Sensory biology. Evolution of sweet taste perception in hummingbirds by transformation of the ancestral umami receptor

Abstract

Sensory systems define an animal's capacity for perception and can evolve to promote survival in new environmental niches. We have uncovered a noncanonical mechanism for sweet taste perception that evolved in hummingbirds since their divergence from insectivorous swifts, their closest relatives. We observed the widespread absence in birds of an essential subunit (T1R2) of the only known vertebrate sweet receptor, raising questions about how specialized nectar feeders such as hummingbirds sense sugars. Receptor expression studies revealed that the ancestral umami receptor (the T1R1-T1R3 heterodimer) was repurposed in hummingbirds to function as a carbohydrate receptor. Furthermore, the molecular recognition properties of T1R1-T1R3 guided taste behavior in captive and wild hummingbirds. We propose that changing taste receptor function enabled hummingbirds to perceive and use nectar, facilitating the massive radiation of hummingbird species.

Fig. 1. Analysis of T1R sequences in birds

(A) A maximum-likelihood tree was constructed using T1R sequences from 13 birds and the Chinese alligator (∇ = nodal bootstrap <80%; scale bar, 0.4 substitutions per site). (B) Amino acid sequences of T1R3 cloned from birds. Gray, transmembrane domains; red, putatively selected sites (table S3).

Fig. 2. Evolution of a sugar receptor in hummingbirds

(A) Functional expression of avian and rodent taste receptors to stimuli [100 mM, except aspartame (15 mM); n = 6 independent experiments, mean ± SE, *P ≤ 0.05]. (B) Sugar responses of hummingbird T1Rs alone or in combination (n = 6 independent experiments, mean ± SE, *P ≤ 0.05). (C) Dose-dependent responses of T1R1-T1R3 from species indicated to amino acids (blue) and sugars (red).

Fig. 3. Molecular basis for the acquisition of sugar binding in hummingbird T1R1-T1R3

(A) T1R3 chimeras containing chicken (black) and hummingbird (red) amino acids were designed (CRD, cysteine-rich domain; TM, transmembrane domains). (B) Responses of T1R3 chimeras and hummingbird T1R1 to l-alanine, sucralose, and sucrose (100 mM). (C) Dose-dependent responses of T1R3 chimeras and hummingbird T1R1 to sucrose. (D) A homology model of the venus flytrap domain of T1R3 shows the putative ligand binding site (yellow), predicted by alignment with ligand-contacting sites of rat mGluR1 (20), and mutations that confer sugar binding, which cluster in three distinct locations (red, green, and blue).

Fig. 4. T1R1-T1R3 agonists evoke taste responses in captive and wild hummingbirds

(A) Captive ruby-throated hummingbirds (n = 3 or 4, mean ± SE) were presented with solutions of test stimuli and sucrose (333 mM), and the drinking bout lengths, time spent drinking, and number of long bouts (>1 s) were recorded (linear mixed-effect models for differences between stimuli and sucrose, ***P ≤ 0.001). Red bars indicate palatability similar to that of carbohydrates. (B) The taste preferences of wild Anna's hummingbirds were measured (mean bout lengths ± SE, sample sizes: table S4, Kolmogorov-Smirnov tests for differences between stimuli and sucrose: *P ≤ 0.05, **P ≤ 0.01, ***P ≤ 0.001). Concentrations: white, 500 mM; gray, 1 M; black, indicated. Red bars indicate equal preference. [Photo credits: (A) M.W.B. and F. Peaudecerf, (B) M.W.B.]