Lowered sensitivity of bitter taste receptors to β-glucosides in bamboo lemurs: an instance of parallel and adaptive functional decline in TAS2R16?

Itoigawa, Akihiro; Fierro, Fabrizio; Chaney, Morgan E.; Lauterbur, M. Elise; Hayakawa, Takashi; Tosi, Anthony J.; Niv, Masha Y.; Imai, Hiroo

doi:10.1098/rspb.2021.0346

Cited by 10 publications

(17 citation statements)

References 52 publications

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“…Frugivorous and nectarivorous primates, for example, are highly sensitive to sugars found in fruit and nectar, for example, fructose and ethanol 53,196–200 . By contrast, folivores exhibit reduced sensitivity to some bitter compounds, particularly to β‐glucopyranosides and glucosinolates 180,198,201,202 . Paradoxically, leaf‐eating is also associated with an expansion of other bitter taste receptor genes ( TAS2R s), allowing folivores to detect a greater breadth of compounds 177 .…”

Section: Overview Of Current Knowledgementioning

confidence: 99%

The sensory ecology of primate food perception, revisited

Veilleux

Dominy

Melin

2022

Evolutionary Anthropology

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Twenty years ago, Dominy and colleagues published “The sensory ecology of primate food perception,” an impactful review that brought new perspectives to understanding primate foraging adaptations. Their review synthesized information on primate senses and explored how senses informed feeding behavior. Research on primate sensory ecology has seen explosive growth in the last two decades. Here, we revisit this important topic, focusing on the numerous new discoveries and lines of innovative research. We begin by reviewing each of the five traditionally recognized senses involved in foraging: audition, olfaction, vision, touch, and taste. For each sense, we provide an overview of sensory function and comparative ecology, comment on the state of knowledge at the time of the original review, and highlight advancements and lingering gaps in knowledge. Next, we provide an outline for creative, multidisciplinary, and innovative future research programs that we anticipate will generate exciting new discoveries in the next two decades.

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Section: Overview Of Current Knowledgementioning

confidence: 99%

The sensory ecology of primate food perception, revisited

Veilleux

Dominy

Melin

2022

Evolutionary Anthropology

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“…The general tendency in salicin sensitivity associated with feeding habits was not found across mammals. As reported in the primate studies ( Imai et al 2012 ; Itoigawa et al 2019 ; Purba et al 2020 ; Itoigawa et al 2021 ; Yang et al 2021 ), functional changes of TAS2Rs in agonist sensitivity had occurred many times independently within the order, family, or genus level by each ecological and evolutionary background. To understand the differences of agonist sensitivity in each species tested in this study, comparative analyses within more closely related species are required.…”

Section: Discussionmentioning

confidence: 65%

“…Tested substances listed in supplementary table S3, Supplementary Material online were commercially purchased and dissolved in the assay buffer (130 mM NaCl, 10 mM glucose, 5 mM KCl, 2 mM CaCl 2 , 1.2 mM MgCl 2 , 10 mM HEPES, pH 7.4), or in dimethyl sulfoxide (DMSO) followed by dilution in the assay buffer not exceeding a final DMSO-concentration of 1% (v/v). The substance concentrations for screening were basically selected from the maximal concentrations in previous studies ( Meyerhof et al 2010 ; Lossow et al 2016 ; Itoigawa et al 2021 ). The calcium responses were expressed as the normalized peak response ( F ) relative to background fluorescence ( F 0 ): Δ F / F ( = [ F − F 0 ]/ F 0 ).…”

Section: Methodsmentioning

confidence: 99%

“…Humans ( Homo sapiens ) and mice ( Mus musculus ) potentially have ∼26 and ∼40 intact TAS2R genes ( Go et al 2005 ; Hayakawa et al 2014 ), whereas platypus and short-beaked echidna have only 7 and 3, respectively ( Zhou et al 2021 ). TAS2R gene repertoire and each receptor function are believed to be related to animals’ feeding habits and foraging behavior ( Hayakawa et al 2014 ; Li and Zhang 2014 ; Liu et al 2016 ; Purba et al 2020 ; Itoigawa et al 2021 ). However, studies focusing on marsupials and monotremes are limited ( Johnson et al 2018 ; Zhou et al 2021 ); therefore, exploring monotreme TAS2R functions will provide insight into not only their molecular adaptation in each monotreme species but may also inform diversification of bitter taste receptors in early mammalian evolution.…”

Section: Introductionmentioning

confidence: 99%

“…β-glucosides include cyanogenic glucosides (CNglcs), highly deleterious and widely distributed biomolecules for feeding deterrents ( Beran et al 2019 ). While TAS2R16 of primates, rodents, and bats have sensitivity to β-glucosides ( Bufe et al 2002 ; Imai et al 2012 ; Jiao et al 2018 , 2021 ; Itoigawa et al 2019 ; Yang et al 2021 ), some primates which regularly feed on plants containing much CNglcs have TAS2R16 low sensitive to β-glucosides ( Itoigawa et al 2021 ). Therefore, β-glucoside detection would be important for survival in various mammals.…”

Section: Introductionmentioning

confidence: 99%

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Functional Diversity and Evolution of Bitter Taste Receptors in Egg-Laying Mammals

Itoigawa

Hayakawa

Zhou

et al. 2022

Molecular Biology and Evolution

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Egg-laying mammals (monotremes) are a sister clade of therians (placental mammals and marsupials) and a key clade to understand mammalian evolution. They are classified into platypus and echidna, which exhibit distinct ecological features such as habitats and diet. Chemosensory genes, which encode sensory receptors for taste and smell, are believed to adapt to the individual habitats and diet of each mammal. In this study, we focused on the molecular evolution of bitter taste receptors (TAS2Rs) in monotremes. The sense of bitter taste is important to detect potentially harmful substances. We comprehensively surveyed agonists of all TAS2Rs in platypus (Ornithorhynchus anatinus) and short-beaked echidna (Tachyglossus aculeatus) and compared their functions with orthologous TAS2Rs of marsupial and placental mammals (i.e., therians). As results, the agonist screening revealed that the deorphanized monotreme receptors were functionally diversified. Platypus TAS2Rs had broader receptive ranges of agonists than those of echidna TAS2Rs. While platypus consumes a variety of aquatic invertebrates, echidna mainly consumes subterranean social insects (ants and termites) as well as other invertebrates. This result indicates that receptive ranges of TAS2Rs could be associated with feeding habits in monotremes. Furthermore, some orthologous receptors in monotremes and therians responded to β-glucosides, which are feeding deterrents in plants and insects. These results suggest that the ability to detect β-glucosides and other substances might be shared and ancestral among mammals.

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Dietary flexibility of the greater bamboo lemur (Prolemur simus), a specialized feeder, in eastern Madagascar

Mihaminekena,

Rakotonanahary,

Frasier

et al. 2024

American J Primatol

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The degree of dietary flexibility in primates is species specific; some incorporate a wider array of resources than others. Extreme interannual weather variability in Madagascar results in seasonal resource scarcity which has been linked to specialized behaviors in lemurs. Prolemur simus, for example, has been considered an obligate specialist on large culm bamboo with >60% of its diet composed of woody bamboos requiring morphological and physiological adaptations to process. Recent studies reported an ever‐expanding list of dietary items, suggesting that this species may not be an obligate specialist. However, long‐term quantitative feeding data are unavailable across this species’ range. To explore the dietary flexibility of P. simus, we collected data at two northern sites, Ambalafary and Sahavola, and one southern site, Vatovavy, from September 2010 to January 2016 and May 2017 to September 2018, respectively. In total, we recorded 4022 h of behavioral data using instantaneous sampling of adult males and females from one group in Ambalafary, and two groups each in Sahavola and Vatovavy. We recorded 45 plant species eaten by P. simus over 7 years. We also observed significant differences in seasonal dietary composition between study sites. In Ambalafary, bamboo was the most frequently observed resource consumed (92.2%); however, non‐bamboo resources comprised nearly one‐third of the diet of P. simus in Sahavola and over 60% in Vatovavy. Consumption of all bamboo resources increased during the dry season at Ambalafary and during the wet season at Vatovavy, but never exceeded non‐bamboo feeding at the latter. Culm pith feeding was only observed at Ambalafary, where it was more common during the dry season. We identify P. simus as a bamboo facultative specialist capable of adjusting its feeding behavior to its environment, indicating greater dietary flexibility than previously documented, which may enable the species to survive in increasingly degraded habitats.

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Lowered sensitivity of bitter taste receptors to β-glucosides in bamboo lemurs: an instance of parallel and adaptive functional decline in TAS2R16?

Cited by 10 publications

References 52 publications

The sensory ecology of primate food perception, revisited

The sensory ecology of primate food perception, revisited

Functional Diversity and Evolution of Bitter Taste Receptors in Egg-Laying Mammals

Dietary flexibility of the greater bamboo lemur (Prolemur simus), a specialized feeder, in eastern Madagascar

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