Genes from the TAS1R and TAS2R Families of Taste Receptors: Looking for Signatures of Their Adaptive Role in Human Evolution

Abstract

Taste perception is crucial in monitoring food intake and, hence, is thought to play a significant role in human evolution. To gain insights into possible adaptive signatures in genes encoding bitter, sweet, and umami taste receptors, we surveyed the available sequence variation data from the 1000 Genomes Project Phase 3 for TAS1R (TAS1R1-3) and TAS2R (TAS2R16 and TAS2R38) families. Our study demonstrated that genes from these two families have experienced contrasting evolutionary histories: While TAS1R1 and TAS1R3 showed worldwide evidence of positive selection, probably correlated with improved umami and sweet perception, the patterns of variation displayed by TAS2R16 and TAS2R38 were more consistent with scenarios of balancing selection that possibly conferred a heterozygous advantage associated with better capacity to perceive a wide range of bitter compounds. In TAS2R16, such adaptive events appear to have occurred restrictively in mainland Africa, whereas the strongest evidence in TAS2R38 was detected in Europe. Despite plausible associations between taste perception and the TAS1R and TAS2R selective signatures, we cannot discount other biological mechanisms as driving the evolutionary trajectories of those TAS1R and TAS2R members, especially given recent findings of taste receptors behaving as the products of pleiotropic genes involved in many functions outside the gustatory system.

Fig. 1.

—Networks from TAS1R genes. Each node represents a different haplotype, and the line length is proportional to the number of mutations along the branch. In the colored networks, circle sizes are proportional to frequencies, which were not considered in the black-and-white network versions. (A) TAS1R1. The haplotypes discriminated are defined by the nonsynonymous variations shown in red, C329T and G1114A. (B) TAS1R2. (C) TAS1R3 encompassing the promoter and the exon–intron region. The haplotypes discriminated are defined by the variations shown in red -T1572C and -T1266C from the promoter, plus G13A and C2269T from the exon–intron region. Variation rs35946613 shown in blue is located in the promoter.

Fig. 2.

—Coalescent-based genealogy, TMRCA of global variation, and ages of individual mutations at TAS1R genes. Mutations are represented by black dots, and figures on the bottom of branches correspond to the number of individuals with that haplotype (x means except). (A) TAS1R1 and (B) TAS1R3. Variations in red and blue as in legend for figure 1.

Fig. 3.

—Networks from TAS2R genes. Each node represents a different haplotype and line length is proportional to the number of mutations along the branch. In the colored networks, circle sizes are proportional to frequencies, which were not considered in the black-and-white network versions. (A) TAS2R16. The alleles discriminated are from the variation shown in red G516T. rs860170, shown in blue, is a nonsynonymous substitution. (B) TAS2R38. The haplotypes discriminated are defined by the variations shown in red P49A, A262V, and V296I (according to residue substitution).

Fig. 4.

—Coalescent-based genealogy, TMRCA of global variation, and ages of individual mutations at TAS2R genes. Mutations are represented by black dots, and figures on the bottom of branches correspond to the number of individuals with that haplotype. (A) TAS2R16. (B) TAS2R38. Variations in red and blue as in legend for figure 3.