Differentiated adaptive evolution, episodic relaxation of selective constraints, and pseudogenization of umami and sweet taste genes TAS1Rs in catarrhine primates

Abstract

BackgroundUmami and sweet tastes are two important basic taste perceptions that allow animals to recognize diets with nutritious carbohydrates and proteins, respectively. Until recently, analyses of umami and sweet taste were performed on various domestic and wild animals. While most of these studies focused on the pseudogenization of taste genes, which occur mostly in carnivores and species with absolute feeding specialization, omnivores and herbivores were more or less neglected. Catarrhine primates are a group of herbivorous animals (feeding mostly on plants) with significant divergence in dietary preference, especially the specialized folivorous Colobinae. Here, we conducted the most comprehensive investigation to date of selection pressure on sweet and umami taste genes (TAS1Rs) in catarrhine primates to test whether specific adaptive evolution occurred during their diversification, in association with particular plant diets.ResultsWe documented significant relaxation of selective constraints on sweet taste gene TAS1R2 in the ancestral branch of Colobinae, which might correlate with their unique ingestion and digestion of leaves. Additionally, we identified positive selection acting on Cercopithecidae lineages for the umami taste gene TAS1R1, on the Cercopithecinae and extant Colobinae and Hylobatidae lineages for TAS1R2, and on Macaca lineages for TAS1R3. Our research further identified several site mutations in Cercopithecidae, Colobinae and Pygathrix, which were detected by previous studies altering the sensitivity of receptors. The positively selected sites were located mostly on the extra-cellular region of TAS1Rs. Among these positively selected sites, two vital sites for TAS1R1 and four vital sites for TAS1R2 in extra-cellular region were identified as being responsible for the binding of certain sweet and umami taste molecules through molecular modelling and docking.ConclusionsOur results suggest that episodic and differentiated adaptive evolution of TAS1Rs pervasively occurred in catarrhine primates, most concentrated upon the extra-cellular region of TAS1Rs.Electronic supplementary materialThe online version of this article (doi:10.1186/s12983-014-0079-4) contains supplementary material, which is available to authorized users.

Expansion of sweet taste receptor genes in grass carp (Ctenopharyngodon idellus) coincided with vegetarian adaptation

“…Sweet taste "blindness" observed in some carnivorous mammals, such as domestic cat, California sea lion, southern fur seal, Pacific harbor seal, Asian small-clawed otter, spotted hyena, fossa, banded linsang, bottlenose dolphin, and vampire bats, have been suggested to be the consequence of pseudogenization of T1R2 since they do not require the receptor for sweet food perception [6,7,10,11]. However, almost all omnivorous and herbivorous mammals with the habit to consume sugars have a functional T1R2 structure [6,7,10,[12][13][14][15]. Unlike pseudogenization of T1R2 in some carnivorous mammals, the evolution of sweet taste in birds is in absence of T1R2 despite food habits [16][17][18].…”

High maltose sensitivity of sweet taste receptors in the Japanese macaque (Macaca fuscata)

“…In addition, these results suggested that the maltose response is related to both Tas1R2 and Tas1R3, indicating that the critical amino acids for binding are different from those for sucrose. In comparisons of Tas1R2 and Tas1R3 VFTD between Hominidae and Cercopithecinae, mutations at 45 and 43 amino acid residues have been observed, respectively13. We infer that these mutations affect sweet taste sensitivity to natural sugars by changing Tas1R2/Tas1R3 function.…”

“…Primate species have various mutations in Tas1R2 and Tas1R3 13. Generally, most sweet taste compounds bind to a huge external membrane domain called the venus flytrap domain (VFTD) of Tas1R214.…”

Potential arms race in the coevolution of primates and angiosperms: brazzein sweet proteins and gorilla taste receptors

“…We obtained TAS1R3 nucleotide sequences from Liu et al () and by searching for the gene name or BLASTing the human sequence against the NCBI and Ensembl databases (Supporting Information Table 1). Hence, we compiled all of the primate TAS1R sequences currently available via Genbank, genome browsers and short read archives.…”