Integrative and Comparative Biology
Integrative and Comparative Biology, volume 55, number 3, pp. 507–517
doi:10.1093/icb/icv058
Society for Integrative and Comparative Biology
SYMPOSIUM
Reception of Aversive Taste
Blair E. Lunceford* and Julia Kubanek1,*,†
*School of Chemistry and Biochemistry, Aquatic Chemical Ecology Center, Institute for Bioengineering and Biosciences,
Georgia Institute of Technology, 311 Ferst Drive, Atlanta, GA 30332, USA; †School of Biology, Aquatic Chemical Ecology
Center, Institute for Bioengineering and Biosciences, Georgia Institute of Technology, 311 Ferst Drive, Atlanta, GA 30332,
USA
From the symposium ‘‘Chemicals that Organize Ecology: Towards a Greater Integration of Chemoreception,
Neuroscience, Organismal Biology, and Chemical Ecology’’ presented at the annual meeting of the Society for Integrative
and Comparative Biology, January 3–7, 2015 at West Palm Beach, Florida.
1
E-mail: [email protected]
Synopsis Many organisms encounter noxious or unpalatable compounds in their diets. Thus, a robust reception-system
for aversive taste is necessary for an individual’s survival; however, mechanisms for perceiving aversive taste vary among
organisms. Possession of a system sensitive to aversive taste allows for recognition of a vast array of noxious molecules via
membrane-bound receptors, co-receptors, and ion channels. These receptor–ligand interactions trigger signal transduction
pathways resulting in activation of nerves and in neural processing, which in turn dictates behavior, including rejection of
the noxious item. The impacts of these molecular processes on behavior differ among species, and these differences have
impacts at the ecosystem level by driving feeding-behavior, organization of communities, and ultimately, speciation. For
example, when comparing mammalian carnivores and herbivores, it is not surprising that herbivores that encounter a
variety of toxic plants in their diets express a larger number of aversive taste receptors than carnivores. Comparing the
molecular mechanisms and ecological consequences of aversive-taste reception among organisms in a variety of types of
ecosystems and ecological niches will illuminate the role of taste in ecology and evolution.
Introduction
Identifying nutritious components in food such as
sugars and amino acids is essential for the survival
of most consumers. Just as important is the need to
identify potential harmful compounds. To do this,
organisms rely primarily on the sense of taste,
which is one of a few types of chemoreception. In
humans, taste or gustation is the sense by which
molecules activate receptors within taste buds, transmitting a neural signal (Chaudhari and Roper 2010).
However, the anatomy and sensitivity of taste receptors, as well as the identity of tastant compounds,
differ among organisms (Liman et al. 2014). In the
context of this review, taste is simply the contact
chemosensation of molecules located in a food
source by a consumer. When the taste of a compound produces rejection by an individual that compound is said to be aversive and the reception of
such tastes is termed ‘‘aversive taste reception’’. In
humans, bitter and sour taste modalities function as
an aversive taste reception mechanism; however,
other organisms have different physiological organizations for aversive taste. The purpose of this review
is to compare the components that make up aversive
taste among different groups of organisms: those
aversive molecules and the respective receptors that
activate signal-transduction pathways resulting in
neural processing and rejection, and which affect
ecosystems and feeding ecology. Due to the extensive
amount of studies done on this subject, this review is
not meant to be comprehensive of all organisms or
cases in which aversive chemosensory pathways have
been studied. Instead, this review seeks to highlight
key examples in different organisms and habitats as
well as the disparity of knowledge of aversive chemoreception between terrestrial and aquatic habitats.
This comparative approach allows generalizations
among sensory types to be made across phylogenic
and habitat boundaries.
Advanced Access publication May 28, 2015
ß The Author 2015. Published by Oxford University Press on behalf of the Society for Integrative and Comparative Biology. All rights reserved.
For permissions please email: [email protected].
508
Ligands and receptors
Aversive compounds in food act as ligands, binding
and activating a consumer’s receptor proteins at the
moment the consumer contacts food. These aversive
ligands produced or sequestered in prey vary widely
in structure and origin, and there is significant interspecific and intraspecific variation in the types and
quantities of deterrent compounds produced (Speed
et al. 2012). Similarly, the receptors in predators that
identify these compounds also vary in structure,
from G-protein-coupled receptors (GPCRs) that amplify signals to transient receptor potential (TRP)
channels that are permeable to cations, to co-receptors (small membrane-bound proteins) that modify
the activity of their larger counterparts (Liman et al.
2014). Thus, there appears to be a coevolutionary
arms race occurring between prey that chemically
deter predators from feeding and predators that
identify and avoid these potentially toxic compounds. This molecular interplay between organisms
drives feeding behavior and community ecology, as
discussed in a later section.
Ligands
Sour and bitter tastes both are aversive to mammals,
and are mediated by different types of compounds.
Unlike sour taste, which senses low pH alone (Liman
et al. 2014), bitter taste senses multiple structural
classes that make up aversive ligands. Denatonium
benzoate and quinine, in addition to other wellstudied bitter ligands, bind receptors of bitterness
and are aversive to many animals, including mammals, birds, fish, and insects (Belitz and Wieser 1985;
Skelhorn and Rowe 2006; Glendinning 2007; Oike
et al. 2007; Weiss et al. 2011). In addition, some
sessile organisms from disparate environments produce the same aversive compounds, as in the case of
the sesquiterpene dialdehyde polygodial, which is
produced by terrestrial plants, freshwater macrophytes, marine sponges, and molluscs (Long and
Hay 2006). This points to the fact that many organisms across varying habitats, most commonly those
organisms that are soft-bodied, slow-moving, or sessile, have evolved production of, or association with,
aversive compounds as a defense against predators
(Freeland and Janzen 1974; Pawlik 1993).
Plants and marine algae produce an array of secondary metabolites, some of which are unpalatable
to herbivores (Hay and Steinberg 1992; Wittstock
and Gershenzon 2002). Some notable examples of
plant-derived toxic compounds include alkaloids,
such as caffeine and colchicine, and cyanogenic glycosides, such as amygdalin, which are found in
B. E. Lunceford and J. Kubanek
almonds and apricots (Meyerhof 2005). Among the
green and red macroalgae in marine systems, terpenes play analogous roles both as activated (rapidly
produced upon perturbation by an external stimulus) and as constitutive (produced all the time) defenses, e.g., the diterpene trialdehyde halimedatrial
produced by algae in the genus Halimeda (Paul
and Fenical 1983), and the acyclic diterpene chlorodesmin produced by Chlorodesmis fastigiata (Paul
et al. 1990). Although it was initially hypothesized
that the bitterness of a substance reflects its toxicity,
a sizeable proportion of bitter compounds appear to
be harmless at typical doses, while still inducing a
negative reaction by consumers (Glendinning 1994).
Many plant secondary metabolites function as deterrents of feeding without being toxic at low doses,
including phenylpropanoid-derived natural products
produced by Micranthemum umbrosum that deter
crayfish from feeding (Lane and Kubanek 2006),
and phlorotannins from brown algae that are induced chemical defenses (produced minutes to days
after a perturbation by an external stimulus) against
gastropods and other consumers (Pavia and Toth
2000). The iridoid glycosides, a class of aversive compounds made by plants such as Plantago lanceolata
deter herbivorous insects (Biere et al. 2004). These
molecules also function as toxins to microbial invaders, indicating multiple defensive roles (Biere
et al. 2004). In addition, positive effects on health
can result from the ingestion of some bitter compounds, such as plants’ tannins that exhibit antioxidant properties and carotenoids that decrease the
risk of macular degeneration in humans (BarrattFornell and Drewnowski 2002). In some of these
cases, plants are slightly ahead of their consumers
in the evolutionary arms race if consumers have
not evolved the machinery to distinguish between
toxic and non-toxic aversive compounds.
Soft-bodied, sessile, or slow-moving marine organisms such as sponges, molluscs, cnidarians, ascidians,
and echinoderms produce a vast array of chemical
defenses, or associate with microorganisms that produce these compounds (Puglisi et al. 2014). In one
study, 69% of extracts from 71 species of Caribbean
sponges were shown to be deterrent to a generalist
coral-reef fish, Thalassoma bifasciatum, in laboratory
feeding assays (Pawlik et al. 1995). Sponges’ chemical
defenses have been widely studied, and belong to
structural classes including terpenes, polyketides,
brominated alkaloids, and saponins (Puglisi et al.
2014). The antifeedant properties of a specific
group of saponins, the triterpene glycosides, have
been characterized in addition to their other defensive roles (Kubanek et al. 2000, 2002). Echinoderms
Reception of aversive taste
such as sea stars and sea cucumbers also contain
terpene glycoside antifeedant compounds (Bryan
et al. 1997), whereas cnidarians such as soft corals
and sea fans produce deterrent terpenes and prostaglandins (Puglisi et al. 2014).
Some marine organisms such as nudibranchs and
sea hares sequester aversive compounds such as terpenes and alkaloids from the sponges and algae they
consume, in turn using them as a chemical defense
(Pawlik 1993). Herbivorous sea slugs known as ascoglossans sequester algal diterpenoid feeding-deterrents from the green algae they consume (Paul and
Van Alstyne 1988). Butter clams of the genus
Saxidomus sequester paralytic shellfish toxins like
the alkaloid saxitoxin from planktonic dinoflagellates
(Pawlik 1993). Some terrestrial organisms also sequester toxins. For example, many species of insects,
including monarch butterflies, aphids, leaf beetles,
and grasshoppers sequester cardenolides, a class of
terpene glycosides, from plants, and these toxins
cause the insects to be unpalatable to predators
(Brower et al. 1968; Agrawal et al. 2012).
In addition, microbes are hypothesized to produce
aversive chemicals that deter animals from a
common food source (Janzen 1977). Microbes that
colonize carrion produce deterrent molecules such as
fatty acids that cause aversion in animals (Burkepile
et al. 2006). This confers an advantage to the microbial competitors over the vertebrate consumers
(Ruxton et al. 2014).
To better understand what structural features of a
molecule cause a ligand to be perceived as bitter,
several databases of bitter compounds have been
constructed (Rodgers et al. 2005; Wiener et al.
2012). These databases only take into account
bitter molecules that are sensed by humans, but
one of them, BitterDB, has the ability to compare
ligands that are bitter to other species to those ligands that are bitter to humans (Wiener et al. 2012).
This is a powerful tool in the comparative study of
perception of aversive tastes.
Receptors
Aversive compounds from prey have been studied
and structurally identified over the past century,
but the receptors for these ligands were not studied
in detail until the recent advent of genomesequencing. The mammalian receptors of bitter
tastes (TAS2Rs) were among the first receptors of
aversive tastes to be identified (Adler et al. 2000;
Chandrashekar et al. 2000). These receptors are
GPCRs that most resemble Class I ‘‘rhodopsin-like’’
GPCRs (Adler et al. 2000; Chaudhari and Roper
509
2010). Thus, they contain short, extracellular N termini, do not contain introns, and their putative
ligand-binding sites are located inside the transmembrane helices (Floriano et al. 2006). Many heterologous studies of these TAS2Rs have linked known
receptors to their respective ligands (Chandrashekar
et al. 2000; Behrens et al. 2004; Kuhn et al. 2004;
Pronin et al. 2004) such as salicin and other bglucopyranosides, which bind to the human
TAS2R16 receptor (Bufe et al. 2002). These receptors
seem to be conserved in vertebrates, with TAS2Rs
described in bats (Zhou et al. 2009), fish (Ishimaru
et al. 2005; Oike et al. 2007), birds (Davis et al.
2010), reptiles, and amphibians (Li and Zhang
2013). In addition, a putative single transmembrane
co-receptor involved in the reception of aversive tastes,
which couples to an unknown endogenous GPCR, has
been described in fish, suggesting an alternate mechanism for taste-reception (Cohen et al. 2010).
In contrast to vertebrates, insects utilize gustatory
receptors (Grs) in their perception of taste (Clyne
et al. 2000). Although Grs contain seven helices
and are embedded in the membrane, they are unrelated to GPCRs and have an inverted membrane topology relative to GPCRs (Zhang et al. 2011; Xu
et al. 2012). Exactly how Grs function isn’t clear,
but they may form ion channels (Sato et al. 2011).
Insects also utilize co-receptors in the perception of
bitter taste, which alter the ligand-specificity of Grs
and thus allow insects to identify a large number of
bitter tastants via a relatively small number of receptors (Moon et al. 2009; Lee et al. 2010; Weiss et al.
2011). The involvement of co-receptors in the mechanisms of aversive taste reception, both of vertebrates
and invertebrates, suggests a wider role for these proteins than originally thought.
Insects and vertebrates also express ion channels
that can function as aversive taste receptors. Ion
channels are proposed to function in sour taste
(i.e., identification of low pH) in mammals and
Drosophila; however, no candidate ion channel or
receptor has been conclusively shown to function
in sour taste (Liman et al. 2014). Not much is
known about the mechanisms of sour taste and
thus it is an open area of research. In addition to
low pH, many mammals are deterred by the vanilloid compound capsaicin, found in chili peppers
(Jordt and Julius 2002). Capsaicin binds to a TRP
ion channel involved in the perception of heat, thus
causing the sensation of ‘‘hot’’ or ‘‘spicy’’ (Jordt
et al. 2003). Insects also sense aversive compounds
via TRP channels. The TRPA1 channel in Drosophila
detects aristolochic acid, an unusual nitro-containing
aromatic compound that is bitter and carcinogenic
510
to humans (Kim et al. 2010). Other TRP channels in
insects sense isothiocyanates (Al-Anzi et al. 2006),
which are found in wasabi, horseradish, and mustard, as well as camphor (Zhang et al. 2013b),
which is found in various trees from Southeast
Asia and is used as an insect repellent. Also, several
members of the ionotropic receptor-family function
in gustation in Drosophila (Koh et al. 2014), suggesting that insects rely more on ion channels for taste
than vertebrates do.
Bacteria have receptors analogous to taste receptors that are involved in chemotaxis. These receptors
operate in a two-component system that, upon encountering a negative stimulus such as a toxic compound, cause bacteria to move their flagella in a
random motion, physically distancing them from
the threat (Porter et al. 2011).
Taste signal transduction and neural
processing
For perception of aversive taste to occur, an organism needs to identify an aversive ligand via a binding
event with one of its taste receptors. The binding of a
ligand to its receptor triggers a signaling event that
includes amplification of the signal in the case of
GPCRs and results in a neuronal signal sent to the
central nervous system (Chandrashekar et al. 2006).
Signaling pathways and neural processing vary
among organisms, as does the anatomy of taste receptors (Liman et al. 2014). Because mammals (specifically mice and humans) and Drosophila are the
most well-studied organisms with regard to taste,
their specific mechanisms are the focus of this
section.
Anatomy of taste receptors
In mammals, taste receptors, including TAS2Rs, are
expressed in taste receptor cells (TRCs), which are
modified epithelial cells arranged in groups called
taste buds and are located throughout the tongue
and mouth. Each TRC encodes receptors for only
one type of taste (e.g., salty, sweet, sour, bitter, or
umami), and within each taste bud there are different types of TRCs such that all modalities of taste are
represented (Yarmolinsky et al. 2009; Voigt et al.
2012). Receptors are expressed on the surface of
the TRC that is exposed to the mouth cavity,
which is referred to as the taste pore. Neurons are
located adjacent to the TRCs within the taste bud,
and carry signals to the central nervous system
(Simon et al. 2006).
In contrast to mammals, insects express Grs in
gustatory receptor neurons (GRNs) that are located
B. E. Lunceford and J. Kubanek
in sensilla thoughout the body, including on the
wings, legs, proboscis, and labellum (Yarmolinsky
et al. 2009). Each sensillum contains two to four
GRNs of which one is a bitter-sensing GRN (Weiss
et al. 2011). In Drosophila, there are four types of
bitter-sensing GRNs, reflecting the number of Grs
they contain: two types of GRN contain a small
number of Grs and are narrowly tuned to bitter
stimuli, whereas the other two types of GRN contain
a large number of Grs and are broadly tuned to
bitter stimuli (Weiss et al. 2011).
In addition to traditional taste organs, receptors
for bitter taste have been found in non-gustatory
tissues such as the gut, both in mammals and in
insects (Wu et al. 2002). These may function as a
second line of defense against potentially noxious
compounds, identifying aversive ligands that may
have been missed or are part of the enteric nervous
system, and functioning in learned aversion to food
that produces sickness (Behrens and Meyerhof 2011;
Vegezzi et al. 2014). In mammals, receptors of bitter
taste are also found in the lungs, potentially identifying harmful compounds in the air (Zhang et al.
2013a). As insects contain GRNs on their legs and
wings, the Grs expressed within those body parts
have functions beyond reception of taste, such as
mate-selection and oviposition (Briscoe et al. 2013;
Liman et al. 2014). Thus, there are systems beyond
taste in which bitter receptors function.
Signal transduction
The first step in signal transduction of bitter taste in
mammals is a binding event between a ligand and its
respective GPCR. This binding event takes place
within the membrane domain of the protein and
causes a conformational change in the receptor
(Singh et al. 2011). The conformational change induces the phosphatidylinositol signaling pathway that
ultimately results in a release of ATP as a neurotransmitter, which excites afferent neurons surrounding
the TRCs in the taste bud (Zhang et al. 2003;
Taruno et al. 2013).
In contrast, not much is known about insects’
signal-transduction mechanism for reception of aversive taste. There is evidence of G-protein signaling
pathways in the GRNs of Drosophila; however, as the
Grs of insects are strikingly different from GPCRs,
they may not function similarly (Kim et al. 2010;
Devambez et al. 2013). There is also evidence that
Grs may function as ionotropic receptors (Sato et al.
2011).
Understanding how insects’ Grs function would
have a great impact on studies of comparative
Reception of aversive taste
chemosensation, especially given that they require a
co-receptor to function. The recent discovery of a
co-receptor involved in the reception of aversive
tastes in fish (Cohen et al. 2010), as well as evidence
of functional oligomerization of mammalian receptors of bitter taste (Kuhn et al. 2010), raises the
question of how prevalent co-receptors are in gustation. In addition, exploring how structure–function
relationships differ between Grs and GPCRs would
give insight into signal transduction in general,
which has implications in fields beyond taste and
ecology, including medicine and pharmacology.
Neural processing
For taste, the output of a signal-transduction event
resulting from binding of aversive ligands is a signal
sent to the central nervous system. In mammals, the
sensory signal is carried by the vagus, glossopharyngeal, and facial nerves to the rostral solitary nucleus
in the brainstem (Chaudhari and Roper 2010). In
Drosophila, taste neurons project to the subesophageal ganglion (SOG), which is located in the ventral
brain (Weiss et al. 2011). There is some debate as to
how taste is coded in the central nervous system.
One model, termed the ‘‘labeled-line,’’ suggests that
a sensory signal for bitter taste would end at the
‘‘bitter’’ processing area in the brain, a sensory
signal for sour would end at the ‘‘sour’’ processing
area in the brain, and so on for each modality of
taste (Liman et al. 2014). Another model suggests a
combinatorial processing method in which a combination of sensory signals results in each specific sensation (Chaudhari and Roper 2010). There is
evidence for both coding strategies both in mammals
and in Drosophila, and a recent study has given
strong support for the labeled line system in mammals (Barretto et al. 2015). Nevertheless, taste, as
sensed through the nervous system is ultimately connected to the behavior of the organism.
Organismal behavior and community
effects
The signal transduction and neural processing of
aversive taste at the molecular scale results in
changes in behavior affecting the whole organism.
This change in behavior comprises innate rejection
of ‘‘deterrent food’’, the initial reaction of an organism consuming an aversive food (e.g., nausea and
vomiting) and learned aversion to a specific noxious
food. In addition, these changes in the behavior of
individuals can result in cascading community-wide
effects, such as the formation of refuges and the protection of species diversity.
511
Organismal behavior: innate and learned aversion
The initial reaction of an organism to an aversive
ligand in their food is focused on rejection of that
food. In humans, this rejection of bitter substances
includes gaping, nausea, and lowered heart rate
(Glendinning 1994; Peyrot des Gachons et al.
2011). Crustaceans have been observed to push
away noxious food (Wight et al. 1990) and birds
shake their heads after being exposed to deterrent
food (Skelhorn and Rowe 2009). Fish expel aversive
food within a second of sampling it with their
mouths (Pawlik et al. 1995), and insects retract
their proboscis when sampling an aversive food
(Yarmolinsky et al. 2009). These are all innate actions aimed at avoiding ingestion of the aversive
compound. In fact, as tasting a bitter substance induces nausea in humans and other mammals, bitter
taste may cause an aversive anticipatory response in
order to protect the body from toxins (Peyrot des
Gachons et al. 2011).
In addition to the innate behavior associated with
the rejection of bitter substances, many organisms,
including birds, snakes, insects, and crustaceans exhibit learned aversion to ingested food that produces
sickness (Burghardt et al. 1973; Lee and Bernays
1988; Wight et al. 1990; Glendinning 2007;
Skelhorn and Rowe 2009). Aposematism, or conspicuous coloration of organisms that contain toxins, is
related to the bitter taste of that organism (Rowland
et al. 2013). Learned and unlearned aversion to aposematic prey has been described extensively in birds,
and birds can associate the level of bitter taste in
their food with its resulting level of toxicosis
(Skelhorn and Rowe 2010; Rowland et al. 2013).
This allows birds to make decisions about feeding
based on the prey’s toxicity, thus affecting foraging
behavior (Skelhorn and Rowe 2010).
Fish also exhibit learned aversion to noxious prey,
which affects their foraging behavior (Crossland
2001; Warburton 2003; Long and Hay 2006).
Multiple species of fish have been shown to learn
aversion in different ways. For example, Fundulus
heteroclitus, the mummichog, learned to avoid food
containing a nudibranch’s defensive chemical, polygodial, by detecting that compound in its food, while
another generalist fish, Chasmodes bosquianus, the
striped blenny, learned to avoid food containing
polygodial by refusing all food that tasted like the
food’s matrix (squid) (Long and Hay 2006). This
difference in type of learned aversion can be directly
translated into a difference in fitness costs, as the
striped blenny had reduced fitness compared with
the mummichog because it refused all food tasting
512
like squid, even food not treated with polygodial,
and thereby limiting its food options (Long and
Hay 2006).
However, there are some organisms, particularly
specialists, which fail to learn aversions to noxious
food in their environments, perhaps because their
physiologies are so well adapted to their preferred
host that encounters with non-host foods are rare.
In bats, generalist frugivorous and insectivorous feeders learn to avoid food associated with gastrointestinal malaise but specialist vampire bats, which are
obligate feeders on blood, do not (Ratcliffe et al.
2003). Likewise, polyphagous insects have been
shown to learn aversion to noxious food (Lee and
Bernays 1988) but some oligophagous insects do not
(Dethier and Yost 1979). Therefore, a tradeoff occurs
between specialization of diet and the ability to learn
aversion to foods associated with toxicosis.
Community effects: formation of refuges
Both innate and learned aversion to unpalatable prey
in individual consumers results in cascading community-wide effects. This is best illustrated through the
formation of refuges that provide protection for
small, sedentary consumers (Hay 1997). These refuges are formed by chemically defended plants and
sessile organisms that shield small consumers from
predation by large herbivores, and these refuges are
found in a variety of terrestrial, freshwater, and
marine environments (Price et al. 1980; Hay 1997).
In the marine environment, chemically defended
seaweed and sponges form refuges for mesograzers
such as amphipods and isopods (Hay 1997; Huang
et al. 2008). The herbivorous marine amphipod
Ampithoe longimana, associates with large, brown
seaweeds such as Dictyota dichotoma and Sargassum
filipendula, which are unpalatable to herbivorous fish
due to diterpene chemical defenses (Duffy and Hay
1991). Pseudamphithoides incurvaria, another marine
herbivorous amphipod, lives in the chemically defended brown alga, Dictyota bartayresii, which protects the amphipod from herbivorous fish as well
(Hay et al. 1990). In addition to seaweeds, a tropical
sponge, Amphimedon viridis, that contains neurotoxic alkaloids such as halitoxin and amphitoxin
has a rich mesofauna comprised mostly of small
crustaceans (Huang et al. 2008). Each of these chemically defended sessile marine organisms provides a
refuge for the small consumers that associate with
them.
A similar situation is seen in freshwater habitats,
as the freshwater moss. Fontinalis novae-angliae produces acetylenic fatty acids that are unpalatable to
B. E. Lunceford and J. Kubanek
large omnivores such as crayfish and Canada geese,
providing a safer habitat for small invertebrates such
as amphipods and isopods, which are known to be
eaten by crayfish and Canada geese (Prusak et al.
2005; Parker et al. 2007). Thus, the deterrent quality
of the moss protects other animals from larger consumers and acts as a refuge from predation.
These associations between mesograzers and the
chemically defended organisms that provide them
refuge can be parasitic or mutualistic, with some
mesograzers providing protection to their sessile
host (Hay 1997). There is also evidence that the
chemical defenses of some seaweeds deter grazing
by amphipods rather than being directed at large
herbivores (Hay et al. 1998). Cyclic-fatty-acid sexpheromones of brown algae belonging to the genus
Dictyopteris protect young developmental stages of
the macrophyte from consumption by mesograzers,
indicating that the alga differs in palatability depending on its developmental stage (Hay et al. 1998). The
relationships among organisms in these refuges can
be complex and dynamic, and are mediated, in part,
by the reception of aversive tastes. These refuges ultimately allow for protection of vulnerable prey species and thus contribute to species diversity within
an ecosystem.
Feeding ecology and the evolution of
taste receptors
As discussed in previous sections, an organism’s reception of aversive taste affects its feeding behavior,
which can result in cascading community-wide effects. As feeding behavior is a significant component
of an organism’s niche, it can be a potential factor in
speciation through sensory drive (Stevens 2013). For
many organisms, the number and sensitivity of receptors of bitter taste reflect the animal’s diet, and
there is significant interspecific and intraspecific variation in the amount, type, and sensitivity of receptors of bitter taste (Shi et al. 2003; Wooding et al.
2006; Zhou et al. 2009; Imai et al. 2012). Thus, the
variation in number and type of such receptors
found in organisms provides insight into their evolutionary relationships.
Variation in receptors
Within vertebrate lineages, fish have a relatively small
number of receptors for bitter taste (four to six),
whereas tetrapods have a greater number, ranging
from 21 to 49 (Shi and Zhang 2006; Hayakawa
et al. 2014). This could reflect a difference in
number or diversity of bitter ligands encountered
in the marine environment versus the terrestrial
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Reception of aversive taste
environment, or that the aversive taste receptors of
fish are broadly tuned (Behrens et al. 2014).
However, the discovery of a co-receptor involved in
fishes’ reception of aversive taste suggests that fish
may have an expanded combinatorial sensory
system in which a small number of GPCRs combine
with co-receptors to detect a wide range of aversive
compounds (Cohen et al. 2010).
Both in mammals and in birds, there is lineagespecific variation in the number of receptors for
bitter taste (Shi and Zhang 2006; Davis et al.
2010). For most mammals, the breadth of diet directly reflects the number and types of receptors for
bitter taste, best illustrated by the carnivore–herbivore dynamic. Carnivores’ genomes contain a small
number of bitter receptors that are hypothesized to
have high sensitivity to bitter compounds, whereas
herbivores’ genomes contain a large number of bitter
receptors that are hypothesized to have lower sensitivity (Glendinning 1994; Li and Zhang 2013).
Herbivores encounter a greater number of aversive
compounds in their diet than do most carnivores
and thus, would be expected to need to identify
more potential toxins while still being able to consume plant material. An exception to this is ruminants whose genomes have a low number of bitter
receptors, reflecting their specialized detoxification
process (Shi and Zhang 2006).
There have also been several lineage-specific evolutionary losses of bitter receptors in mammals. An
arresting example of this has occurred in vampire
bats, which are obligate feeders on blood (Hong
and Zhao 2014), and do not exhibit learned aversion
to foods that cause gastrointestinal malaise (Ratcliffe
et al. 2003). There may be a link between the losses
both of the repertoire of bitter receptors and of the
learned mechanism of aversion that is associated
with dietary specialization. Marine mammals exhibit
an extreme case of loss of taste receptors as, in addition to all their receptors for bitter taste, they have
lost receptors for sweet, umami, and sour tastes
(Jiang et al. 2012; Feng et al. 2014). This loss may
have resulted from a variety of life-history traits, including the shift to an all-meat diet, swallowing their
food whole, or the salinity of the ocean (Feng et al.
2014).
Insects also exhibit variation in type and number
of gustatory receptors (Grs) among species, reflecting
the wide range of niches that insects occupy (Liman
et al. 2014). The genomes of two species of mosquitoes that are vectors of disease contain comparable
numbers of Grs as those found in the Drosophila
genome, which contains 68 Grs: the genome of
Anopheles gambiae (vector of malaria) contains 76
Grs and that of Aedes aegypti (vector of yellow
fever) contains 91 Grs (Hill et al. 2002; Kent et al.
2008). As Grs function in contact chemosensation,
these mosquitoes’ Gr families are important targets
for the development of new pesticides (Kent et al.
2008).
The genomes of some insects, such as the honeybee, Apis mellifera, and the ant, Harpegnathos saltator, contain significantly lower numbers of Grs than
does Drosophila, 10 and 17, respectively (Robertson
and Wanner 2006; Zhou et al. 2012). This could be
due to specialized feeding strategies or that both of
these insects are eusocial and rely on volatile pheromones for communication (Zhou et al. 2012; Liman
et al. 2014). However, the genomes of other species
of ants and wasps, some of which are also eusocial,
have larger numbers of Grs, ranging from 46 to 116
(Smith et al. 2011; Zhou et al. 2012). An increase in
next-generation sequencing efforts will assist in linking the known chemical ecology of insects to their Gr
repertoires.
In addition, there is evidence of sexual dimorphism in the expression of Grs in ants and butterflies
(Zhou et al. 2012; Briscoe et al. 2013). In the butterfly species Heliconius melpomene, there are significantly more Grs expressed on the legs of females
than on those of males, suggesting that oviposition
by females drives the evolution of Gr in butterflies
(Briscoe et al. 2013). Thus, we see that receptors of
aversive taste both in vertebrates and invertebrates
are important targets for gene-duplication and selective loss of genes throughout evolution.
Conclusion
The evolutionary arms race between prey and predators drives the production of a wide variety of aversive compounds as well as of receptors of taste and
the mechanisms of reception. The variation and diversity of consumers’ mechanisms for the reception
of aversive taste has ecological and evolutionary consequences, such as the formation of refuges and the
correlation between feeding ecology and organisms’
repertoire of taste receptors. Comparison among organisms of these mechanisms for sensing taste gives
insight into the importance of aversive taste in evolution. There is significant variation in type and expression of taste receptors within populations of
consumers (Perry et al. 2007; Briscoe et al. 2013).
Likewise, there is variation in the types and numbers
of aversive ligands made by producers (Hay 1997).
The interplay of these variations on individual fitness
can drive speciation events, as was recently discovered in hummingbirds (Baldwin et al. 2014). On the
514
other hand, understanding interspecific variation can
illuminate how taste evolved. As aquatic environments have unique constraints both on taste and
on olfaction (Mollo et al. 2014), studying taste in
marine ecosystems gives insight into the origin of
taste and the molecular mechanisms that drive it.
Thus, a greater focus on taste in marine and freshwater environments, which has historically been lacking, would benefit the study of taste as a whole.
Overall, the study of reception, of taste and of aversive taste specifically, is of great importance to the
fields of ecology and evolution.
Funding
The authors acknowledge grant IOS-1354837 from
the U.S. National Science Foundation which supports their research on chemoreception.
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