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

Abstract

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.

TAS1 receptors. An overview of their functions, expression and genetic variations

“…Finally, various in vitro experiments were conducted in order to identify why the insectivorous bats lost their ability to perceive sweetness. The researchers concluded that the VFD of the TAS1R3 version from insectivorous bats is modified, making the protein unresponsive to sugars (Jiao et al, 2021). In contrast, another study investigating 42 species of bats found that the Tas1r2 gene is under the same level of purifying selection in both fruit and insect eating bats.…”

Understanding the evolution of nutritive taste in animals: Insights from biological stoichiometry and nutritional geometry

“…The loss of taste receptor function has been linked, in part, to evolutionary shifts in feeding ecology, including dietary specialization, that reduce the selective pressures on taste receptor genes (Feng et al, 2014;Jiang et al, 2012aJiang et al, , 2012bLiu et al, 2016;Zhao et al, 2010Zhao et al, , 2012. For example, sweet taste has been independently lost in multiple lineages of terrestrial carnivores, including the strictly carnivorous felids, cetaceans, vampire bats (Antinucci & Risso, 2017;Jiang et al, 2012a;Zhao et al, 2012), and insectivorous bats (Jiao et al, 2021). This loss of sweet taste has been linked to pseudogenization of the T1R2 (sweet) receptor gene following dietary shifts toward obligate carnivory (Antinucci & Risso, 2017) as the relative lack of carbohydrates in animal tissue is thought to reduce selective pressure for maintaining a functioning sweet taste receptor (Jiang et al, 2012a).…”

Role of feeding specialization in taste receptor loss: insights from sweet and umami receptor evolution in Carnivora

“…Nevertheless, Zhao and Zhang (2012) pointed to mismatches between feeding specializations and taste receptor presence/absence in mammals and birds and concluded that Jiang et al’s (2012a) hypothesis is unwarranted. The role of feeding specialization in taste receptor loss has been debated since then and is currently subject of controversy and misunderstanding ( Jiang et al 2012b ; Feng and Zhao 2013 ; Liu et al 2016 ; Feng and Liang 2018 ; Jiao et al 2021 ; Zhong et al 2021 ).…”

“…This is because protein dysfunction may also result from a regulatory mutation that abolishes gene expression or an unapparent coding-region missense mutation that causes crucial change in protein structure ( Albalat and Cañestro 2016 ). It is of note that Jiao et al (2021) postulated loss of the sweet taste receptor despite apparently intact TAS1R2 and TAS1R3 in insectivorous bats based on their indifference toward sucrose, fructose, and glucose. However, the TAS1R2+TAS1R3 heterodimer of these bats responded to an artificial sweetener, neohesperidin dihydrochalcone, and possibly may respond to carbohydrates contained in insects that were not tested by Jiao et al (2021) , e.g., trehalose, the principal sugar circulating in insect hemolymph ( Gillott 2005 ).…”

“…It is of note that Jiao et al (2021) postulated loss of the sweet taste receptor despite apparently intact TAS1R2 and TAS1R3 in insectivorous bats based on their indifference toward sucrose, fructose, and glucose. However, the TAS1R2+TAS1R3 heterodimer of these bats responded to an artificial sweetener, neohesperidin dihydrochalcone, and possibly may respond to carbohydrates contained in insects that were not tested by Jiao et al (2021) , e.g., trehalose, the principal sugar circulating in insect hemolymph ( Gillott 2005 ). Moreover, given the time that has elapsed since the purported convergent loss of the sweet receptor from insectivorous bats (~20 to ~50 million years depending on the clade— Jiao et al 2021 ), lack of any recognizable inactivating mutations in the insectivorous bat TAS1R2 is unexpected.…”