Each animal species lives in a separate sensory world that is coordinated with its
behavioral ecology. A dramatic example of this occurs for the sense of taste 1] where sensory perception and diet choice are intimately intertwined.
The evolutionary basis for the existence of a small number of primary taste qualities
(sweet, bitter, sour, salty, umami, and perhaps a few others) is that these qualities
evolved to detect and motivate consumption of critical nutrients and detect and avoid
potential poisons. It is widely believed that sweet taste evolved in animals that
eat plants to detect energy-rich simple sugars such as glucose, fructose, and sucrose.
In contrast, bitter taste presumably functions to insure that an animal avoids poisons;
most poisons are bitter and most bitter substances are harmful although this relationship
is not perfect. Salty taste is thought to enable detection of sodium, an absolutely
essential mineral. When some species of animals become deficient in sodium—usually
this occurs in herbivorous animals—a powerful appetite for salty taste is aroused.
And for many species, salt is consumed even when there is no apparent need. For sour
taste, many have suggested that it is involved in the detection of the ripeness of
fruits. Finally, the fifth basic taste, umami or savory, probably serves to signal
amino acids and protein. This however remains speculative. Other classes of compounds
may also interact with the taste system (e.g., fatty acids, calcium, starch), but
they do not give rise to the (to humans) strong qualitative percept that the other
five do.
To obtain a clearer understanding of the functional significance for these basic taste
qualities, we have studied the order Carnivora. Our goal is to understand how taste
receptors and taste perception in different species are related to different feeding
ecologies with a particular focus on sweet compounds. For example, some Carnivora
species are obligate carnivores (e.g., cats), whereas others are almost completely
herbivorous, sometimes feeding on virtually a single plant (e.g., giant panda). If
the function of sweet taste is to detect simple sugars in plants, we predict that
animals that do not consume plants would not need/have sweet taste perception. By
examining sweet taste perception across a number of species in this order, we can
put this prediction to the test.
Many years ago, we 2] demonstrated that domestic and wild cats (Felis and Panthera species) are indifferent to all sweeteners tested but are highly responsive to certain
amino acids and fats. We speculated that these species may not have the ability to
perceive sweet (to humans) sugars. Following the discovery of the major sweet taste
receptor, the T1R2?+?T1R3 heterodimer (review: 3]), we demonstrated that the cat’s indifference to sweeteners can be explained by the
pseudogenization of the Tas1r2 gene which encodes the T1R2 receptor. That is, the sweet taste receptor of the domestic
cat as well as closely related wild cats such as lions and tigers has accumulated
numerous germ-line mutations of the Tas1r2 gene, thereby rendering the sweet receptor non-functional 4].
We next reasoned that other exclusively meat-eating species might also have an inactive
form of this gene. Sequencing of the entire coding region of the Tas1r2 gene from 12 Carnivora species revealed that seven of these species, all exclusive
meat eaters, had independently fixed a defective Tas1r2 allele 5]. Since these disabling mutations occurred at different places within the Tas1r2 gene in each species, this loss of sweet taste function in multiple species in the
Carnivora has occurred independently and thus repeatedly during their evolution. Behavioral
tests of two of the genotyped species, the Asian otter (defective Tas1r2) and the spectacled bear (intact Tas1r2), were consistent with the genetic findings: The former showed no preference for
sweet-tasting compounds, while the latter preferred sugars and some non-caloric sweeteners.
These results indicate that the independent loss of a functional Tas1r2 is widespread among obligate carnivores. We suggest that this loss is a consequence
of the relaxation of selective pressures maintaining receptor integrity.
A striking study with birds provides additional support for the hypothesis that sweet
taste exists to detect simple sugars. All birds apparently lack a homolog for the
Tas1r2 gene; this loss likely occurred as the non-avian reptile and bird lines split. Thus,
it would seem that birds should not be able to taste sweet sugars. But if this were
the case, how can one explain the behavior of avian species that consume sweet sugars
such as hummingbirds? Baldwin et al. 6,7] provide one answer: The receptor dimer T1R1?+?T1R3, the amino acid or umami receptor
in mammals, has been repurposed in these bird species to detect simple sugars thereby
opening a novel source of energy not available to many other birds. In sum, these
studies provide strong support for the hypothesis that sweet taste perception exists
to provide an ability to identify energy-rich sugars.
More recently 8], we conducted behavioral and molecular studies with giant pandas, animals that consume
plants, but ones (bamboo) without abundant simple sugars. Would this member of the
order Carnivora retain sweet taste perception, or would the absence of a need to find
specific plants that taste sweet also result in relaxed selection for maintenance
of receptor function? We found that sweet taste perception is fully functional in
giant pandas. Although giant pandas thus retain an avidity for sweet compounds, genetic
evidence suggests that this species has lost umami taste perception 9], but as yet we know of no behavioral studies verifying this nor do we understand
why this may have occurred and how widespread such loss might be.
Although loss of sweet taste seems common for animals that do not consume plants,
are there species that have lost even more of the basic tastes? And if so, how can
this be interpreted? Based on genetic studies, we 5] and others 10] have reported that many mammalian species that have returned to the sea (e.g., sea
lions, dolphins, whales) may have independently lost function for several, perhaps
all, taste quality perception. These genetic studies are consistent with anatomy (many
of the species do not have identifiable taste cell structures) and behavior (many
eat their food whole, without apparently “tasting†it). The factors responsible for
this extensive loss of taste function in marine mammals remain to be determined.
In summary, these data dramatically illustrate how plastic the taste system is and,
as illustrated through the sweet taste modality, how it has adapted to changes in
diet as species evolved. Similar changes are likely in the other taste qualities.
For example, it is likely that species differences in the repertoires of bitter receptors
reflect different classes of poisons that these species are likely to confront 11]. Species variation in salt taste perception is also likely to be coordinated with
diet. For example, it is possible that strict carnivores may not perceive NaCl in
the same way as do herbivorous mammals since carnivores’ all-meat diet likely provides
sufficient Na+. Finally, as a third example, the human umami or amino acid receptor responds to
only a few compounds (glutamate and a few others). However, this receptor acts as
a more general amino acid receptor for rodents and other species. These species differences
may also be explained by different feeding ecologies although this remains to be determined.
Future comparative research will surely reveal many more interesting and important
relationships between taste function, food choice, and diet.