Genetic variation in bitter taste receptor genes influences the foraging behavior of plateau zokor (Eospalax baileyi)

Abstract The ability to detect bitter tastes is important for animals; it can help them to avoid ingesting harmful substances. Bitter taste perception is mainly mediated by bitter taste receptor proteins, which are encoded by members of the Tas2r gene family and vary with the dietary preference of a specific species. Although individuals with different genotypes differ in bitterness recognition capability, little is known about the relationship between genetic variation and food selection tendencies at the intraspecific level. In this study, we examined the relationship between genotypes and diet in plateau zokor (Eospalax baileyi), a subterranean rodent endemic to the Qinghai‐Tibet Plateau that caches food for the winter. We assayed the composition and taste profile of each plant contained in temporary caches and vicinity quadrats, which were representative of selected and available food, respectively. Bitter plant selection indices (E bitter) were estimated. We also sequenced 26 candidate Tas2r genes from zokors and determined their relationships with the E bitter of their caches. We identified four key results: (1) zokors varied considerably in both bitter food preference and Tas2r sequences; (2) five genes (zTas2r115,zTas2r119,zTas2r126,zTas2r134, and zTas2r136) exhibited allelic variation that was significantly associated with E bitter; (3) synonymous SNPs, nonsynonymous SNPs, and pseudogenization are involved in the genotype–phenotype relationship; (4) the minor genotypes of zTas2r115,zTas2r134, and zTas2r136 and the major genotypes of zTas2r119 and zTas2r126 cached more bitter plants. Our results link Tas2r variation with food selection behavior at the population level for the first time.

[1]  Yvonne Feierabend,et al.  Population Genetics A Concise Guide , 2016 .

[2]  Jianzhi Zhang,et al.  Molecular evidence for the loss of three basic tastes in penguins , 2015, Current Biology.

[3]  A. Reverter,et al.  Characterization of the porcine nutrient and taste receptor gene repertoire in domestic and wild populations across the globe , 2014, BMC Genomics.

[4]  Tong-zuo Zhang,et al.  Foraging Strategy of Plateau Zokors (Eospalax baileyi Thomas) When Collecting Food for Winter Caches , 2014 .

[5]  Jianzhi Zhang,et al.  Diet shapes the evolution of the vertebrate bitter taste receptor gene repertoire. , 2014, Molecular biology and evolution.

[6]  Tong-zuo Zhang,et al.  Diet selection in overwinter caches of plateau zokor (Eospalax baileyi) , 2014, Acta Theriologica.

[7]  X. Xia DAMBE5: A Comprehensive Software Package for Data Analysis in Molecular Biology and Evolution , 2013, Molecular biology and evolution.

[8]  S. Shabalina,et al.  Sounds of silence: synonymous nucleotides as a key to biological regulation and complexity , 2013, Nucleic acids research.

[9]  E. Nevo,et al.  Effects of Supplemental Dietary Tannic Acid on Digestion in Plateau Zokors (Eospalax baileyi) , 2012 .

[10]  J. Brand,et al.  Major taste loss in carnivorous mammals , 2012, Proceedings of the National Academy of Sciences.

[11]  M. Nei,et al.  MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. , 2011, Molecular biology and evolution.

[12]  Marc J. Lajeunesse,et al.  Plant traits that predict resistance to herbivores , 2011 .

[13]  M. Tomonaga,et al.  Diversification of bitter taste receptor gene family in western chimpanzees. , 2011, Molecular biology and evolution.

[14]  M. Behrens,et al.  The molecular receptive ranges of human TAS2R bitter taste receptors. , 2010, Chemical senses.

[15]  C. China Pharmacopoeia,et al.  Pharmacopoeia of the People's Republic of China , 2010 .

[16]  Lippincott-Schwartz,et al.  Supporting Online Material Materials and Methods Som Text Figs. S1 to S8 Table S1 Movies S1 to S3 a " Silent " Polymorphism in the Mdr1 Gene Changes Substrate Specificity Corrected 30 November 2007; See Last Page , 2022 .

[17]  S. Begall,et al.  Subterranean Rodents: News from Underground , 2007 .

[18]  P. Breslin,et al.  Variability in a taste-receptor gene determines whether we taste toxins in food , 2006, Current Biology.

[19]  Rasmus Wernersson,et al.  Virtual Ribosome—a comprehensive DNA translation tool with support for integration of sequence feature annotation , 2006, Nucleic Acids Res..

[20]  L. Jorde,et al.  Worldwide haplotype diversity and coding sequence variation at human bitter taste receptor loci , 2005, Human mutation.

[21]  Monica C. Chen,et al.  Genomic organization, expression, and function of bitter taste receptors (T2R) in mouse and rat. , 2005, Physiological genomics.

[22]  N. Ryba,et al.  The receptors and coding logic for bitter taste , 2005, Nature.

[23]  John Quackenbush,et al.  The TIGR Gene Indices: clustering and assembling EST and known genes and integration with eukaryotic genomes , 2004, Nucleic Acids Res..

[24]  Per Capita,et al.  About the authors , 1995, Machine Vision and Applications.

[25]  Martin Ebeling,et al.  Evolutionary relationships of the Tas2r receptor gene families in mouse and human. , 2003, Physiological genomics.

[26]  Jianzhi Zhang,et al.  Adaptive diversification of bitter taste receptor genes in Mammalian evolution. , 2003, Molecular biology and evolution.

[27]  C. G. Faulkes Mosaic Evolution of Subterranean Mammals — Regression, Progression and Global Convergence , 2000, Heredity.

[28]  J. Thompson,et al.  The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. , 1997, Nucleic acids research.

[29]  G. Pyke Optimal Foraging Theory: A Critical Review , 1984 .

[30]  J. Sambrook,et al.  Molecular Cloning: A Laboratory Manual , 2001 .

[31]  V. S. Ivlev,et al.  Experimental ecology of the feeding of fishes , 1962 .