Early origin of sweet perception in the songbird radiation

Toda, Yasuka; Ko, Meng-Ching; Liang, Qiaoyi; Miller, Eliot T.; Rico‐Guevara, Alejandro; Nakagita, Tomoya; Sakakibara, Ayano; Uemura, Kana; Sackton, Timothy B.; Hayakawa, Takashi; Sin, Simon Yung Wa; Ishimaru, Yoshiro; Misaka, Takumi; Oteíza, Pablo; Crall, James D.; Edwards, Scott V.; Buttemer, William A.; Matsumura, Shuichi; Baldwin, Maude W.

doi:10.1126/science.abf6505

Cited by 37 publications

(27 citation statements)

References 64 publications

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“…This combination of critical domains represents an interesting example of convergence with the independent acquisition of sweet taste seen in the songbird radiation: in addition to the modifications we have described to distinct ligand-binding domains (T1R3 in hummingbirds and T1R1 in songbirds), we now show that the CRD-TMD region of the opposite paralog (T1R1 in hummingbirds; fig. 2 c–d , T1R3 in songbirds; Toda et al 2021b ) also plays a critical role in both radiations. Each acquisition of carbohydrate and sweetener detection therefore requires modifying a combination of both domains, but hummingbirds and songbirds recruit alternate paralogs in a mirror-image fashion ( fig.…”

Section: Resultsmentioning

confidence: 99%

“…The savory, or umami, receptor of vertebrates is a heterodimer composed of two G-protein coupled receptors, T1R1 and T1R3. In hummingbirds and in songbirds, the T1R1–T1R3 receptor, ancestrally responsive likely only to amino acids ( Nelson et al 2002 ; Baldwin et al 2014 ), has convergently undergone a functional shift, enabling these species to detect sugars ( Baldwin et al 2014 ; Toda et al 2021b ). A common way that novel functions emerge is through gene duplication and neofunctionalization of one duplicate, which can permit the ancestral function to be retained ( Innan and Kondrashov 2010 ); in avian sugar sensing, however, a single receptor may be responsible for detecting both sugars and amino acids, potentially requiring a trade-off.…”

Section: Introductionmentioning

confidence: 99%

“…A common way that novel functions emerge is through gene duplication and neofunctionalization of one duplicate, which can permit the ancestral function to be retained ( Innan and Kondrashov 2010 ); in avian sugar sensing, however, a single receptor may be responsible for detecting both sugars and amino acids, potentially requiring a trade-off. In songbirds, amino acid responses are robust in some species but reduced in others ( Toda et al 2021b ). Since receptors of only a single hummingbird have previously been tested, diversity within hummingbirds is unexplored, and whether hummingbirds can respond to and prefer amino acids is not known.…”

Section: Introductionmentioning

confidence: 99%

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Synergism, Bifunctionality, and the Evolution of a Gradual Sensory Trade-off in Hummingbird Taste Receptors

Cockburn

Sadanandan

et al. 2022

Molecular Biology and Evolution

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Sensory receptor evolution can imply trade-offs between ligands, but the extent to which such trade-offs occur and the underlying processes shaping their evolution is not well understood. For example, hummingbirds have re-purposed their ancestral savory receptor (T1R1-T1R3) to detect sugars, but the impact of this sensory shift on amino acid perception is unclear. Here, we use functional and behavioral approaches to show that the hummingbird T1R1-T1R3 acts as a bifunctional receptor responsive to both sugars and amino acids. Our comparative analyses reveal substantial functional diversity across the hummingbird radiation and suggest an evolutionary timeline for T1R1-T1R3 re-tuning. Finally, we identify a novel form of synergism between sugars and amino acids in vertebrate taste receptors. This work uncovers an unexplored axis of sensory diversity, suggesting new ways in which nectar chemistry and pollinator preferences can coevolve.

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Section: Resultsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Synergism, Bifunctionality, and the Evolution of a Gradual Sensory Trade-off in Hummingbird Taste Receptors

Cockburn

Sadanandan

et al. 2022

Molecular Biology and Evolution

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“…More broadly, sequencing and assembling a genome from a nectivorous tanager adds to the collection of obligate nectivores sequenced among the vertebrate Tree of Life ( Feng et al 2020 ; Supplementary Table S2), providing another avenue of research into the genetic basis of adaptations common to a nectivorous lifestyle, including: sweet taste perception ( e.g. , Baldwin et al 2014; Toda et al 2021 ), sugar metabolism ( e.g. , Schondube and Del Rio 2004; Workman et al 2018), spatial memory of floral resources ( e.g.…”

Section: Resultsmentioning

confidence: 99%

A reference genome for the nectar-robbing Black-throated Flowerpiercer (Diglossa brunneiventris)

Hiller

Brumfield

Faircloth

2021

G3 Genes|Genomes|Genetics

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Black-throated Flowerpiercers (Diglossa brunneiventris) are one species representing a phenotypically specialized group of tanagers (Thraupidae) that have hooked bills which allow them to feed by stealing nectar from the base of flowers. Members of the genus are widely distributed in montane regions from Mexico to northern Argentina, and previous studies of Diglossa have focused on their systematics, phylogenetics, and interesting natural history. Despite numerous studies of species within the genus, no genome assembly exists to represent these nectivorous tanagers. We described the assembly of a genome sequence representing a museum-vouchered, wild, female Diglossa brunneiventris collected in Peru. By combining Pacific Biosciences Sequel long-read technology with 10X linked-read and reference-based scaffolding, we produced a 1.08 Gbp pseudochromosomal assembly including 600 scaffolds with a scaffold N50 of 67.3 Mbp, a scaffold L50 of 6, and a BUSCO completeness score of 95%. This new assembly improves representation of the diverse species that comprise the tanagers, improves on scaffold lengths and contiguity when compared to existing genomic resources for tanagers, and provides another avenue of research into the genetic basis of adaptations common to a nectivorous lifestyle among vertebrates.

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“…These molecular interaction sites or regulatory sites at protein surfaces can be hotspots of protein adaptation. Indeed, some specific molecular interactions have been linked to adaptive evolution in several case studies ( Hughes and Nei 1988 ; Bachtrog 2008 ; Schott et al 2014 ; Levin and Malik 2017 ), a recent study on sweet taste receptors in the songbird radiation ( Toda et al 2021 ), and large-scale studies based on proteins with high-quality structural models ( Slodkowicz and Goldman 2020 ). In the latter study, the authors showed that amino acids under positive selection in mammals tend to cluster closer to binding sites of exogenous ligands than expected by chance ( Slodkowicz and Goldman 2020 ), suggesting an important role of functionally important regions in adaptive evolution.…”

Section: Discussionmentioning

confidence: 99%

Intermolecular Interactions Drive Protein Adaptive and Coadaptive Evolution at Both Species and Population Levels

Peng

Svetec

Zhao

2021

Molecular Biology and Evolution

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Proteins are the building blocks for almost all the functions in cells. Understanding the molecular evolution of proteins and the forces that shape protein evolution is essential in understanding the basis of function and evolution. Previous studies have shown that adaptation frequently occurs at the protein surface, such as in genes involved in host-pathogen interactions. However, it remains unclear whether adaptive sites are distributed randomly or at regions associated with particular structural or functional characteristics across the genome, since many proteins lack structural or functional annotations. Here, we seek to tackle this question by combining large-scale bioinformatic prediction, structural analysis, phylogenetic inference, and population genomic analysis of Drosophila protein-coding genes. We found that protein sequence adaptation is more relevant to function-related rather than structure-related properties. Interestingly, intermolecular interactions contribute significantly to protein adaptation. We further showed that intermolecular interactions, such as physical interactions, may play a role in the co-adaptation of fast-adaptive proteins. We found that strongly differentiated amino acids across geographic regions in protein-coding genes are mostly adaptive, which may contribute to the long-term adaptive evolution. This strongly indicates that a number of adaptive sites tend to be repeatedly mutated and selected in evolution, in the past, present, and maybe future. Our results highlight the important roles of intermolecular interactions and co-adaptation in the adaptive evolution of proteins both at the species and population levels.

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Early origin of sweet perception in the songbird radiation

Cited by 37 publications

References 64 publications

Synergism, Bifunctionality, and the Evolution of a Gradual Sensory Trade-off in Hummingbird Taste Receptors

Synergism, Bifunctionality, and the Evolution of a Gradual Sensory Trade-off in Hummingbird Taste Receptors

A reference genome for the nectar-robbing Black-throated Flowerpiercer (Diglossa brunneiventris)

Intermolecular Interactions Drive Protein Adaptive and Coadaptive Evolution at Both Species and Population Levels

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