate olfaction began in an aquatic environment
where odor perception takes place (Buck, 2000). where water is the medium for odorants. Fishes are spe-
cialists in water-soluble odorant detection (amino acids,
Odor perception. The second part of the process, odor bile acids, sex steroids, and prostaglandins). There are
perception, occurs in the cerebrum, which is unusual more water-soluble odorants than volatile. A plethora of
because the other senses are processed by the thalamus. evidence confirms greater fish olfactory acuity in detect-
Olfactory receptor cells are actually olfactory sensory ing and discriminating odorants compared with other
neurons, which is perhaps the source of this unique neu- vertebrates (Hara, 1975, 1994; Laberge and Hara, 2001).
robiology of olfaction. The olfactory bulb and olfactory Despite this greater acuity, the active odorant detection
Yearbook of Physical AnthropologyHUMAN OLFACTION 65
space is constrained in the water because the diffusion a model for pheromone detection without a vomeronasal
of odorants is 10,000 times slower than in air. Fishes organ. Recall that a fish sensory epithelium contains
have responded to this environmental challenge variably. three types of sensory cells, two of which respond to
Some remain immobile and pump local water through social cues and sex pheromones (Hamdani and Døving,
the olfactory system using cilia or muscles, waiting for 2007). Given the slow diffusion of odorants through
the currents to bring the odorant to them. Others water, having one type of cell dedicated to odorants and
increase their active odorant detection space by swim- two types dedicated to conspecific chemical communica-
ming through the water to the odors (Rosenthal and tion makes evolutionary sense.
Lobel, 2006). Fishes use pheromones primarily to medicate social
The long evolutionary lifespan of fishes has led to a behavior: predator avoidance and social and reproductive
great diversity of olfactory organs. Contrast the keen cues. Different species of fishes have different antipreda-
ability of predatory sharks and eels who detect even tion pheromones. Some may release chemical cues that
extremely diffuse odorants to the relatively poor olfac- provoke a physiological change (e.g., increase in body
tory ability of the pike (Hara, 1975). As an evolutionarily depth in carp) or evasion (in response to the odor of dead
older class of animals, fishes have primitive or ancestral conspecifics or predators who have eaten conspecifics).
olfactory receptor genes but exhibit wide variation in Other chemical signals (perhaps bile acids or L-amino
these genes between individuals and species (Niimura acids) allow fish to identify kin (e.g., fish schools), aggre-
and Nei, 2005; Shi and Zhang, 2009). Regardless of vari- gate as a species, or to migrate. Specific sex-related phero-
ation in olfactory acuity, all fishes smell by moving water mones (steroids and prostaglandins) allow fishes to distin-
through the nares (nostril-like structures). Fish nares guish between males (male–male aggression) and females
(even in lunged fishes) bypass the pharynx, leading (mating) and to spawn (Sorensen and Stacey, 2004).
instead to the olfactory rosette lined with sensory epithe-
lium containing three types of sensory cells, one of which EARLY TETRAPODS, AMPHIBIANS, AND
responds to odorants whereas the other two respond to REPTILES
social cues and sex pheromones (Hamdani and Døving,
2007). After detection, information from the receptor cell Biology
is conveyed to the olfactory bulb. The earliest four-limbed animals (tetrapods) were
aquatic before they made the initial transition to land.
Genetics Modern amphibians begin life in the water and finish on
the land (though some return to the water as adults).
The evolution of vertebrate olfactory receptor genes This dual adaptation allowed early tetrapods (and mod-
follows the expected pattern of three separate evolution- ern amphibians) to reap the benefits of resources in both
ary lineages: fishes, amphibians, and mammals (Niimura environments. As such, amphibians have olfactory
and Nei, 2005). Fishes retain the greatest number of an- organs and genes specialized for detecting both volatiles
cestral olfactory receptor gene lineages (eight of nine), and water-soluble odorants. In water, odorants are
but the smallest number of olfactory receptor genes detected in a manner similar to fishes: the nasal cavity
(100); still, this limited set of genes has the greatest is flooded with water via the respiratory pump (Reiss
amount of variation in all major classes of animals and Eisthen, 2008).
reflecting a longer evolutionary history (Fuchs et al., On land, amphibians and some reptiles engage in
2001; Glusman et al., 2001). Birds and mammals retain gular pumping or pulse ventilation (essentially swallow-
the smallest number of gene lineages (two) but greatest ing air) to establish olfactory contact with the surround-
number of genes (1,000). Indeed, olfactory receptor ing medium (Jorgensen, 2000). During buccopharyngeal
genes are the largest mammalian gene family. The evo- ventilation, the mandible moves upward (with the mouth
lutionary intermediary, amphibians, retains gene fami- closed) pushing the maxilla cranially and compressing
lies common to both fishes and mammals (but share the nostrils. Oscillatory throat movements then force air
more with mammals) (Freitag et al., 1998). into the lungs (Stebbins and Cohen, 1995). Respiratory
Shi and Zhang (2009) conducted a phylogenetic analy- function is secondary and achieved via diffusion through
sis of the vertebrate olfactory receptor family and found thin membranes (Langdon, 2005). In other amphibians
two main types of olfactory receptor genes that were dis- and reptiles (chelonians, crocodiles, and some lizards),
tinct early in vertebrate history. Niimura and Nei (2005) the ribs take on the suction function of the pharynx, cre-
found five Class I and one Class II genes common to ating a sort of air pump (Langdon, 2005). Many reptiles
both fishes and tetrapods. Specialization of these genes and some amphibians must alternate breathing with
to a particular medium is implied in the common associ- movement during locomotion because of the interference
ation of Class I genes with fishes and water-soluble odor- of lateral trunk flexion in rib suction pumping. This pre-
ants and Class II genes with mammals and airborne cludes smelling during locomotion. Thus, many reptiles
(volatile) odorants (Niimura and Nei, 2006). Unfortu- and amphibians are like motionless fishes, waiting for
nately, mammals also have active Class I genes (humans odorants to come to them.
retain 100), which makes this distinction murkier
(Freitag et al., 1998; Collin, 2007).
Genetics
Pheromones Roughly 200 million years ago, an olfactory receptor
gene radiation occurred, coinciding with the time of rep-
Most vertebrates use the vomeronasal organ for phero- tile dominance (Fuchs et al., 2001). This genetic radiation
mone detection, but fishes lack this organ (along with suggests a major adaptive shift and/or speciation event at
modern adult humans). Yet, fishes use pheromones to this time, likely related to the terrestrial environment.
communicate regularly and indeed have vomeronasal An order of fishes commonly called coelacanths are
organ-related genes (Niimura and Nei, 2006). Fishes are thought to represent a transitional state between fishes
Yearbook of Physical Anthropology66 K.C. HOOVER
and tetrapods because they possess leg-like structures. a richer olfactory experience (Gilbert, 2008). Evidence of
Known originally from fossils, there are two living spe- these bones first appears in Early Cretaceous fossils
cies left (Janvier, 2007). One species, Latimeria chalum- associated with the order Therapsida from which mam-
nae is particularly relevant to a discussion on the evolu- mals descend. There is some debate as to whether ther-
tion of olfaction. L. chalumnae share a class of olfactory apsid turbinates served only respiratory or respiratory
receptor genes with amphibians and mammals but not and olfactory functions (Kemp, 2006).
other fishes (Freitag et al., 1998). When odorant-bearing air enters the nasal cavity, odor
As discussed earlier, Class I olfactory receptor genes molecules bind to the olfactory receptors and initiate a
are commonly associated with water-soluble odorant chain of biochemical events that ultimately transmit in-
detection and Class II olfactory receptor genes with vola- formation to the olfactory bulb (Wolfe et al., 2009). The
tile odorant detection. Indeed, Class II olfactory receptor olfactory epithelium contains roughly 20 million olfac-
genes in both L. chalumnae and aquatic mammals (such tory sensory neurons, the dendrites of which end in ol-
as the dolphin Stenella coeruleoalba) are nonfunctional factory receptors and the axons of which pass through
(pseudogenes). A secondary class of olfactory receptor the cribiform plate and bundle into the olfactory nerve.
genes evolved in early prototetrapods that underwent At this point, the nerve enters the olfactory bulb. Den-
selective pressure in tetrapods. These olfactory genes drites connect olfactory sensory neurons to mitral and
then became pseudogenized (accumulating enough muta- tufted cells, which together form structures called glo-
tions to render them nonfunctional) in mammals that meruli (Mackay-Sim and Royet, 2006; Wolfe et al., 2009).
returned to the sea. What the original function of these Extrapolating from comparative anatomy, the limited
genes in coelacanths was and why they were pseudogen- number of human olfactory sensory neurons should
ized remain to be answered. Were they under selective result in roughly 700 glomeruli. Recent research indi-
pressure in coelacanths, or did these Class II olfactory cates that humans have roughly 6,000 glomeruli, three
receptor genes take on a new function in terrestrial ver- times that of a mouse for one-third the neurons (Maresh
tebrate olfaction (Collin, 2007)? Indeed, the frequency of et al., 2008), suggesting a much more complex mecha-
duplication and gene loss in vertebrate evolutionary his- nism before the odor signal is sent to the brain for addi-
tory points to adaptive processes in functional variation tional processing.
across divergent lineages (Shi and Zhang, 2009). Odor signals from the olfactory bulb are processed in
the limbic system of the brain (primary olfactory cortex,
Pheromones amygdala–hippocampal complex, and entorhinal cortex).
The primary functions of the limbic system are emotion,
Although amphibians detect odorants in a similar learning, and memory; hence, the emotionally evocative
manner to fishes (which is slightly modified on land), the quality of odors. Even though the detection and sensa-
detection of pheromones is altogether different. Unlike tion of odor is slower than the other senses, olfaction is
fishes, most amphibians detect pheromones via the vom- unique among the senses in that olfactory sensory neu-
eronasal organ (often through the mouth) but there are rons are the foremost projection of the mammalian
a few exceptions: the lungless salamander breathes and brain; in essence, the olfactory system is the only biologi-
detects pheromones in the external environment through cal structure in which the brain sends its neurons into
its skin, the caelicians (an order of amphibians that the environment like a probe. (Although taste is a sense
resembles earthworms) through a tentacle that is located that interacts directly with the environment, taste recep-
between the eye and nostril (Freitag et al., 1998), and tor cells are not neurons.)
snakes (reptiles) via tongue flicks.
There are two distinct families of receptors associated
with the vomeronasal organ in most tetrapods (Niimura
and Nei, 2006). Sensory neurons in the vomeronasal Genetics
organ (unlike those in the olfactory epithelium) termi- Mammalian olfactory genetics are divergent from the
nate in the accessory olfactory bulb, from where informa- vertebrate lineage in the sheer size of the olfactory re-
tion is carried to the limbic system of the brain (Freitag ceptor gene family. This gene family comprises 1% of the
et al., 1998) and appropriate behavioral responses are active genome and is the largest gene family identified
initiated (e.g., move to food, move away from predator, across all species (Buck, 2000). Thus, mammals may be
or mate). evidence of a second adaptive radiation (after the reptil-
ian olfactory radiation 200 million years ago). Mamma-
MAMMALS lian olfactory receptor genes are located on most chromo-
Biology somes with a tendency to cluster near chromosome ends,
or telomeres (Fuchs et al., 2001). Telomeres serve as
Mammals are unlike other vertebrate tetrapods in chromosomal caps that conserve the integrity of DNA
that they use an organ (the nose) to detect volatile odors. during cell division. Recombination (or reshuffling of ho-
The nose has a primary function during respiration to mologous chromosomal DNA) is more frequent toward
warm and humidify the air prior to oxygenating the the telomeres (Jobling et al., 2004). Recombination can
lungs. One of the distinctive features in the evolution of result in gene duplication. Thus, these telomeric loci
mammals is the appearance of nasal turbinates (scroll- may be artifacts of an olfactory receptor gene expansion
shaped spongy bones in the nasal passages of verte- wherein individual genes or genomic segments were
brates), which have two functions. Turbinates warm the duplicated rapidly (Fuchs et al., 2001). In mammals, the
air before its entering the lungs but also push some of overall biological olfactory apparati and genes are con-
the inhaled air cranially through the olfactory cleft into served—even in those species that returned to water.
the olfactory epithelium (Hillenius, 1992; Hillenius and Even though the human olfactory receptor gene family
Ruben, 2004). This biological innovation enables retro- contains fewer active genes compared with other mam-
nasal smelling, creating with taste the flavor of food and mals, it is still large and complex (Table 2). For a review
Yearbook of Physical AnthropologyHUMAN OLFACTION 67
TABLE 2. Known human olfactory receptor genes, psuedogenes, pared with pseudogenes and introns. They also found
and single-nucleotide polymorphisms (compiled from HORDE; high nonsynonymous substitution rates in OR genes and
Oleander et al., 2004) a small but significant overall reduction in variability in
Chromosome Genes Pseudogenes SNPs the entire OR gene cluster compared with other genomic
regions. They argue that these variations are the result of
1 63 32 309 weak positive selection acting on human nucleotide diver-
2 2 9 6
3 10 21 39 sity.
4 – 11 – In another single nucleotide polymorphism (SNP)
5 4 4 9 study on chromosome 17, Menashe and coworkers (2002)
6 16 21 87 investigated 71 SNPs (31 newly identified in this
7 15 21 45 research and 43 confirmed from previous research) in 12
8 1 11 0 coding regions and three introns along in a 400-kb olfac-
9 25 14 128 tory receptor gene cluster. Their data revealed signifi-
10 1 7 3 cant differences between four geographically and cultur-
11 170 205 854
ally distinct human populations (Pygmies, Bedouins,
12 17 24 65
13 – 8 –
Yemenite, and Ashkenazi Jews), which they propose
14 23 22 152 form the basis for future genotype–phenotype studies
15 5 13 21 using this genomic area. Although they recognize that
16 2 1 9 drift may be operating in these isolated populations,
17 14 4 71 their findings of greater functionality in pygmy olfactory
18 2 2 – receptor genes and population-specific variation in pseu-
19 20 21 102 dogenization may reflect the evolution of differential ol-
20 – – – factory repertoires.
21 – 3 – Alonso and coworkers (2008) surveyed 3 million SNPs in
22 1 – 6
23 (X) 1 11 3
the HapMap database in four populations (60 Nigerian
23 (Y) – – – Yorubans, 45 Japanese from Tokyo, 45 Beijing Han Chi-
Total 392 465 1909 nese, and 60 unrelated individuals from Utah). They found
that heterozygotes dominate significantly (exceeding
Hardy–Weinberg limits on frequency of a trait not under
of the human olfactory subgenome (genes and their genomic the force of selection or drift). They argue (but do not test)
environment), see Glusman and coworkers (2001). that this could be heterozygote selection as those individu-
Results from previous studies examining human olfac- als have double the number of odorant binding sites in the
tory diversity indicate high olfactory receptor gene varia- genome compared with homozygotes. They further suggest
tion between individuals, sexes, and within and between that, if this is selection, it could actually be an evolutionary
populations (Firestein, 2001; Menashe et al., 2002, 2003; response to human olfactory receptor loss.
Zhang and Firestein, 2002; Gilad and Lancet, 2003;
Menashe and Lancet, 2006; Zhang et al., 2007; Moreno- Copy number variation. In a microarray study on 851
Estrada et al., 2008). Some researchers (Gilad et al., olfactory receptor genes and pseudogenes using a sample
2003b; Menashe et al., 2003; Menashe and Lancet, 2006) of 25 individuals from three populations (European,
have suggested that adaptation has influenced patterns Asian, and Nigeria/Yoruba), Hasin and coworkers (2008)
of genetic variation within the olfactory gene family, found several interesting results. Copy number varia-
including weakly expressed pseudogenes. Yet, despite its tions are higher in pseudogenes than in intact genes.
evolutionary significance and ongoing adaptive function, Derived olfactory receptor genes (after the human–chim-
very little is understood about the genetic basis of varia- panzee split) in both species were affected significantly
tion in odor perception, let alone the evolutionary con- more by copy number variation than conserved olfactory
text of this variation and its role in phenotypic expres- receptor genes (those with one-to-one orthologs between
sion and behavior. species). Lastly, they found that deletion alleles for copy
Humans exhibit high interindividual variation in ol- number variations are human-derived and suggest these
factory receptor genes and pseudogenes, and some might be used in future phenotype–genotype smell per-
research has indicated the existence of variation in cul- ception studies. Unfortunately, the authors of this study
tural and geographically distinct populations (e.g., did not address the presence of possible variation
between Africans and non-Africans and Ashkenazi and between the three human population samples.
Sephardic Jews) (Gilad and Lancet, 2003; Menashe and Genes. Gilad and coworkers (2003a,b) suggest that most
Lancet, 2006; Menashe et al., 2003; Zhang et al., 2007). human olfactory receptor genes exhibit little evidence of
Although these may be the result of bottlenecks and evolutionary constraint and some have important func-
geographic isolation, selection and cultural practices tions that are shared with apes. They further argue that
may all serve to conserve olfactory receptor genes a subset of olfactory receptor genes were under positive
(Menashe and Lancet, 2006; Menashe et al., 2003). This selection in humans, and some are still undergoing posi-
has yet to be studied with robust sample sizes from vari- tive selection.
ous geographically distributed populations within the Gilad and Lancet (2003) resequenced 32 single-disrup-
context of each one’s geohistorical context. tion pseudogenes belonging to 14 olfactory receptor gene
clusters in two population groups (pygmies and Euro-
Single nucleotide polymorphisms. Gilad and co- peans). They find higher frequencies of derived genes in
workers (2000) report population sequence diversity of seven Europeans (two Ashkenazi Jews and five Euro-
genomic segments in a 450-kb cluster of olfactory receptor peans, whose national origin were not identified in the
genes on human chromosome 17. They found a lower ratio published literature) but lower diversity of genes and
of nucleotide diversity to divergence in intact genes com- few rare alleles compared with the seven pygmies. They
Yearbook of Physical Anthropology68 K.C. HOOVER
argue that the derived genes and lower diversity in RNA, but not translated into protein) in the olfactory ep-
Europeans may be a signature of recent (and perhaps ithelium and may share neurons with active olfactory re-
still active) purifying selection following a population ceptor genes. (Oddly, they also found that many olfactory
bottleneck (e.g., genetic drift). receptor genes are expressed in nonolfactory tissues, but
In a brief communication to Nature Genetics, Menashe did not find evidence of these genes having secondary
and coworkers (2003) genotyped 189 individuals with functions in these tissues.)
varying ethnic backgrounds and found 178 different
functional genomes. Only the human leukocyte antigen
system (the human major histocompatibility complex) Pheromones
has such interindividual variation in the genome. In addition to the large olfactory receptor gene family,
A caveat in interpreting these results is the generally there are two others: V1R (35 genes) and V2R (150
small sample sizes. With such small sample sizes, statis- genes) (Buck, 2000; Liberles and Buck, 2006). These
tical power is lost. A large-enough effect must first be gene families belong to the accessory olfactory system.
established to warrant general conclusions from a small The sticky wicket with human pheromones is that many
sample size. humans (3%) do not have the vomeronasal organ,
A counter argument to the possibility of positive selec- thought to be necessary for pheromone detection
tion in human olfactory receptor genes was presented by (Keverne, 1982; Meredith, 2001). Lack of a vomernasal
Gimelbrant and coworkers (2004). Looking at the evolu- organ, however, does not preclude pheromone detection;
tionary genetics of humans since the human–chimp diver- fishes lack the organ but are expert pheromone senders
gence and using the recently sequenced chimp genome, and receivers. Wysocki and Preti (2004) suggest that the
they find only evidence for weak purifying selection, olfactory neuroepithelium has taken on the task of the
which they argue is expected given the shrinking number vomeronasal organ.
of olfactory receptor genes in both species. This comple- There are four types of pheromones: primer, signaler,
ments the findings of Gilad and Lancet (2003) who found modulator, and releaser (Wysocki and Preti, 2004). Each
a signature of genetic drift in European populations for one is a chemical cue that provides information on
the pseudogenes they resequenced. A caveat in comparing behavior and emotional state. If the less-rigorous defini-
this study with the others that find significant variation, tion of a pheromone (e.g., chemical signals between two
however, is the parameters of this study, which is genomic organisms that provide information or evoke a response)
and interspecies. Nevertheless, their findings do suggest is applied to humans, there is evidence that humans
whatever effect might be present in studies using only use all four types of pheromones. Some work quickly
human DNA, this is lost in an interspecies study. (releaser) and some work more slowly (primer).
Moreno-Estrada and coworkers (2008) found signa- Primer pheromones are associated with endocrine and
tures of positive selection in OR511, an olfactory receptor reproductive physiology (Meredith, 2001; Wysocki and
gene shared with chimpanzees, which is noted for an Preti, 2004). McClintock’s (1971) famous study on men-
excess of amino acid replacement mutations. The strual cycling found that women living together (in her
research group used the Human Genome Diversity Cell study, a dorm) synchronize around a driver female. Phero-
Line, which contains over 1,000 DNA samples from indi- monal cues in other species accelerate or retard ovulation
viduals from 39 geographically and/or ethnically distinct onset. Wysocki and Preti (2004) review the brief literature
populations. This is the first anthropological genetics on this phenomenon in humans noting that lactating
study using such populations relative to olfactory recep- women may increase variation in menstrual cycling and
tor genes and has great potential to open the field to evo- male hormones may increase sexual receptivity.
lutionary questions. They argue that the variation Signaler pheromones may or may not elicit a response,
between human populations pre-dates human population simply acting to communicate information (e.g., ‘‘we are
expansion out of Africa and is mildly selective. kin’’ or ‘‘I am good to mate with’’). In humans, the most
likely candidate for a signaler pheromone is our major
Pseudogenes. Diurnal primates with trichromatic color histocompatibility complex, the human leukocyte antigen
vision tend to have an increased number of inactive (or system. The human leukocyte antigen system plays a
pseudogenized) olfactory receptor genes (Niimura and major role in interindividual variation in natural body
Nei, 2003; Go and Niimura, 2008). Although not as impov- odor (Santos et al., 2005), and certain olfactory receptor
erished as our ocean-dwelling mammalian relatives (most genes are indeed linked to human leukocyte antigen
of whose olfactory receptor genes are redundant), humans genes (Ehlers et al., 2000). This odor print allows for kin
also have a great number of redundancies. Although recognition (primarily between mother and child), biolog-
humans have the basic mammalian olfactory genetic ical sex differentiation, possibly sexual orientation, social
package, many of the genes are pseudogenized (Niimura rank (e.g., dominance), and mating compatibility for
and Nei, 2003; Zhang et al., 2007; Go and Niimura, 2008). increased reproductive success (Wysocki and Preti,
There are 10 million olfactory neurons, and more than 2004). For mating success, the inference is that body
half the olfactory receptor genes (600) in the olfactory odor is an olfactory signal for the immune system.
gene family are pseudogenes. Within the human species, Reproductive fitness is enhanced by children surviving
however, there is variation in the extent of pseudogeniza- to reproductive age, and survival rates increase with
tion. Results from three studies indicate greater diversity stronger more diverse immune systems. Thus, mating
in the pseudogenes of pygmy populations compared with with someone who has a differing immune system will
non-African populations (Menashe et al., 2002, 2003; enhance the offspring’s chance of survival (and increase
Gilad and Lancet, 2003). These researchers argue this net reproductive success). Indeed, Setchell and co-
variation in olfactory repertoires is a signature of past ev- workers (2010) found an association between mate
olutionary pressure. choice, major histocompatibility complex genetic diver-
Zhang and coworkers (2007) found that olfactory re- sity, and increased reproductive success in a group of
ceptor pseudogenes may be expressed (transcribed into semi-free-ranging male mandrills: the effect was strong
Yearbook of Physical AnthropologyHUMAN OLFACTION 69
enough to overcome the role of male dominance in repro- olfaction by non-human primates (even those with dichro-
ductive success. matic and trichromatic vision) when encountering new
Modulator pheromones are used for mood and emotion foods. This suggests that olfaction plays an overlooked but
modification. A few studies (reviewed in Wyscoki and Preti, significant role in regulating primate behavior, which has
2004) show that humans are sensitive to mood odors. Spe- evolutionary significance in human prehistory.
cifically, humans are able to smell fear. Subjects watching a Humans also show substantial variability in their per-
scary film left an odor behind that was detectable to new ception of odors (Gilbert and Wysocki, 1987; Lancet et al.,
subjects entering the room (the control was a comedy film), 1993; Menashe and Lancet, 2006; Keller et al., 2007). In
who then responded to the odor. This is reminiscent of the one case, genetic variability in OR7D4 (an olfactory recep-
alarm signals used by fishes. Another example is the effect tor gene) is associated with different perceptual responses
of androstenone on females. Both males and females to androstenone (Keller et al., 2007). Secreted by the
secrete androstenone (a steroid) in sweat, but males secrete gonads of male pigs, androstenone was first noted as a sex
far greater concentrations of it and are less sensitive to it. pheromone when this steroid stimulated lordosis in
Female subjects in clinical trials showed increased focus female sows. Humans also emit the steroid in sweat
and a sensation of being relaxed when exposed to the smell (males to a greater order of magnitude than females
(via the upper lip). These are two examples of how a chemi- [Wysocki and Preti, 2004]). Androstenone is variously
cal emitted by one human indicates the emotional state of described as either sour/urine or vanilla/musk/floral.
another and/or evokes a behavioral/emotional response in Roughly 60% of adults can detect this chemical (Wysocki
the receiver rapidly. et al., 1989). Long purported to have a genetic component
Releaser pheromones are signals meant to elicit an im- (Wysocki and Beauchamp, 1984), androstenone pheno-
mediate behavioral response and are associated with typic sensitivity is now linked to underlying genetic varia-
sexual attraction. In humans, our strongest evidence of tion in two SNPs in linkage disequilibrium in the olfactory
releaser pheromones are in infants’ responses to moth- receptor gene OR7D4 (Keller et al., 2007). The case of
er’s breast odor (Varendi and Porter, 2001). But, sexual androstenone is frustrating. Keller and coworkers (2007)
attraction may indeed have a pheromonal component to argue that smellers and nonsmellers of androstenone are
it. Thus, the possibility remains that humans are uncon- distinguished by genotype. However, some nonsmellers
sciously responding either physiologically or behaviorally can become sensitive to androstenone after repeated test-
to chemical signals. ing whereas other nonsmellers cannot (Wysocki et al.,
1989). Males produce more androstenone, but their sensi-
tivity to it decreases around adolescence, suggesting a de-
THE HUMAN OLFACTORY REPERTOIRE velopmental component (Wysocki and Gilbert, 1989).
Olfactory repertoires, the array of odors perceivable by Women may lose sensitivity in some cases but in others
an organism, vary between and within species. What is the gain sensitivity (Wysocki and Beauchamp, 1991). Children
human olfactory repertoire and how extensive is it? The find the smell unpleasant, whereas some adults will note
oft-cited figure of 10,000 odorants detectable by humans is a hedonic quality to it. Although there is clearly a genetic
incorrect. Avery Gilbert (2008) tracked down the source of component (Wysocki and Beauchamp, 1984; Wysocki et
this number and found it was an estimate (based on false al., 1989; Keller et al., 2007; Keller and Vosshall, 2007),
assumptions) made by a chemical engineer and cited in an the change in sensitivity thresholds and the ability to
article in 1954 by researchers from a consulting company, become sensitized to it suggest a more complex interaction
Arthur D. Little, Inc. Somehow, this number became fixed, with developmental changes and a certain amount of plas-
even among some researchers who study olfaction! ticity in ability to learn to detect the odor.
The human olfactory repertoire is quite large. Despite In another genotype–phenotype study, Menashe and co-
the varying strategies to get odorants to the olfactory ep- workers (2007) found a clear association between SNP dis-
ithelium, terrestrial animals share the capacity to detect ruptions to the olfactory receptor gene OR11H7P and
odorants that meet certain criteria. Detectable volatile detection thresholds for isovaleric acid (which has a smell
odorants (with a vapor pressure above 0.01 mm Hg) are similar to human sweat). This is a clear case of genetic
water repellent (hydrophobic) with a weak polar region, mutations causing hyperosmia (enhanced detection sensi-
and are small/light (molecular weights up to but less tivity) to a particular odor. Another intriguing finding is
than 300 Da or 5.8 3 10222 g) (Silver and Walker, 1997; that the sample of individuals screened for this study were
Wolfe et al., 2009, p 331). more hyperosmic than hyposmic, suggesting that perhaps
Although humans do not have as low an odor concentra- there is a larger genomic effect of decreased odor detection
tion detection threshold as other animals (e.g., dogs), we thresholds downstream of olfactory receptor genes.
can actually track odors quite well using only our noses. Knaapila and coworkers (2008) assessed the contribu-
Porter and coworkers (2007) had humans follow a ten me- tions of genetics and environment to perception variation
ter long chocolate-scented trail and found that 66% of the (intensity and pleasantness) in several odors: cinnamon,
subjects were able to follow the trail successfully and that chocolate, turpentine, and isovaleric acid. These odors
internostril comparison increased success as each nostril were selected because previous studies suggested there
was able to track a 3.5 cm region separate from the other might be a genetic component to variation in their detec-
nostril. With nose plugs, no one could follow the trail. Fur- tion and/or perception. The sample consisted of 856
thermore, tracking speed doubled after practice and sub- twins (83 monozygotic pairs and 275 dizygotic pairs)
jects ventured off-trail fewer times. The authors of the between the ages of 10 and 60 years, with a fairly even
study argue that human olfaction ultimately has a greater male to female percentage ratio (44:56). Twins were
inherent ability than typically conferred and that the mis- recruited from Australia, Denmark, and Finland. Age
apprehension of human olfactory acuity perhaps lies more was modestly correlated with intensity ratings, and
with behavioral demands rather than actual ability. there were no sex variations between countries. They
A growing body of evidence (Laska et al., 2000; Dominy found that the genetic component explained 18% of the
et al., 2001; Hiramatsu et al., 2009) points to the use of total variation, and the most important factor was non-
Yearbook of Physical Anthropology70 K.C. HOOVER
shared environmental effects (e.g., individual exposure common). Medical practitioners tend to overlook smell-
and learning to the odor perception and preferences). loss complaints, which often remain undiagnosed. Even if
The authors suggest that some odorants are detected by diagnosed, medical practitioners rarely take the matter
a limited number of receptors and more susceptible to further. Even though we do not think about it actively,
genetic effects, whereas other odorants are detectable by smell is central to our lives. We use it to taste our food
multiple receptors and free from genetic polymorphisms (with the help of taste receptors), alert us to dangers
associated with specific anomias (odor desensitivity). (including bad food), and trigger memories. Thus, without
Humans even exhibit tremendous cultural variation in smell, basic functions are greatly impaired.
olfactory stimuli and value (Airkem Inc., 1952; Gilbert There are many other olfactory disorders that affect the
and Wysocki, 1987; Classen, 1990, 1992, 1993, 1994, sense of smell. Environmental sensitivity (also called multi-
1999; Pandya, 1990, 1993, 2007; Stoddart, 1990;Lancet ple chemical sensitivity), although possibly impacting the
et al., 1993; Zimmer, 2002; Menashe et al., 2003; Drob- sense of smell, is not an olfactory disorder. This syndrome is
nik, 2006; Menashe and Lancet, 2006; Keller and Vos- poorly understood and has been described mainly via symp-
shall, 2007; Keller et al., 2007; Moreno-Estrada et al., toms reported to clinicians. The triggers may be inhaled or-
2008). Classen (1993) reviews odor-related culture-bound ganic and inorganic chemical compounds (with or without
olfactory values. For instance, the Dassanetch of Ethio- odor) such as pollens, cleaning solutions, and molds. Other
pia believe that local environments create human odor. triggers have nothing to do with olfaction (such as ingested
For these cattle-herders, the species of cattle determines foods and radiation). The symptoms for some may include
the odor of the herder. The Ongee of the Andaman perceived increased sensitivity to odors, but not all individu-
Islands believe all living beings are made of pure smell. als experience this sensation (instead they may experience
A lack of smell is death. Bodily scents diffused during muscle fatigue, irregular heartbeat, urinary problems, con-
the day are collected and returned to the body by a spirit stipation, or heartburn to name a few) (Das-Munshi, et al.
who lives in our bones (pure smell) and renews life. Lost 2006). Results of clinical studies comparing self-reported
scents are carried on the wind and attract hungry spi- afflicted and unafflicted individuals indicate no differences
rits. The Ongee have many cultural rituals to control in perceptual ability between groups, further suggesting
odor but take the precaution of seasonally migrating this is a cognitive processing issue rather than an actual
between the forest and sea (timed by the changing direc- sensory one. Gilbert (2008) reports that the AMA renamed
tion of the winds) to minimize their scent being caught this syndrome ‘‘idiopathic environmental intolerance’’
by the spirits. Lastly, the Tukano-speaking tribes in Co- because there is no known etiology or physiological compo-
lumbia each have specific odors (fish for one, roots for nent yet identified. Thus, this is not specifically an olfactory
another). Odors form the basis on which tribal identity disorder, even if there is an olfactory component.
is constructed. Olfactory boundaries create a sense of
place or territory. This idea of identity and smell is also Neurodegenerative disorders. Doty and coworkers
common cross-culturally. When the Japanese encoun- (1984) found that all humans experience a gradual loss of
tered the Europeans after roughly 100 years of seclusion, olfactory acuity between the decades of 30 and 50 followed
they called the Europeans ‘‘smells like butter.’’ by a sharp decline after 70. Oddly, the gradual decline is
specific to certain odors. The smell of rose and banana
remain strong, but other smells fade—quite often the
APPLIED OLFACTORY RESEARCH
unpleasant ones, which is why the elderly are often less
In addition to the elucidation of the evolutionary ori- sensitive to unpleasant odors (Gilbert, 2008). Current
gins, functioning, and neuronal process of vertebrate efforts are underway to increase sensitivity in clinical prac-
olfaction, there are practical applications of the research. tice to older patients who complain of smell loss. Up to 50%
Clinical outcomes of understanding this sensory system of individuals aged over 65 years, however, experience a
contribute to understanding and possibly treating neuro- complete loss of olfactory ability (Murphy et al., 2003).
degenerative disorders, obesity, and individuals with Abnormally decreased sensitivity to odor and partial anos-
impaired olfaction. Practical and profitable outcomes of ol- mias are early warning signs of neurodegenerative disor-
factory studies contribute to the consumer industry (per- ders (Muller et al., 2002; Doty, 2003; Getchell et al., 2003;
fumes, food, beverage, cleaning supplies, and pesticides). Smutzer et al., 2003; Haehner et al., 2007; Wilson et al.,
2007). Individuals diagnosed as anosmic or partially anos-
Biomedicine mic can be assessed for risk of neurodegeneration. The link
between these disorders and anosmia is unclear.
Olfactory disorders. Anosmia (complete olfactory dys-
fucntion), partial anosmia (odorant-specific insensitivity), Nutrition and obesity. An emerging focus in childhood
hyposmia (generally reduced olfactory ability), parosmia obesity (and potential predictor of adult obesity) is the
(olfactory dysfunction resulting in perception of all smells relationship between chronic ear infections (very com-
as unpleasant), and phantosmia (olfactory hallucinations, mon in our society) and diet. The destruction of the ol-
often unpleasant) are quality of life problems. Common factory epithelium that occurs during sinus infections
complaints include problems cooking, mood changes, (often associated with middle ear infections) leaves the
decreased appetite, eating spoilt food, body odor, sexual afflicted with a diminished sense of smell. Thus, taste is
dysfunction, and lack of awareness of dangerous toxins accomplished through taste receptors (limited to five or
(Nimmemark, 2004; Hummel and Nordin, 2005). Anosmia six distinct sensations) whereas flavor (accomplished
and hyposmia are more common and may have links to through both taste and smell receptors) is reduced. The
obesity (Richardson et al., 2004; Hummel and Nordin, reduced ‘‘taste’’ of their food may draw the afflicted to-
2005). The National Institute on Deafness and Other ward richer, fattier foods (Tanasescu et al., 2000; Scal-
Communications Disorders reports on their Website that fani, 2001; Snyder et al., 2001, 2003a,b; Richardson et
1–2% of North Americans self-report a smell disorder of al., 2004; Chapo et al., 2005; Bartoshuk et al., 2006).
some kind. This debilitating condition has variable etiolo- Indeed, recent research suggests a connection between
gies (head trauma and neurodegeneration being the most obesity and food preferences relative to olfactory varia-
Yearbook of Physical AnthropologyHUMAN OLFACTION 71
tion and ability (Obrebowski et al., 2000; Bartoshuk et Food and beverage. Food and beverage companies
al., 2006; Duffy, 2007). thrive on signature scents and flavors (the intersection
Interestingly, the connection between smell loss and a of scent and taste). The wine industry alone sells itself
preference for less nutrition foods seems quite often in el- on terroir, the scent and taste of the land where the
derly females. An increased appetite for sweet and/or fatty grapes were grown. The idea that one product alone can
things is common with elderly females who experience a taste and smell a certain way because it comes from a
loss of olfactory ability (Duffy et al., 1995). Although this specific geographic location is powerful to the consumer
does not correlate significantly with weight gain (or loss), marketing industry.
decreased nutrition is a problem. And, loss of smell in el-
derly is often associated with anorexia. With enhanced fla-
vor, food becomes interesting to the individual, and the SUMMARY
anorexia goes into remission (Gilbert, 2008). Olfaction is the oldest evolutionary sense. The origins of
Another area of increasing interest is the purported olfaction lie in the water. Smelling provided the earliest
functional role of developmental and epigenetic condi- marine organisms with a means of getting food to their
tioning (often pointed to as an underlying behavioral mouths, finding mates, and avoiding predators. The odor-
cause of obesity via fetal/developmental programming). ant-rich and vast marine niche has generated more vari-
Schaal and coworkers (2000) suggest that there is an ele- ety in olfactory structures and greater olfactory acuity in
ment of fetal programming to odor preference in new- fishes over the course of millions of years of evolution
borns. Anise is not a common spice used in France, but (especially in comparison with much younger classes of
his group found that the newborn children of women vertebrates like mammals, amphibians, and birds). One
using anise during pregnancy reacted positively or neu- drawback to water-soluble odorants is the relatively slow
trally to the scent of anise compared with the negative diffusion rate compared with volatiles. Amphibians
responses from those whose mothers did not consume it. occupy both water and terrestrial niches (usually starting
The suggestion that a mother may biologically influence in the one and finishing in the other). As such, they have
a child’s odor instincts during pregnancy (and perhaps evolved unusual respiratory and olfaction structures (e.g.,
afterward) is intriguing given the genetic variation in swallowing air) that allow them to exploit both environ-
the human olfactory repertoire. Clearly, there is a syner- ments. Mammals are fully adapted to the terrestrial niche
gistic dynamic between genes, biology, and culture. and are capable of smelling any hydrophobic volatile with
a low molecular weight.
Taste and smell industry The complexity of the olfactory gene family in verte-
The ethnographic data pointing to cultural variation in brates is evidenced by the multiple ancestral gene fami-
olfaction and experimental data pointing to variation in lies seen in fishes. Amphibians bear the evidence of their
perception–behavior relationships (Airkem Inc., 1952; Gil- hybrid olfactory ability in the maintenance of genes for
bert and Wysocki, 1987; Classen, 1990, 1992, 1993, 1994, water and airborne scents (emphasizing the volatiles).
1999; Pandya, 1990, 1993, 2007; Zimmer, 2002) suggest Mammals have taken to volatiles, expanding the olfac-
that the taste and smell industry could be making more tory gene family from roughly 100 genes in fishes to
individually tailored chemical compounds for its clients roughly 1,000 in extant mammals. Olfactory genes are
(who in turn produce foods, cleaning products, perfumes, the largest gene family in the mammalian genome (or
etc.). A clearer understanding of the interaction between any species’ genome for that matter). Primates with tri-
genes and odor perception has the potential to impact the chromatic vision have many redundant genes in this
taste and smell consumer product industry in terms of family. Humans have extended this redundancy such
product development and demographic marketing. that we only have roughly 400 active genes left (though
variation between geographically distinct human groups
Antiperspirants. A certain amount of olfactory research suggests significant intraspecies variation in olfactory
is fueled by a billion dollar industry, deodorants and pseudogenes). Despite the loss of active olfactory genes,
antiperspirants. Givaudon has made large contributions humans may be experiencing positive selection for het-
to our understanding of the components of human sweat erozygotes, perhaps maintaining a diversity of receptor
(and their variation between males and females) cells. In other words, we might be compensating for gene
(Wysocki and Preti, 2004). loss in other ways or have derived a specialized geneti-
cally compact efficient system of olfaction.
Pesticides. The pesticide industry thrives on research
Another aspect of olfaction is pheromones, which ena-
related to pheromones. These studies are used to create
ble organisms to communicate via chemical secretions.
artificial versions of pheromones that will lure common
Pheromones are used by all species. Even humans are
pests to a trap where they will be killed. There is a
subject to the forces of pheromonal communication. A
growing industry in human pheromones (particularly
chemical communication may send information on the
androstenone), as sex (releaser) pheromones, but there is
emotional status of an individual (‘‘I’m afraid’’) or may
no scientific evidence to support this marketing. Plus,
elicit a specific response (sexual arousal). In the former
marketing a smelly component of human sweat as a sex
situation, the receiver may then respond by increasing
pheromone counter the billion dollar antiperspirant and
alertness to danger. In the latter, the receiver is aroused.
deodorant industry!
In fishes and humans, there is no vomeronasal organ,
Perfumes. Perfume is another area of applied olfactory but amphibians, reptiles, and other mammals use vom-
research. Scent preferences vary cross-culturally, and the eronasal organ as the primary method of detecting pher-
perfume industry could better capitalize on this by knowing omones. In fishes and humans, the receptors lie in the
their demographic. A related industry, cleaning products, olfactory epithelium.
also capitalizes on olfactory research. Knowing which prod- Aside from the academic study of olfaction in biology,
ucts produce calming effects or awakening effects can better genetics, neurobiology, and anatomy/physiology, there
inform the selection of shower and personal cosmetic scents. are many practical applications of olfactory research.
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