It is generally believed that most mammals perceive five basic taste qualities: sweet, umami (tasty), bitter, salty, and sour. The receptors for sweet, umami and bitter tastes are G protein-coupled receptors (GPCRs). Sweet taste is mediated largely by a heteromer of two closely related Tas1r (type 1 taste receptor) family GPCRs: Tas1r2 and Tas1r3. Tas1r1, another member of the Tas1r family, in combination with Tas1r3, forms an umami taste receptor. Tas1r receptors are class C GPCRs. Unlike sweet and umami tastes, bitter taste is mediated by Tas2r family GPCRs, which belong to class A GPCRs and are structurally unrelated to Tas1r family receptors. The genes encoding Tas2r receptors, the Tas2r genes, differ substantially in gene number and primary sequences among species, most likely reflecting the likelihood that these genes are required for detecting toxic or harmful substances in a species’ ecological niche.
Sweet taste Tas1r2 genes are pseudogenized in domestic cats which show indifference to sweet taste. Similarly, in other members (e.g., tiger and cheetah) of the cat family Tas1r2 genes are pseudogenized. In a recent study Jiang et al. (1) sequenced all exons of Tas1r2 genes from several carnivore species including obligate carnivores (e.g., domestic and wild cats), relatively omnivorous species (e.g., bears), and strict herbivores (e.g., giant panda). They found that loss-of-function mutations occurred in different positions of exons of Tas1r2 genes of obligate carnivores (Fig. 1), which are scattered on the phylogenetic tree (Fig. 2). This result indicates that pseudogenization of Tas1r2 genes resulting in loss of sweet taste occurred independently in several carnivore lineages in relatively short periods of time.
Fig. 2. Evolutionary tree of Tas1r2 genes from 18 species of carnivores. Species with a pseudogenized Tas1r2 are marked with a diamond (red and gray depict species characterized in this study and the previous study, respectively).
Furthermore, Jiang et al. showed that in sea lion (Carnivora) and dolphin (Cetacea) which swallow whole food and have a reduced number of taste buds on tongue Tas1r1 and Tas1r3 genes are pseudogenized. They also failed to find intact Tas2r genes that encode bitter taste receptors in the dolphin genome. This result indicates the loss of umami taste as well as the loss of sweet taste in sea lion and dolphin and suggests the loss of bitter taste in the latter. Jiang et al. present the view that the loss of taste receptor genes is a consequence of dietary specialization in mammals (1).
However, Zhao and Zhang (2) pointed out that (i) although Tas1r2 genes are pseudogenized only in obligate carnivores in Jiang et al. (1), ferret and Canadian otter, which are also obligate carnivores, still possess intact Tas1r2 genes and (ii) although three pinnipeds share the common ancestry of obligate meat-eating, none of the null mutations in Tas1r2 genes are shared by these species. Moreover, a previous study of Zhao and Zhang’s group (3) showed that (iii) Tas1r2 genes are pseudogenized in vampire bats which feed solely on blood containing carbohydrate and (iv) Tas1r2 genes are missing in herbivorous horse and omnivorous pig as well as in all available birds’ genome sequences irrespective of their diet. Tas1r1 genes that encode umami taste receptors are pseudogenized in all bats regardless of their diet (fruit, insect, blood) (4). In Zhao and Zhang’s view the relationship between the diet of species and the loss of function of taste receptor genes is quite complex and sometimes inconsistent.
Jiang et al. (5) responded to Zhao and Zhang (2) stating that (i) prefect correspondence between the exclusive meat-eating diet and the loss of taste receptor genes should not be expected because the loss of sweet taste receptor genes occurs stochastically and therefore is a time-dependent and ongoing process after diet switch, (ii) whether the common ancestor depended solely on meat-eating diet is not known, (iii) vampire bats unlikely require sweet taste because of the very small amount of carbohydrate in blood, and (iv) some studies showed the presence of Tas1r2 genes in horse and pig and these species show preference of sweet taste.
Although Jiang et al. (5) responded to Zhao and Zhang’s (2) questions, some questions remain unanswered. For example, why are no sweet taste receptor genes found in birds regardless of their diets?
Although the two groups of authors have different opinions on the relationship of the diet and loss of taste receptor genes, both of them recognize a need for better understanding of physiological mechanisms of taste and taste receptors to understand the relationship between diet and gene loss (1, 2).
The abstract of Jiang et al.’s paper (1) is as follows.
Mammalian sweet taste is primarily mediated by the type 1 taste receptor Tas1r2/Tas1r3, whereas Tas1r1/Tas1r3 act as the principal umami taste receptor. Bitter taste is mediated by a different group of G protein-coupled receptors, the Tas2rs, numbering 3 to ~ 66, depending on the species. We showed previously that the behavioral indifference of cats toward sweet-tasting compounds can be explained by the pseudogenization of the Tas1r2 gene, which encodes the Tas1r2 receptor. To examine the generality of this finding, we sequenced the entire coding region of Tas1r2 from 12 species in the order Carnivora. Seven of these nonfeline species, all of which are exclusive meat eaters, also have independently pseudogenized Tas1r2 caused by ORF-disrupting mutations. Fittingly, the purifying selection pressure is markedly relaxed in these species with a pseudogenized Tas1r2. In behavioral tests, the Asian otter (defective Tas1r2) showed no preference for sweet compounds, but the spectacled bear (intact Tas1r2) did. In addition to the inactivation of Tas1r2, we found that sea lion Tas1r1 and Tas1r3 are also pseudogenized, consistent with their unique feeding behavior, which entails swallowing food whole without chewing. The extensive loss of Tas1r receptor function is not restricted to the sea lion: the bottlenose dolphin, which evolved independently from the sea lion but displays similar feeding behavior, also has all three Tas1rs inactivated, and may also lack functional bitter receptors. These data provide strong support for the view that loss of taste receptor function in mammals is widespread and directly related to feeding specializations.
1. Jiang P, Josue J, Li X, Galser D, Li W, Brand JG, Margolskee RF, Reed DR, Beauchamp GK. 2012. Major taste loss in carnivorous mammals. Proc. Natl. Acad. Sci. USA. 109:4956-4961.
2. Zhao H, Zhang J. 2012. Mismatches between feeding ecology and taste receptor evolution: An inconvenient truth. Proc. Natl. Acad. Sci.USA, doi: 10.1073/pnas.1205205109.
3. Zhao H, Zhou Y, Pinto CM, Charles-Dominique P, Galindo-Gonzalez J, Zhang S, Zhang J. 2010. Evolution of the sweet taste receptor gene Tas1r2 in bats. Mol. Biol. Evol. 27; 2642-2650.
4. Zhao H, Xu D, Zhang S, Zhang J. 2012. Genomic and genetic evidence for the loss of umami taste in bats. Genome Biol. Evol. 4:73-79.
5. Jiang P, Josue J, Li X, Galser D, Li W, Brand JG, Margolskee RF, Reed DR, Beauchamp GK. 2012. Reply to Zhao and Zhnag: Loss of taste receptor function in mammals is directly related to feeding specializations. Proc. Natl. Acad. Sci. USA, doi: 10.1073/pnas.1205581109.