Abstract
Bitter taste perception enables the detection of potentially toxic molecules and thus evokes avoidance behavior in vertebrates. It is mediated by bitter taste receptors, TAS2Rs. One of the best-studied TAS2R is TAS2R38. Phenylthiocarbamide (PTC) perception and TAS2R38 receptors vary across primate species, and this variation may be related to variation in dietary preferences. In particular, we previously found that the low sensitivity of TAS2R38s in Asian colobines likely evolved as an adaptation to their leaf-eating behavior. However, it remains unclear whether this low PTC sensitivity is a general characteristic of the subfamily Colobinae, a primate group that feeds predominantly on leaves. We performed genetic analyses, functional assays with mutant proteins, and behavioral analyses to evaluate the general characteristics of TAS2R38 in colobines. We found that PTC sensitivity is lower in TAS2R38s of African colobines than in TAS2R38s of omnivorous macaques. Furthermore, two amino acids shared between Asian and African colobines were responsible for low sensitivity to PTC, suggesting that the last common ancestor of extant colobines had this phenotype. We also detected amino acid differences between TAS2R38s in Asian and African colobines, indicating that they evolved independently after the separation of these groups.
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Acknowledgements
The authors would like to thank Dr. Takashi Ueda, Dr. Yoshiro Ishimaru, Dr. Takumi Misaka, and Dr. Keiko Abe for providing the Ga16/gust44 and pEAK10 vectors, as well as Dr. Hiroaki Matsunami for providing HEK293T cells. We also wish to express our gratitude to Yumi Tsujiuchi, Taiki Okumura, and other keepers and veterinarians at the Japan Monkey Centre for taking care of the colobines, supporting behavioral assays, and collecting genetic samples, as well as Atsushi Yamanaka and the Center for Human Evolution Modeling Research at the Primate Research Institute, Kyoto University for taking care of the Japanese macaques. This study was funded by JSPS KAKENHI (#16H01338, #15H02421, #18H0400, and #19K21586 to HI; #16K18630 to TH; and #17K15203 to NSH); research grants from the Kobayashi International Scholarship Foundation (to HI); PMDSU nos. 1050/IT3.11/LT/2017 and 1486/IT3.11/PN/2018 and nos. 219.6/D3/PG/2019, 121/SP2H/LT/DRPM/2019 from the Ministry of Research, Technology and Higher Education to BS; Cooperative Research Programme of Kyoto University (Kyodo Riyo Theme nos. 2017-B-51, 2018-B-35, 2019-B-55 and Sandwich-like PMDSU No: 1056/D3.2/PG/2018 to LHPSP). This work was also supported by JSPS and DG-RSTHE under the Japan-Indonesia Research Cooperative Program and Core-to-Core Program.
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LHPSP conducted the experiments, wrote the first draft, and analyzed and interpreted the data. KAW conducted the experiments, analyzed and interpreted data, and revised the manuscript. NSH and TH conducted the experiments, analyzed the data, and revised the draft. AI analyzed the data and revised the draft. SN collected samples. BJ analyzed the data and revised the draft. BS designed the experiments, and revised the manuscript. HI designed the experiments, and wrote the final draft. All authors agree to be held accountable for the content in the manuscript and approve the final version.
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Colobine behavioral assays were conducted at the Japan Monkey Centre, Inuyama, Japan. The study was approved by the Research Ethics Committee of the Japan Monkey Centre in accordance with the Ethical Guidelines for Research of the institution (April 1, 2016) as Collaborative Research with the Japan Monkey Centre (#2018015). The Japanese macaque assay was conducted at the Primate Research Institute, Kyoto University. Both experiments were approved by the Animal Welfare and Animal Care Committee of Primate Research Institute, Kyoto University (#2018–201) and were conducted in compliance with the Guidelines for Care and Use of Nonhuman Primates of the Primate Research Institute, Kyoto University (Version 3, issued in 2010). These guidelines were prepared based on the provisions of the Guidelines for Proper Conduct of Animal Experiments (June 1, 2006; Science Council of Japan), Basic Policies for the Conduct of Animal Experiments in Research Institutions under the Jurisdiction of the Ministry of Health, Labour and Welfare (effective on June 1, 2006; Ministry of Health, Labour and Welfare), Fundamental Guidelines for Proper Conduct of Animal Experiment and Related Activities in Academic Research Institutions (Notice No. 71 of the Ministry of Education, Culture, Sports, Science and Technology dated June 1, 2006), and Standards Relating to the Care and Management of Laboratory Animals and Relief of Pain (Notice No. 88 of the Ministry of the Environment dated April 28, 2006).
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Purba, L.H.P.S., Widayati, K.A., Suzuki-Hashido, N. et al. Evolution of the bitter taste receptor TAS2R38 in colobines. Primates 61, 485–494 (2020). https://doi.org/10.1007/s10329-020-00799-1
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DOI: https://doi.org/10.1007/s10329-020-00799-1