Independent evolution of bitter-taste sensitivity in humans and chimpanzees

Abstract

It was reported over 65 years ago that chimpanzees, like humans, vary in taste sensitivity to the bitter compound phenylthiocarbamide (PTC). This was suggested to be the result of a shared balanced polymorphism, defining the first, and now classic, example of the effects of balancing selection in great apes. In humans, variable PTC sensitivity is largely controlled by the segregation of two common alleles at the TAS2R38 locus, which encode receptor variants with different ligand affinities. Here we show that PTC taste sensitivity in chimpanzees is also controlled by two common alleles of TAS2R38; however, neither of these alleles is shared with humans. Instead, a mutation of the initiation codon results in the use of an alternative downstream start codon and production of a truncated receptor variant that fails to respond to PTC in vitro. Association testing of PTC sensitivity in a cohort of captive chimpanzees confirmed that chimpanzee TAS2R38 genotype accurately predicts taster status in vivo. Therefore, although Fisher et al.'s observations were accurate, their explanation was wrong. Humans and chimpanzees share variable taste sensitivity to bitter compounds mediated by PTC receptor variants, but the molecular basis of this variation has arisen twice, independently, in the two species.

Major taste loss in carnivorous mammals

“…Another case of convergent evolution of taste was found in the Tas2r38 receptor gene. Mutations in the Tas2r38 gene have resulted in independent loss of phenylthiocarbamide sensitivity in some humans, chimpanzees, and macaques (30,31). Notably, the mutations in chimpanzees and macaques are start codon mutations, resembling the case with sea lion and fur seal Tas1r2s (30,31).…”

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

“…In particular, exchanging tryptophan in position 201 for leucine or phenylalanine caused severely reduced PTC responsiveness and, practically, a loss of activation by PROP. Intriguingly, Trp-5.46 is found only in the haplorrhine primate clade including human and chimpanzee, which exhibit exquisitely PTC-as well as PROP-sensitive TAS2R38 receptors (33,66). Hence, it seems that PTC/PROP-sensitive TAS2R38 evolved within the Primate order in the haplorrhine branch.…”

African Genetic Diversity: Implications for Human Demographic History, Modern Human Origins, and Complex Disease Mapping

“…Furthermore, Wooding and coworkers (237) showed that PTC taste sensitivity in chimpanzees is associated with different amino acid haplotypes at the TAS2R38 gene compared to humans, implying a unique origin of the taster/nontaster variants in humans and chimpanzees.…”

“…For example, the ability to taste phenylthiocarbamide (PTC), a synthetic bitter substance, is a highly variable trait in humans (83). Although several TAS2R loci contribute to variability in PTC taste perception (54,55), 50%--85% of the phenotypic variance in PTC sensitivity is attributed to variation at the TAS2R38 gene (237).. Studies have identified three amino acid substitutions at TAS2R38 that are in nearly complete LD in non-African populations and that form two common amino acid haplotypes (a taster haplotype PAV and a nontaster haplotype AVI; PAV is dominant). Furthermore, considerably more haplotype variability has been observed in Africa (M.C.…”