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

Abstract

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.

The avian taste system

“…The sensitivity of T1R1-T1R3 to amino acids and sugars changes across different bird species. Alanine, lysine, arginine, asparagine, valine, serine, and glycine trigger the T1R1-T1R3 heterodimer more than other amino acids (Cockburn et al, 2022).…”

“…Rajapaksha et al (2016) reported 767 taste buds in chicken, 66% of which on the palate and the rest on the base of the oral cavity. In the past few years, fascinating aspects of the avian taste system have been discovered which highlight the evolutionary relevance of the avian taste system to adapt to dietary requirements in several bird species (Baldwin et al, 2014;Toda et al, 2021;Cockburn et al, 2022). Looking to the future, the recent release of the whole genome sequence of 363 bird species in 2020 and the initiative to sequence the genome of all the 10,000 bird species (B10K project: https://b10k.genomics.cn) will provide the opportunity to further understand the role of taste system in avian biology and evolution (Feng et al, 2020).…”

“…The T1R1-T1R3 heterodimer has been found in all birds studied to date across all feeding styles including carnivores (e.g., falcon), piscivores (e.g., sea birds), micro-faunivores (e.g., some ducks), insectivores (e.g., swift, flycatcher), omnivores (e.g., quail), herbivores (e.g., some ducks), and granivores (e.g., chicken, finches, pigeons) (Shi and Zhang, 2006;Roura et al, 2008;Zhao et al, 2011). However, in addition to amino acids, the T1R1-T1R3 sensor in songbirds has mutated to sense simple sugars consistent with a feeding strategy specialized in sugar-rich food resources (Baldwin et al, 2014;Toda et al, 2021;Cockburn et al, 2022). The latter has been further elaborated in Section 4.2.…”

Bitter taste receptors of the zebra finch (Taeniopygia guttata)

“…Although in general five basic taste modalities act in concert to assess the nutritional quality of food, a considerable number of animals have lost some taste modalities ( Antinucci and Risso, 2017 ). A well known example is the pseudogenization of the sweet taste receptor in all bird species, although several bird clades with a high demand for sweet tasting nutritional resources such as nectar, achieved the subsequent modification of the umami taste receptor for sweet compound detection ( Baldwin et al, 2014 ; Toda et al, 2021 ; Cockburn et al, 2022 ). In the past, it was believed that birds possess an inferior sense of taste, an assumption that was supported by the loss of the sweet tasting ability as well as a small number of bitter taste receptors ( Niknafs and Roura, 2018 ).…”