Genomic and genetic evidence for the loss of umami taste in bats

Abstract

Umami taste is responsible for sensing monosodium glutamate, nucleotide enhancers, and other amino acids that are appetitive to vertebrates and is one of the five basic tastes that also include sour, salty, sweet, and bitter. To study how ecological factors, especially diets, impact the evolution of the umami taste, we examined the umami taste receptor gene Tas1r1 in a phylogenetically diverse group of bats including fruit eaters, insect eaters, and blood feeders. We found that Tas1r1 is absent, unamplifiable, or pseudogenized in each of the 31 species examined, including the genome sequences of two species, suggesting the loss of the umami taste in most, if not all, bats regardless of their food preferences. Most strikingly, vampire bats have also lost the sweet taste receptor gene Tas1r2 and the gene required for both umami and sweet tastes (Tas1r3), being the first known mammalian group to lack two of the five tastes. The puzzling absence of the umami taste in bats calls for a better understanding of the roles that this taste plays in the daily life of vertebrates.

FIG. 1.—

The species tree of the bats examined for Tas1r taste receptor genes. The phylogeny and divergence times follow Teeling et al. (2005). Dietary preferences are indicated by various colors, and the functional status of the Tas1r genes is also indicated. Tas1r1 is umami specific, Tas1r2 is sweet specific, and Tas1r3 is used for both tastes. The Tas1r2 data are from Zhao, Zhou, et al. (2010), whereas those of Tas1r1 and Tas1r3 are from the present study.

FIG. 2.—

Alignment of a fragment of Tas1r1 exon 6 from 10 bats, with dog Tas1r1 used as a reference. Dashes (–) indicate alignment gaps and the question marks (?) represent the nucleotides that are not sequenced. Codons in the correct reading frame are indicated by shading and the premature stop codons are boxed. Premature stop codons created by nonsense mutations should appear in the correct reading frame, whereas those created by the indels should appear in an incorrect reading frame. The numbers in parentheses indicate the order of premature stop codons. Regions corresponding to the transmembrane domains (TM2–TM7) are indicated. See figure 1 for the full species names.