Birds Generally Carry a Small Repertoire of Bitter Taste Receptor Genes

Abstract

As they belong to the most species-rich class of tetrapod vertebrates, birds have long been believed to possess an inferior taste system. However, the bitter taste is fundamental in birds to recognize dietary toxins (which are typically bitter) in potential food sources. To characterize the evolution of avian bitter taste receptor genes (Tas2rs) and to test whether dietary toxins have shaped the repertoire size of avian Tas2rs, we examined 48 genomes representing all but 3 avian orders. The total number of Tas2r genes was found to range from 1 in the domestic pigeon to 12 in the bar-tailed trogon, with an average of 4, which suggested that a much smaller Tas2r gene repertoire exists in birds than in other vertebrates. Furthermore, we uncovered a positive correlation between the number of putatively functional Tas2rs and the abundance of potential toxins in avian diets. Because plant products contain more toxins than animal tissues and insects release poisonous defensive secretions, we hypothesized that herbivorous and insectivorous birds may demand more functional Tas2rs than carnivorous birds feeding on noninsect animals. Our analyses appear to support this hypothesis and highlight the critical role of taste perception in birds.

Keywords: Tas2r; birds; bitter taste; diet; feeding ecology.

Fig. 1.—

The bitter taste receptor gene repertoires of 48 birds and their dietary preferences. Species tree and divergence times were taken from a recent study (Jarvis et al. 2014). Dietary information was from the literature and the Animal Diversity Web (supplementary table S1, Supplementary Material online). C, carnivore; I, insectivore; F, frugivore; Fo, folivore; G, granivore; N, nectarivore; O, omnivore.

Fig. 2.—

Evolutionary relationships of all 136 intact Tas2r genes from 48 birds and 3 crocodilians. The tree was reconstructed using the Bayesian approach with the best fitting model of GTR+I+G. Branch lengths were drawn to the scale. Putative species-specific gene duplications were marked in the branches with various colors, and members from Passeriformes were bracketed. The detailed information about species and gene names and Bayesian posterior probabilities was shown in supplementary fig. S1, Supplementary Material online, and the NJ tree showing a similar topology to this tree was provided in supplementary fig. S3, Supplementary Material online.

Fig. 3.—

Evolutionary changes of intact Tas2r gene numbers in 48 birds and 3 crocodilians. The estimated Tas2r gene numbers for ancestral lineages were shown with black, whereas the numbers of gene gains and gene losses were indicated with purple and green, respectively.

Fig. 4.—

Dietary preferences impact the avian Tas2r gene repertoires. (A) PIC in putatively functional Tas2r gene number is positively correlated with that in diet preference; (B) PIC in total Tas2r gene number remains an increasing trend as PIC in diet codes increases, although it was only marginally significant. According to the amount of potential toxins in its diet, each bird was coded as 0 (carnivore), 1 (folivore), 1 (insectivore), 1 (frugivore), 1 (granivore), 1 (nectarivore), and 1 (omnivore). The Spearman’s rank correlation coefficient (ρ) with a two-tailed P value was used to evaluate the association.