Major taste loss in carnivorous mammals

Peihua Jiang; Jesusa Josue; Xia Li; Dieter Glaser; Weihua Li; Joseph G. Brand; Robert F. Margolskee; Danielle R. Reed; Gary K. Beauchamp

doi:10.1073/pnas.1118360109

Edited by Dennis T. Drayna, National Institutes of Health, Rockville, MD, and accepted by the Editorial Board February 2, 2012 (received for review November 7, 2011)

Abstract

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.

Footnotes

↵¹To whom correspondence may be addressed. E-mail: pjiang{at}monell.org or beauchamp{at}monell.org.
↵²Present address: AmeriPath Northeast, Shelton, CT 06484.
↵³Present address: Center for Resuscitation Science, Translational Research Laboratory, University of Pennsylvania Health System, Philadelphia, PA 19104.

Author contributions: P.J., X.L., J.G.B., R.F.M., D.R.R., and G.K.B. designed research; P.J., J.J., X.L., D.G., and W.L. performed research; P.J. and G.K.B. analyzed data; and P.J., J.G.B., R.F.M., D.R.R., and G.K.B. wrote the paper.
The authors declare no conflict of interest.
This article is a PNAS Direct Submission. D.T.D. is a guest editor invited by the Editorial Board.
Data deposition: The sequences reported in this paper have been deposited in the GenBank database [accession nos. JN130349–JN130360 (sea lion, fur seal, Pacific Harbor seal, Asian small-clawed otter, spotted hyena, fossa, banded linsang, aardwolf, Canadian otter, spectacled bear, raccoon, and red wolf Tas1r2 sequences, respectively); JN413105 (sea lion Tas1r1); JN413106 (sea lion Tas1r3); JN622015 (dolphin Tas1r1); JN622016 (dolphin Tas1r2); JN622017 (dolphin Tas1r3); and JN622018–JN622027 (dolphin Tas2rs)].
This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1118360109/-/DCSupplemental.