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Independent evolution of bitter-taste sensitivity in humans and chimpanzees

Nature volume 440, pages 930–934 (2006)Cite this article

Abstract

It was reported over 65 years ago that chimpanzees, like humans, vary in taste sensitivity to the bitter compound phenylthiocarbamide (PTC)1. This was suggested to be the result of a shared balanced polymorphism, defining the first, and now classic, example of the effects of balancing selection in great apes. In humans, variable PTC sensitivity is largely controlled by the segregation of two common alleles at the TAS2R38 locus, which encode receptor variants with different ligand affinities2,3,4. Here we show that PTC taste sensitivity in chimpanzees is also controlled by two common alleles of TAS2R38; however, neither of these alleles is shared with humans. Instead, a mutation of the initiation codon results in the use of an alternative downstream start codon and production of a truncated receptor variant that fails to respond to PTC in vitro. Association testing of PTC sensitivity in a cohort of captive chimpanzees confirmed that chimpanzee TAS2R38 genotype accurately predicts taster status in vivo. Therefore, although Fisher et al.'s observations1 were accurate, their explanation was wrong. Humans and chimpanzees share variable taste sensitivity to bitter compounds mediated by PTC receptor variants, but the molecular basis of this variation has arisen twice, independently, in the two species.

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Figure 1: Hypothetical origins of PTC taster and nontaster alleles in humans and chimpanzees.
Figure 2: Patterns of genetic variation in TAS2R38 in human, chimpanzee and gorilla.
Figure 3: Translation, membrane localization and functional characteristics of ch TAS2R38 alleles.
Figure 4: Chimpanzee responses to PTC.

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Acknowledgements

Chimpanzee samples were contributed by Sunset Zoo, Riverside Zoo, Kitwe Point Sanctuary, the Jane Goodall Institute, J. Wickings, the Centre International de Recherches Medicales, the Primate Foundation of Arizona, the New Iberia Primate Center and the Southwest Foundation for Biomedical Research. Chimpanzee samples were imported under a CITES permit. Comments and technical assistance were provided by C. Anderson, D. Drayna, L. Jorde, U-k. Kim, M. Pyrski, A. Rogers, J. Seger and E. Wooding. Funding was provided by grants from the NIH, the Centers for Disease Control, the Muscular Dystrophy Association, the Wenner-Gren Foundation, the National Science Foundation and the German Science Foundation.

Author information

Author notes

  1. Michael J. Bamshad

    Present address: Departments of Pediatrics and Genome Sciences, University of Washington, Seattle, Washington, 98195, USA

Authors and Affiliations

  1. Department of Human Genetics, University of Utah, 15 North 2030 East, Salt Lake City, Utah, 84112-5330, USA

    Stephen Wooding, Michael T. Howard, Diane M. Dunn, Robert B. Weiss & Michael J. Bamshad

  2. German Institute of Human Nutrition Potsdam-Rehbruecke, Arthur-Scheunert-Allee 114-116, Nuthetal, 14558, Germany

    Bernd Bufe & Wolfgang Meyerhof

  3. Department of Comparative Medicine, Southwest Foundation for Biomedical Research, San Antonio, Texas, 78245-0549, USA

    Christina Grassi & Maribel Vazquez

  4. School of Human Evolution and Social Change, Arizona State University, Tempe, Arizona, 85287-2402, USA

    Anne C. Stone

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Correspondence to Stephen Wooding or Michael J. Bamshad.

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Supplementary information

Supplementary Figure 1

This file contains a JPEG of Supplementary Figure 1: Schematic of artificial expression constructs. (JPG 104 kb)

Supplementary Figure 2

This file contains a JPEG of Supplementary Figure 2: Schematic of constructs used for testing receptor response to PTC. (TXT 9 kb)

Supplementary Figure 3

This file contains a JPEG of Supplementary Figure 3: Transfection and expression of TAS2R38 in HEK cells. (JPG 179 kb)

Supplementary Figure 4

This file contains a JPEG of Supplementary Figure 4: Membrane localization and functional characteristics of the AGG-chTAS2R38 (-99aa) construct. (JPG 261 kb)

Supplementary Figure Legends

This file contains the Supplementary Figure Legends. (JPG 216 kb)

Supplementary Notes 1

This file contains the raw genotype and phenotype data. (DOC 21 kb)

Supplementary Notes 2

This file is a text file conversion of an SAS (Statistical Analysis System) file that generates summary statistics describing the raw data. (XLS 18 kb)

Supplementary Notes 3

This file is a text file conversion of an SAS (Statistical Analysis System) file used to test for differences in response between TAS2R38 heterozygotes and homozygotes. (TXT 3 kb)

Supplementary Notes 4

This file is a text file conversion of an SAS (Statistical Analysis System) file used to test for association between TAS2R38 genotype and PTC sensitivity phenotype. (TXT 9 kb)

Supplementary Notes 5

This file is a text file conversion of an SAS (Statistical Analysis System) file used to test for differences in response of predicted tasters and nontasters between the test and control treatments. (TXT 9 kb)

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Wooding, S., Bufe, B., Grassi, C. et al. Independent evolution of bitter-taste sensitivity in humans and chimpanzees. Nature 440, 930–934 (2006). https://doi.org/10.1038/nature04655

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