Mammals have three members of the small taste receptor gene family responsible for the perception of sweet and savory tastes: two genes (T1R2 and T1R3) comprise the canonical sweet receptor, and a third gene, T1R1, acts with T1R3 to make the savory receptor. Here, in a joint effort with a team of international collaborators, we show that even though birds are missing the taste receptor gene (T1R2) required by other vertebrates to perceive carbohydrates and sweeteners, hummingbirds still detect sugars—but in a novel way. This project spanned multiple fields and field sites, integrating taste tests on wild birds, behavioral analysis of captive animals, bioinformatics, receptor cloning, and cell-based functional assays.
The first published avian genome, that of the chicken, revealed a surprising lack of T1R2. Chickens are sweet-insensitive: however, many nectar-feeding birds appear highly attuned to sugars like sucrose, fructose and glucose. Our initial field experiments with a panel of artificial sweeteners as well as high-speed filming and choice tests on captive birds indicated a rapid response to sugars rather than a post-ingestive metabolic sensing of caloric value. As the response appeared sensory, we pursued a candidate gene approach to search for possible taste receptors, and cloned T1R taste receptors from chickens, hummingbirds, and swifts. By analyzing genomes from an additional 10 birds and an alligator, we documented widespread absence of T1R2 and identified signatures of positive selection in the remaining hummingbird T1Rs.
Together with Dr. Yasuka Toda at the University of Tokyo, we were able to test the function of these receptors in cell culture. We used a cell-based luminescence assay to measure functional responses. As expected, chicken and swift receptors responded to amino acids, but, surprisingly, the umami receptor in hummingbirds had acquired a new function and was now sensitive to carbohydrates as well. Chimeric studies of receptors containing hummingbird and chicken sequence identified 19 mutations involved in this functional change: since divergence from swifts, the umami receptor underwent extensive re-modeling. Further behavioral tests with wild hummingbirds revealed that most agonists from the cell-based assay were appetitive, while artificial sweeteners which did not activate the receptors were not preferred—a concordance between in vivo and in vitro studies that indicates that this re-purposed receptor guides hummingbird taste behavior.
Diet shifts have profound physiological effects and evolutionary ramifications: the radiation of hummingbirds is likely due, at least in part, to their ability to colonize an empty niche. However, much remains to be learned about the roles of taste in changes in diet, and the causes and effects of shifts in diet and perception are often unclear. For instance, birds appear to have lost T1R2 early in their evolutionary history. As they are the descendants of carnivorous dinosaurs, birds may have experienced relaxed selection on the sweet receptor similar to that seen in mammalian carnivores; alternatively, the loss could be due to the overall genome-wide reduction seen in birds. In Chapter 3, we begin to investigate causes and consequences of the changes in hummingbird taste receptors, and present new behavioral studies regarding the ability to detect amino acids. Together, these findings raise questions about the evolution of sensory systems and of neural circuits underlying perception: studying taste receptors in a comparative context yields insight into basic aspects of the evolutionary process as well as molecular mechanisms underlying behavior. / Biology, Organismic and Evolutionary
| Identifer | oai:union.ndltd.org:harvard.edu/oai:dash.harvard.edu:1/17467228 |
| Date | 01 May 2017 |
| Creators | Baldwin, Maude Wheeler |
| Contributors | Edwards, Scott V. |
| Publisher | Harvard University |
| Source Sets | Harvard University |
| Language | English |
| Detected Language | English |
| Type | Thesis or Dissertation, text |
| Format | application/pdf |
| Rights | embargoed |
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