Reply to Zhao and Zhang: Loss of taste receptor function in mammals is directly related to feeding specializations

Jiang, Peihua; Josue, Jesusa; Li, Xia; Gläser, Dieter; Li, Weihua; Brand, Joseph G.; Margolskee, Robert F.; Reed, Danielle R.; Beauchamp, Gary K.

doi:10.1073/pnas.1205581109

Cited by 6 publications

(9 citation statements)

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“…We and others have argued that taste function and diet are intimately connected through coordinated evolutionary processes that fit one to the other [1] , [2] , [3] , [4] . Specifically for sweet taste, animal species that routinely consume plants express taste preferences for simple sugars and have functional sweet taste receptors (T1R2+T1R3), whereas many species that do not consume plants (e.g., strict carnivores) often do not prefer sugars and during evolution have lost sweet taste receptor function through detrimental mutations [1] , [2] , [5] , [6] . It is thought that selection to maintain sweet taste receptor function is due to the need to identify plants rich in calories that are provided by the presence of simple sugars.…”

Section: Introductionmentioning

confidence: 99%

The Bamboo-Eating Giant Panda (Ailuropoda melanoleuca) Has a Sweet Tooth: Behavioral and Molecular Responses to Compounds That Taste Sweet to Humans

Jiang

Josue-Almqvist

Jin³

et al. 2014

PLoS ONE

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A growing body of behavioral and genetic information indicates that taste perception and food sources are highly coordinated across many animal species. For example, sweet taste perception is thought to serve to detect and motivate consumption of simple sugars in plants that provide calories. Supporting this is the observation that most plant-eating mammals examined exhibit functional sweet perception, whereas many obligate carnivores have independently lost function of their sweet taste receptors and exhibit no avidity for simple sugars that humans describe as tasting sweet. As part of a larger effort to compare taste structure/function among species, we examined both the behavioral and the molecular nature of sweet taste in a plant-eating animal that does not consume plants with abundant simple sugars, the giant panda (Ailuropoda melanoleuca). We evaluated two competing hypotheses: as plant-eating mammals, they should have a well-developed sweet taste system; however, as animals that do not normally consume plants with simple sugars, they may have lost sweet taste function, as has occurred in strict carnivores. In behavioral tests, giant pandas avidly consumed most natural sugars and some but not all artificial sweeteners. Cell-based assays revealed similar patterns of sweet receptor responses toward many of the sweeteners. Using mixed pairs of human and giant panda sweet taste receptor units (hT1R2+gpT1R3 and gpT1R2+hT1R3) we identified regions of the sweet receptor that may account for behavioral differences in giant pandas versus humans toward various sugars and artificial sweeteners. Thus, despite the fact that the giant panda's main food, bamboo, is very low in simple sugars, the species has a marked preference for several compounds that taste sweet to humans. We consider possible explanations for retained sweet perception in this species, including the potential extra-oral functions of sweet taste receptors that may be required for animals that consume plants.

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Section: Introductionmentioning

confidence: 99%

The Bamboo-Eating Giant Panda (Ailuropoda melanoleuca) Has a Sweet Tooth: Behavioral and Molecular Responses to Compounds That Taste Sweet to Humans

Jiang

Josue-Almqvist

Jin³

et al. 2014

PLoS ONE

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“…and whales (Cetacea) [21,23,24]. Although the Colobinae display a certain degree of dietary specialization and feeds mainly on leaves, no massive loss of TAS1R genes was found.…”

Section: Discussionmentioning

confidence: 99%

“…For example, TAS1R1 is a pseudogene in the herbivorous giant panda (family Ursidae) [20,21], and the TAS1R2 gene is inactivated in cats (family Felidae), vampire bats, chickens, zebra finches, the western clawed frog, and some carnivorous mammals [5,22,23]. However, research on the evolution of sweet and umami taste genes revealed that taste perception of sweet and umami is not be as conserved as previously thought, and the structural integrity of TAS1R is sometimes inconsistent with the known functions of these genes and the tastes involved [24]. For example, although TAS1R2 is a pseudogene in some species of carnivores, some other obligate carnivores (such as ferrets and Canadian otters) still possess an intact TAS1R2 gene [25].…”

Section: Introductionmentioning

confidence: 99%

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

et al. 2014

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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.

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“…Understanding why some animal species possess, or lack, certain taste senses has generated considerable interest among taste researchers, particularly in cases where specific taste functions have been lost within some animal lineages (12, 13). 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 (11, 12, 69, 70, 71, 72). For example, sweet taste has been independently lost in multiple lineages of terrestrial carnivores, including the strictly carnivorous felids, cetaceans, and vampire bats (12, 13, 71).…”

Section: Lack and Loss Of Taste Senses Among Animal Speciesmentioning

confidence: 99%

Understanding the Evolution of Nutritive Taste in Animals: Insights from Biological Stoichiometry and Nutritional Geometry

Demi

Taylor

Reading

et al. 2021

Preprint

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A major conceptual gap in taste biology is the lack of a general framework for understanding the evolution of different taste modalities among animal species. We turn to two complementary nutritional frameworks, biological stoichiometry theory and nutritional geometry, to develop hypotheses for the evolution of different taste modalities in animals. We describe how the attractive tastes of Na, Ca, P, N and C containing compounds are consistent with principles of both frameworks based on their shared focus on nutritional imbalances and consumer homeostasis. Specifically, we suggest that the evolution of multiple nutritive taste modalities can be predicted by identifying individual elements that are typically more concentrated in the tissues of animals than plants. Additionally, we discuss how consumer homeostasis can inform our understanding of why some taste compounds (i.e., Na, Ca and P salts) can be either attractive or aversive depending on concentration. We also discuss how these complementary frameworks can help to explain the phylogenetic distribution of different taste modalities and improve our understanding of the mechanisms that lead to loss of taste capabilities in some animal lineages. The ideas presented here will stimulate research that bridges the fields of evolutionary biology, sensory biology and ecology.

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Reply to Zhao and Zhang: Loss of taste receptor function in mammals is directly related to feeding specializations

Cited by 6 publications

References 6 publications

The Bamboo-Eating Giant Panda (Ailuropoda melanoleuca) Has a Sweet Tooth: Behavioral and Molecular Responses to Compounds That Taste Sweet to Humans

The Bamboo-Eating Giant Panda (Ailuropoda melanoleuca) Has a Sweet Tooth: Behavioral and Molecular Responses to Compounds That Taste Sweet to Humans

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

Understanding the Evolution of Nutritive Taste in Animals: Insights from Biological Stoichiometry and Nutritional Geometry

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