Loss of sweet taste despite the conservation of sweet receptor genes in insectivorous bats

Autor: Libiao Zhang, Huan-Wang Xie, Hengwu Jiao, Huabin Zhao, Nima Zhuoma, Peihua Jiang
Rok vydání: 2021
Předmět:
Zdroj: Proceedings of the National Academy of Sciences of the United States of America
ISSN: 1091-6490
0027-8424
DOI: 10.1073/pnas.2021516118
Popis: Significance The sense of taste provides key information on diet, but evolution of taste receptor genes in vertebrates is sometimes unable to predict their feeding ecology. Here we use behavioral experiments and functional assays to demonstrate the loss of sweet taste despite the conservation of sweet receptor genes in insectivorous bats. Although sweet taste receptor genes were highly conserved between frugivorous and insectivorous bats at the sequence level, our behavioral experiments revealed dramatic divergence in two bat species with distinct diets: the insectivorous bat showed no preference for natural sugars, whereas the frugivorous bat showed strong preferences for sucrose and fructose. Our cell-based assays from multiple representative bat species across the phylogeny further supported the behavioral preference tests.
The evolution of taste perception is usually associated with the ecology and dietary changes of organisms. However, the association between feeding ecology and taste receptor evolution is unclear in some lineages of vertebrate animals. One example is the sweet taste receptor gene Tas1r2. Previous analysis of partial sequences has revealed that Tas1r2 has undergone equally strong purifying selection between insectivorous and frugivorous bats. To test whether the sweet taste function is also important in bats with contrasting diets, we examined the complete coding sequences of both sweet taste receptor genes (Tas1r2 and Tas1r3) in 34 representative bat species. Although these two genes are highly conserved between frugivorous and insectivorous bats at the sequence level, our behavioral experiments revealed that an insectivorous bat (Myotis ricketti) showed no preference for natural sugars, whereas the frugivorous species (Rousettus leschenaultii) showed strong preferences for sucrose and fructose. Furthermore, while both sweet taste receptor genes are expressed in the taste tissue of insectivorous and frugivorous bats, our cell-based assays revealed striking functional divergence: the sweet taste receptors of frugivorous bats are able to respond to natural sugars whereas those of insectivorous bats are not, which is consistent with the behavioral preference tests, suggesting that functional evolution of sweet taste receptors is closely related to diet. This comprehensive study suggests that using sequence conservation alone could be misleading in inferring protein and physiological function and highlights the power of combining behavioral experiments, expression analysis, and functional assays in molecular evolutionary studies.
Databáze: OpenAIRE