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Independent evolution of bitter-taste sensitivity in humans and chimpanzees

Nature 440, 930–934 (13 April 2006) | Download Citation

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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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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

    • Michael J. Bamshad

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

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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Competing interests

Reprints and permissions information is available at npg.nature.com/reprintsandpermissions. The authors declare no competing financial interests.

Corresponding authors

Correspondence to Stephen Wooding or Michael J. Bamshad.

Supplementary information

Image files

  1. 1.

    Supplementary Figure 1

    This file contains a JPEG of Supplementary Figure 1: Schematic of artificial expression constructs.

  2. 2.

    Supplementary Figure 3

    This file contains a JPEG of Supplementary Figure 3: Transfection and expression of TAS2R38 in HEK cells.

  3. 3.

    Supplementary Figure 4

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

  4. 4.

    Supplementary Figure Legends

    This file contains the Supplementary Figure Legends.

Text files

  1. 1.

    Supplementary Figure 2

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

  2. 2.

    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.

  3. 3.

    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.

  4. 4.

    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.

Word documents

  1. 1.

    Supplementary Notes 1

    This file contains the raw genotype and phenotype data.

Excel files

  1. 1.

    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.

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DOI

https://doi.org/10.1038/nature04655

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