Evolution of bitter receptor genes and ontogenetic dietary shift in a frog.

Abstract

Vertebrate Tas2r taste receptors detect bitter compounds that are potentially poisonous. Previous studies found substantial variation in the number of <i>Tas2r</i> genes across vertebrates, with some frog species carrying the largest number. Peculiar among vertebrates, frogs undergo metamorphosis, often associated with a dietary shift between tadpoles and adults. A possible explanation for the large size of frog <i>Tas2r</i> families could be that distinct sets of <i>Tas2r</i> genes are required for tadpoles and adults, suggesting differential expression of <i>Tas2r</i> genes between tadpoles and adults. To test this hypothesis, we first examined 20 amphibian genomes and found that amphibians generally possess more <i>Tas2r</i> genes than do other vertebrate clades. We next focused on the American bullfrog (<i>Lithobates catesbeianus</i>) to examine the expression of its <i>Tas2r</i> genes in herbivorous tadpoles and insectivorous adult frogs. We report that close to one fifth of its 180 <i>Tas2r</i> genes are differentially expressed (22 genes enriched in adults and 11 in tadpoles). Tuning properties were determined for a subset of differentially expressed genes by a cell-based functional assay, with the adult-enriched <i>Tas2r</i> gene set covering a larger range of ligands compared to the tadpole-enriched subset. These results suggest a role of <i>Tas2r</i> genes in the ontogenetic dietary shift of frogs and potentially initiate a new avenue of ontogenetic analysis of diet-related genes in the animal kingdom.