Diet Shapes the Evolution of the Vertebrate Bitter Taste Receptor Gene Repertoire

Abstract

Vertebrate Tas2r taste receptors bind to bitter compounds, which are typically poisonous, to elicit bitter sensation to prevent the ingestion of toxins. Previous studies noted a marked variation in the number of Tas2r genes among species, but the underlying cause is unclear. To address this question, we compile the Tas2r gene repertoires from 41 mammals, 4 birds, 2 reptiles, 1 amphibian, and 6 fishes. The number of intact Tas2r genes varies from 0 in the bottlenose dolphin to 51 in the Western clawed frog, with numerous expansions and contractions of the gene family throughout vertebrates, especially among tetrapods. The Tas2r gene number in a species correlates with the fraction of plants in its diet. Because plant tissues contain more toxic compounds than animal tissues do, our observation supports the hypothesis that dietary toxins are a major selective force shaping the diversity of the Tas2r repertoire.

Gourds and squashes ( Cucurbita spp.) adapted to megafaunal extinction and ecological anachronism through domestication

“…Previous studies have reported that herbivores have slightly higher TAS2R copies than carnivores, presumably to detect plant-based toxins more acutely (30), and that the common ancestor of modern whales completely lost functional TAS2R copies, probably as a result of feeding behaviors and the switch to a marine environment (33). Similarly, in our analysis, dietary breadth is significantly correlated with TAS2R count, presumably because a wider range of possible food species necessitates sensitivity to a more diverse range of toxic compounds, and because narrow dietary specialists have little need for toxin detection.…”

“…Larger numbers of intact TAS2R genes are associated with greater ability to detect and avoid toxins via their bitterness, and interspecific variation in copy number is hypothesized to reflect ecological and evolutionary diversity (30)(31)(32). Previous studies have reported that herbivores have slightly higher TAS2R copies than carnivores, presumably to detect plant-based toxins more acutely (30), and that the common ancestor of modern whales completely lost functional TAS2R copies, probably as a result of feeding behaviors and the switch to a marine environment (33).…”

“…To identify intact, putatively functional TAS2R gene copies in the mammalian genomes, we first adapted the strategy of Li and Zhang (30) by generating BLAST databases (54) from each genome assembly and queried them for the annotated human (n = 25) and mouse (n = 35) TAS2R protein sequences (30) using TBlastN, enforcing an e-value threshold of ≤10 −10 . This approach previously has proven robust for localizing TAS2R variants across diverse species, with conserved transmembrane domains in TAS2R genes providing reliable amino acid targets for the TBlastN queries (30). From the TBlastN output, we generated a bed file for each species containing genomic coordinates of candidate TAS2R regions, merged overlapping regions, added 100 nucleotides to each flank, and used BEDtools (55) to generate nucleotide FASTA files for the corresponding regions from the genome assemblies.…”

Vampire bats exhibit evolutionary reduction of bitter taste receptor genes common to other bats

“…Although vertebrate bitter taste receptor genes (T2Rs or Tas2rs) diverge tremendously in number from 0 in the bottlenose dolphin to 51 in the African clawed frog [2], multiple intact T2Rs are maintained to ensure the functionality of detecting toxins in food sources for these animals, with the exception of the bottlenose dolphin [2,3]. The dolphin represents the first mammal to lack functional bitter taste receptors, probably because they swallow food whole, rendering the taste dispensable [3].…”

Comprehensive Analysis of Mouse Bitter Taste Receptors Reveals Different Molecular Receptive Ranges for Orthologous Receptors in Mice and Humans

“…In higher vertebrates frequent independent expansions and pseudogenization events resulted in differently sized Tas2r gene repertoires (12). Consequently, the number of putatively functional Tas2r genes varies considerably in vertebrates, ranging from 0 in baleen and tooth whales as well as penguins (13)(14)(15)(16) to more than 50 in Western clawed frogs and 80 in Coelacanth (17)(18)(19)(20). Thus, humans with ϳ25 and mice with ϳ35 putatively functional members possess average size Tas2r repertoires (21).…”