Pseudogenization of the umami taste receptor gene Tas1r1 in the giant panda coincided with its dietary switch to bamboo

Abstract

Although it belongs to the order Carnivora, the giant panda is a vegetarian with 99% of its diet being bamboo. The draft genome sequence of the giant panda shows that its umami taste receptor gene Tas1r1 is a pseudogene, prompting the proposal that the loss of the umami perception explains why the giant panda is herbivorous. To test this hypothesis, we sequenced all six exons of Tas1r1 in another individual of the giant panda and five other carnivores. We found that the open reading frame (ORF) of Tas1r1 is intact in all these carnivores except the giant panda. The rate ratio (ω) of nonsynonymous to synonymous substitutions in Tas1r1 is significantly higher for the giant panda lineage than for other carnivore lineages. Based on the ω change and the observed number of ORF-disrupting substitutions, we estimated that the functional constraint on the giant panda Tas1r1 was relaxed ∼ 4.2 Ma, with its 95% confidence interval between 1.3 and 10 Ma. Our estimate matches the approximate date of the giant panda's dietary switch inferred from fossil records. It is probable that the giant panda's decreased reliance on meat resulted in the dispensability of the umami taste, leading to Tas1r1 pseudogenization, which in turn reinforced its herbivorous life style because of the diminished attraction of returning to meat eating in the absence of Tas1r1. Nonetheless, additional factors are likely involved because herbivores such as cow and horse still retain an intact Tas1r1.

FIG. 1.

A species tree of the carnivores studied in this work. Branch lengths are not drawn to scale except for the giant panda branch. Dates indicated by blue arrows are inferred from fossil records, whereas dates indicated with the purple arrow and dash lines are inferred from the molecular genetic evidence of this study.

FIG. 2.

Posterior probability distributions of the time at which the functional constraint on the giant panda Tas1r1 was completely relaxed, based on the observations from (A) the rate of nucleotide substitutions, (B) the number of ORF-disrupting substitutions, and (C) both.