Evolution of the sweet taste receptor gene Tas1r2 in bats

Abstract

Taste perception is an important component of an animal's fitness. The identification of vertebrate taste receptor genes in the last decade has enabled molecular genetic studies of the evolution of taste perception in the context of the ecology and dietary preferences of organisms. Although such analyses have been conducted in a number of species for bitter taste receptors, a similar analysis of sweet taste receptors is lacking. Here, we survey the sole sweet taste-specific receptor gene Tas1r2 in 42 bat species that represent all major lineages of the order Chiroptera, one of the most diverse groups of mammals in terms of diet. We found that Tas1r2 is under strong purifying selection in the majority of the bats studied, with no significant difference in the strength of the selection between insect eaters and fruit eaters. However, Tas1r2 is a pseudogene in all three vampire bat species and the functional relaxation likely started in their common ancestor, probably due to the exclusive feeding of vampire bats on blood and their reliance on infrared sensors rather than taste perception to locate blood sources. Our survey of available genome sequences, together with previous reports, revealed additional losses of Tas1r2 in horse, cat, chicken, zebra finch, and western clawed frog, indicating that sweet perception is not as conserved as previously thought. Nonetheless, we found no common dietary pattern among the Tas1r2-lacking vertebrates, suggesting different causes for the losses of Tas1r2 in different species. The complexity of the ecological factors that impact the evolution of Tas1r2 calls for a better understanding of the physiological roles of sweet perception in different species.

FIG. 1.

The species tree of the 42 bats studied, with the dietary preferences indicated by various colors. The tree topology and approximate divergence times follow Teeling et al. (2005). The common ancestor of vampire bats discussed in the paper is marked with a solid circle. Branch colors indicate sets of branches used in testing the selective pressures on Tas1r2 in Table 1.

FIG. 2.

Alignment of Tas1r2 nucleotide sequences from the three vampire bats and one New World fruit bat for the regions examined in this work. Dashes indicate alignment gaps and question marks represent unamplified nucleotides. Codons in the correct reading frame are indicated by shading and premature stop codons are boxed. Regions corresponding to the seven transmembrane (TM) domains are indicated.

FIG. 3.

Evolutionary trees of combined Cytb and RAG2 genes from the three vampire bats and two New World fruit bats. (a) The NJ tree. Bootstrap percentages from 500 replications are shown on interior branches. (b) The linearized tree. Estimated divergence dates are shown with open arrow heads, whereas the calibration time is indicated with a solid arrow head. The scale shows the Tamura-Nei distance.

FIG. 4.

A species tree of mammals marked with multiple losses of functional Tas1r2. The Tas1r2 genes studied by amplification and sequencing of Tas1r2 are underlined, whereas those studied by genome sequence analysis are not. Birds are used as the outgroup of mammals. Note that Tas1r2 originated in the common ancestor of bony vertebrates (Grus and Zhang 2009), and therefore, the absence of Tas1r2 in individual mammalian and avian species are due to gene losses.