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Functional decline of sweet taste sensitivity of colobine monkeys

Abstract

For many primates, sweet taste is palatable and is an indicator that the food contains carbohydrates, such as sugars and starches, as energy sources. However, we have found that Asian colobine monkeys (lutungs and langurs) have low sensitivity to various natural sugars. Sweet tastes are recognized when compounds bind to the sweet taste receptor TAS1R2/TAS1R3 in the oral cavity; accordingly, we conducted a functional assay using a heterologous expression system to evaluate the responses of Javan lutung (Trachypithecus auratus) TAS1R2/TAS1R3 to various natural sugars. We found that Javan lutung TAS1R2/TAS1R3 did not respond to natural sugars such as sucrose and maltose. We also conducted a behavioral experiment using the silvery lutung (Trachypithecus cristatus) and Hanuman langur (Semnopithecus entellus) by measuring the consumption of sugar-flavored jellies. Consistent with the functional assay results for TAS1R2/TAS1R3, these Asian colobine monkeys showed no preference for sucrose or maltose jellies. These results demonstrate that sweet taste sensitivity to natural sugars is low in Asian colobine monkeys, and this may be related to the specific feeding habits of colobine monkeys.

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Acknowledgements

The authors would like to thank Drs. T. Ueda, T. Misaka, and H. Matsunami for providing cells and vectors, and Dr. K. A. Widayati, L. H. Purba, and S. Nila for supporting the collection of fecal samples from Javan lutungs. Our thanks are also due to T. Hoshino, T. Funahashi, and other keepers and veterinarians of the Japan Monkey Centre for taking care of the colobine monkeys, supporting behavioral experiments, and collecting genetic samples. We also thank A. Yamanaka and CHEMR of KUPRI for taking care of the Japanese macaques. This study was financed by JSPS KAKENHI (#16H01338, #15H02421, #15H05242, and #25257409 to HI; #12J04270 and #16K18630 to TH; and #12J04300 and #17K15203 to NSH), research grants from Kobayashi International Scholarship Foundation, and the JSPS bilateral research program between Japan and Indonesia.

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Correspondence to Hiroo Imai.

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The authors declare that they have no conflicts of interest.

Ethical approval

Colobine monkey behavioral experiments were conducted at the Japan Monkey Centre, Aichi, Japan. The study was approved by the Research Ethics Committee of the Japan Monkey Centre (#2017-014) based on the Ethical Guidelines for Research in Japan Monkey Centre (April 1st, 2016) as Collaborative Research of the Japan Monkey Centre (#2017013) The Japanese macaque experiment 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 (#2017-178) and were in compliance with the Guidelines for Care and Use of Nonhuman Primates of the Primates 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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Nishi, E., Suzuki-Hashido, N., Hayakawa, T. et al. Functional decline of sweet taste sensitivity of colobine monkeys. Primates 59, 523–530 (2018). https://doi.org/10.1007/s10329-018-0679-2

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  • DOI: https://doi.org/10.1007/s10329-018-0679-2

Keywords

  • Colobine monkeys
  • Taste sensitivity
  • Natural sugars
  • Sweet taste receptor
  • TAS1R2/TAS1R3