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.

Vampire bats exhibit evolutionary reduction of bitter taste receptor genes common to other bats

“…B 281: 20141079 mutations, and T2R3 and T2R38 contain disruptive mutations in one of the three vampire bats, suggesting that the four genes were pseudogenized independently. Therefore, we found extensive losses of T2Rs in vampire bats, but the common disruptive mutations that cause pseudogenization among all three vampire bats are absent, despite them sharing a common ancestry of blood-feeding [9,30,31].…”

“…Genomic DNAs were isolated using Qiagen DNeasy kits. Polymerase chain reactions (PCRs) were performed following our previously described methods [9,10]. PCR products were sequenced directly with the same primer sets as for PCR amplifications.…”

“…Furthermore, vampire bats use odour cues for prey detection [12] and use infrared sensors to locate capillary-rich areas of skin [7,13]. These capabilities may have further reduced their taste sensitivity [9]. To test whether bitter taste receptor genes (T2Rs) have been relaxed from selective constraint in vampire bats, we sampled all three vampire bats and 11 non-vampire bats across the phylogeny and examined nine one-to-one orthologous T2Rs that are shared in four bats representing two major groups of bats (Yangochiroptera and Yinpterochiroptera) and thus are assumed to be functionally conserved in all bats.…”

Major taste loss in carnivorous mammals

“…We proposed that this behavioral insensitivity was a consequence of the pseudogenization of Tas1r2 (14). Tas1r2 also is known to be pseudogenized in chicken, tongueless Western clawed frogs, and vampire bats (11,15). The loss of the sweet taste receptor in chicken and vampire bats is consistent with their sweet insensitive behavior (16,17).…”

Mismatches between feeding ecology and taste receptor evolution: An inconvenient truth

“…It is probable that the pseudogenization of Tas1r2 in vampire bats is related to the narrowness of their diet rather than the specific diet they use. Tas1r2 is also missing in the genome sequences of the herbivorous horse and omnivorous pig, but no satisfactory explanation exists (2). Furthermore, Tas1r2 is absent in all bird genomes sequenced thus far (2), irrespective of their diet.…”