A matter of Taste

hummingbirdhummingbirdhummingbird“Evolution of sweet taste perception in hummingbirds by transformation of the ancestral umami receptor” Baldwin et al Science 2014

 

Why study birds to understand sensory perception?

Birds are a group of therapod dinosaurs that evolved during the mid Mesozoic era (~150 million years ago). They represent one of the most diverse extant vertebrate clades inhabiting almost all terrestrial environments across all seven continents, the Arctic and the Antarctic.  Birds also have radiated to fill a huge array of ecological niches from large birds of prey, to the very tiny nectar feeding hummingbirds. An essential part of species radiation and successful novel niche colonization is the ability to adapt sensory systems to new environments.  So birds represent a good model for understanding variation in sensory perception.

What sense, which species and why?

With sensory systems such as olfaction and bitter taste perception we know that there is a considerable amount of gene gain and loss across lineages reflective of ecological niche. However, sweet and savory taste receptors don’t vary in number and they have highly conserved sequence.  Sweet perception is governed by the combination of 2 proteins T1R2+T1R3 and savory by T1R1+T1R3. We observe an ancestral loss of the T1R2 in the bird lineage – meaning that birds cannot perceive sweetness. How is it then that we have nectar loving hummingbirds – how can they taste sweetness without an essential part of that receptor?

What did we find ?

A new vertebrate sweet taste receptor ! We tested the response of a variety of bird savory receptors (chicken, hummingbird, swift) to different amino acids and sugars. We found that the hummingbird savory receptor responded to several different sugars (sucrose, fructose and glucose) but not to artificial sweeteners. But the chicken and swift savory receptors did not respond to sugars. And so it appeared that the savory receptor in Hummingbirds can perceive sweetness. We wanted to know what changes in the savory receptor of hummingbirds have allowed a new function to evolve. So we made up chimeric proteins that had a range of different chicken (non-sugar detecting) and hummingbird (sugar detecting) savory receptor regions combined and we tested their abilities to detect sugars. By making a series of these chimeras we could narrow down the part of the protein complex that was involved in the new sugar detecting function and we found evidence of positive selection in these regions. So we had found a new vertebrate sweet taste receptor !

Does this new sweet taste receptor dictate behavior in hummingbirds? We studied the behavior of a captive ruby-throated hummingbird model and a wild population of Anna’s hummingbirds in response to different sugar, water, artificial sweeteners and amino acids etc just as we had tested for the receptor response assays in vitro. We tested whether the hummingbirds behavior showed a preference for sugar solutions over water and aspartame solutions as our in vitro tests had shown – they made their decision on calorific value within a staggering 200 milliseconds and showed a distinct preference for sugar. We also tested a wild population of hummingbirds from the Santa Monica mountains (CA, USA) and found again a strong preference for sugar solutions. Our study shows that several simple sugars (sucrose, fructose and glucose) all effect a rapid, appetitive flavor response in hummingbirds that is facilitated by the adaptive evolution of a savory receptor into a new sweet taste receptor.



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