Identification of non-taster Japanese macaques for a specific bitter taste

Suzuki, Nami; Sugawara, Tohru; Matsui, Atsushi; Go, Yasuhiro; Hirai, Hirohisa; Imai, Hiroo

doi:10.1007/s10329-010-0209-3

Cited by 29 publications

(22 citation statements)

References 15 publications

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“…This phenotypic variation of PTC perception has been found in many primate taxa, and the causal gene was first identified as TAS2R38 in humans [37]–[40]. Different types of nonsense mutations in TAS2R38 orthologues and PTC inactivation in homozygous individuals were also found in Japanese macaques ( Macaca fuscata ) as types of intraspecific variation [41]. Similar to the occurrence of the non-functional allele of TAS2R38 about 0.5 mya in chimpanzees, phylogenetic analyses revealed that the non-functional allele of TAS2R38 arouse between 0.3–1.6 mya in humans and at around 0.5 mya in Japanese macaques [41], [42].…”

Section: Discussionmentioning

confidence: 84%

“…Different types of nonsense mutations in TAS2R38 orthologues and PTC inactivation in homozygous individuals were also found in Japanese macaques ( Macaca fuscata ) as types of intraspecific variation [41]. Similar to the occurrence of the non-functional allele of TAS2R38 about 0.5 mya in chimpanzees, phylogenetic analyses revealed that the non-functional allele of TAS2R38 arouse between 0.3–1.6 mya in humans and at around 0.5 mya in Japanese macaques [41], [42]. The occurrence of PTC non-tasters in multiple species may thus have resulted from similar selective pressure by a global alteration of climate and flora during the Pleistocene epoch, which was characterized by repeated global glaciations.…”

Section: Discussionmentioning

confidence: 90%

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Eco-Geographical Diversification of Bitter Taste Receptor Genes (TAS2Rs) among Subspecies of Chimpanzees (Pan troglodytes)

Hayakawa

Sugawara

et al. 2012

PLoS ONE

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Chimpanzees (Pan troglodytes) have region-specific difference in dietary repertoires from East to West across tropical Africa. Such differences may result from different genetic backgrounds in addition to cultural variations. We analyzed the sequences of all bitter taste receptor genes (cTAS2Rs) in a total of 59 chimpanzees, including 4 putative subspecies. We identified genetic variations including single-nucleotide variations (SNVs), insertions and deletions (indels), gene-conversion variations, and copy-number variations (CNVs) in cTAS2Rs. Approximately two-thirds of all cTAS2R haplotypes in the amino acid sequence were unique to each subspecies. We analyzed the evolutionary backgrounds of natural selection behind such diversification. Our previous study concluded that diversification of cTAS2Rs in western chimpanzees (P. t. verus) may have resulted from balancing selection. In contrast, the present study found that purifying selection dominates as the evolutionary form of diversification of the so-called human cluster of cTAS2Rs in eastern chimpanzees (P. t. schweinfurthii) and that the other cTAS2Rs were under no obvious selection as a whole. Such marked diversification of cTAS2Rs with different evolutionary backgrounds among subspecies of chimpanzees probably reflects their subspecies-specific dietary repertoires.

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Section: Discussionmentioning

confidence: 84%

Section: Discussionmentioning

confidence: 90%

Eco-Geographical Diversification of Bitter Taste Receptor Genes (TAS2Rs) among Subspecies of Chimpanzees (Pan troglodytes)

Hayakawa

Sugawara

et al. 2012

PLoS ONE

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“…Another case of convergent evolution of taste was found in the Tas2r38 receptor gene. Mutations in the Tas2r38 gene have resulted in independent loss of phenylthiocarbamide sensitivity in some humans, chimpanzees, and macaques (30,31). Notably, the mutations in chimpanzees and macaques are start codon mutations, resembling the case with sea lion and fur seal Tas1r2s (30,31).…”

Section: Discussionmentioning

confidence: 99%

Major taste loss in carnivorous mammals

Jiang

Josue

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

242

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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.diet | sweetener I t is widely believed that most mammals perceive five basic taste qualities: sweet, umami, bitter, salty, and sour. The receptors for sweet, umami and bitter tastes are G protein-coupled receptors (GPCRs) (1). Sweet taste is mediated largely by a heteromer of two closely related Tas1r (type 1 taste receptor) family GPCRs: Tas1r2 and Tas1r3 (2-5). Tas1r1, another member of the Tas1r family, in combination with Tas1r3, forms an umami taste receptor (6). 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 (7,8). 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 (9-11).Direct evidence for a close correlation between taste function and feeding ecology comes from work on domestic and wild Felidae. Cats, obligate carnivores, are behaviorally insensitive to sweet-tasting compounds (12, 13). We proposed that this behavioral insensitivity was a consequence of the pseudogenization of Tas1r2 (14). Tas1r2 also is known to be pseudogenized in chicken, tongueless Western clawed frogs, and vampire bats (11,15). The loss of th...

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“…The less common variants of hTAS2R38, namely AAI, PVI, and AAV, show intermediate sensitivity to PTC (Bufe et al, ). Few studies of nonhuman primates have explored the functional divergence of TAS2R38 with respect to PTC sensitivity, including studies of Macaca fuscata and Pan troglodytes (Suzuki et al, ; Wooding et al, ).…”

Section: Introductionmentioning

confidence: 99%

Functional divergence of the bitter receptor TAS2R38 in Sulawesi macaques

Widayati

Yan

Suzuki‐Hashido

et al. 2019

Ecology and Evolution

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Bitter perception is mediated by G protein‐coupled receptors TAS2Rs and plays an important role in avoiding the ingestion of toxins by inducing innate avoidance behavior in mammals. One of the best‐studied TAS2Rs is TAS2R38, which mediates the perception of the bitterness of synthetic phenylthiocarbamide (PTC). Previous studies of TAS2R38 have suggested that geographical separation enabled the independent divergence of bitter taste perception. The functional divergence of TAS2R38 in allopatric species has not been evaluated. We characterized the function of TAS2R38 in four allopatric species of Sulawesi macaques on Sulawesi Island. We found variation in PTC taste perception both within and across species. In most cases, TAS2R38 was sensitive to PTC, with functional divergence among species. We observed different truncated TAS2R38s that were not responsive to PTC in each species of Macaca nigra and M. nigrescens due to premature stop codons. Some variants of intact TAS2R38 with an amino acid substitution showed low sensitivity to PTC in M. tonkeana. Similarly, this intact TAS2R38 with PTC‐low sensitivity has also been found in humans. We detected a shared haplotype in all four Sulawesi macaques, which may be the ancestral haplotype of Sulawesi macaques. In addition to shared haplotypes among Sulawesi macaques, other TAS2R38 haplotypes were species‐specific. These results implied that the variation in TAS2R38 might be shaped by geographical patterns and local adaptation. OPEN RESEARCH BADGES This article has earned an Open Data Badge for making publicly available the digitally‐shareable data necessary to reproduce the reported results. The data is available at https://doi.org/10.5061/dryad.908jf3r.

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Identification of non-taster Japanese macaques for a specific bitter taste

Cited by 29 publications

References 15 publications

Eco-Geographical Diversification of Bitter Taste Receptor Genes (TAS2Rs) among Subspecies of Chimpanzees (Pan troglodytes)

Eco-Geographical Diversification of Bitter Taste Receptor Genes (TAS2Rs) among Subspecies of Chimpanzees (Pan troglodytes)

Major taste loss in carnivorous mammals

Functional divergence of the bitter receptor TAS2R38 in Sulawesi macaques

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