Lineage-specific evolution of bitter taste receptor genes in the giant and red pandas implies dietary adaptation

Abstract

Taste 2 receptors (TAS2R) mediate bitterness perception in mammals, thus are called bitter taste receptors. It is believed that these genes evolved in response to species‐specific diets. The giant panda (Ailuropoda melanoleuca) and red panda (Ailurus fulgens styani) in the order Carnivora are specialized herbivores with an almost exclusive bamboo diet (>90% bamboo). Because bamboo is full of bitter tasting compounds, we hypothesized that adaptive evolution has occurred at TAS2R genes in giant and red pandas throughout the course of their dietary shift. Here, we characterized 195 TAS2R genes in 9 Carnivora species and examined selective pressures on these genes. We found that both pandas harbor more putative functional TAS2R genes than other carnivores, and pseudogenized TAS2R genes in the giant panda are different from the red panda. The purifying selection on TAS2R1, TAS2R9 and TAS2R38 in the giant panda, and TAS2R62 in the red panda, has been strengthened throughout the course of adaptation to bamboo diet, while selective constraint on TAS2R4 and TAS2R38 in the red panda is relaxed. Remarkably, a few positively selected sites on TAS2R42 have been specifically detected in the giant panda. These results suggest an adaptive response in both pandas to a dietary shift from carnivory to herbivory, and TAS2R genes evolved independently in the 2 pandas. Our findings provide new insight into the molecular basis of mammalian sensory evolution and the process of adaptation to new ecological niches.

TAS2R20 variants confer dietary adaptation to high‐quercitrin bamboo leaves in Qinling giant pandas

“…Bitter taste perception provides an important means for animals to detect bitter compounds in the environments that they occupy. As animals explore new environments and diets, they may encounter distinct bitterness, which imposes selective pressure on their bitter taste receptor genes, leading to individual differences in bitter taste sensitivity (Li & Zhang, 2013;Shan et al, 2018;Shi, Zhang, Yang, & Zhang, 2003;Wooding et al, 2006). The TAS2R genes of the giant panda are expected to have experienced selective pressure during the course of the dietary shift of pandas from carnivorous to omnivorous to herbivorous and, finally, their specialization for bamboo consumption.…”

“…Multiple lines of evidences indicate that plants have been components of pandas' diet for several million years, and this type of diet poses the challenge of tolerating large amounts of bitter compounds. Our previous work showed that there are more putatively functional TAS2Rs in the giant panda than in other carnivores, which might be expected because the abundant bitter substances encountered by pandas could lead to a requirement for more functional TAS2Rs for bitter taste perception (Shan et al, 2018).…”

“…Animals taste receptor genes evolve in response to species-specific diets (Jiang et al, 2012;Li et al, 2005;Liu et al, 2016;Sato & Wolsan, 2012;Shan, Wu, Wang, Zhang, & Wei, 2018;Zhao, Yang, Xu, & Zhang, 2010). Food-derived compounds stimulate taste receptors on specialized cells within taste buds, causing pleasant or unpleasant sensations and, thus, influencing the dietary preferences of animals (Breslin, 2013;Chandrashekar, Hoon, Ryba, & Zuker, 2006;Fujikura, 2015).…”

“…TAS2R49 is now designated as TAS2R20 according to the last Gene Nomenclature Committee of the Human Genome Organization (http://www.genen ames.org/, last accessed April 30, 2016), and this gene has been directionally selected at two nonsynonymous sites A52V and Q296H in the panda population from the Qinling Mountains (Qinling pandas) (Shan et al, 2018;Zhao et al, 2013).…”

Vertical Clinging and Leaping Ahead: How Bamboo Has Shaped the Anatomy and Physiology of Hapalemur

“…If they do have bitter taste receptors, that might suggest that they are at least acutely aware of the toxicity of the specific part they are consuming. By retaining some taste, the bamboo lemurs could be selecting less bitter and less toxic parts of the shoot, as bamboo-consuming pandas are suggested to do (Shan et al, 2018). If they lack the ability to taste cyanide, then they either use another method to discern cyanide composition or they simply ignore it.…”