On the Origin and Evolution of Sweet Taste Mediated by Tas1r2-Tas1r3 in Vertebrates

Sweet taste is a crucial chemosensory modality for detecting natural sugar compounds, which are primarily derived from angiosperms. In vertebrates, excluding birds, sweet taste is typically mediated by the Tas1r2-Tas1r3 heterodimer, and the receptor function often reflects dietary adaptations to sugar-rich diets. To gain insight into early vertebrate dietary transitions, we identified Tas1r genes in 58 vertebrate species and one outgroup and conducted functional assays in 10 representative species spanning six major clades, including one coelacanth, two amphibians, one squamate, two turtles, two crocodilians, and one mammal. Cell-based assays showed that only the desert tortoise and American alligator exhibited detectable responses to natural sugars via Tas1r2-Tas1r3, while all other tested species showed no response. To trace the evolutionary origin of sweet taste perception, we reconstructed ancestral Tas1r2 and Tas1r3 receptors for tetrapods, amniotes, and sauropsids. Functional assays of these ancestral receptors revealed no sugar sensitivity. Integrating our results with previously published data, we conclude that Tas1r2-Tas1r3-mediated sweet taste likely originated in amniotes and did not exist in earlier-diverging vertebrates such as cartilaginous fishes, bony fishes, and amphibians. These findings suggest that sweet taste arose independently in vertebrate lineages after the origin of angiosperms, and likely represents lineage-specific adaptations to angiosperm-derived dietary resources.