Role of feeding specialization in taste receptor loss: insights from sweet and umami receptor evolution in Carnivora.

Abstract

Controversy and misunderstanding surround the role of feeding specialization in taste receptor loss in vertebrates. We refined and tested the hypothesis that this loss is caused by feeding specializations. Specifically, feeding specializations were proposed to trigger time-dependent process of taste receptor loss through deprivation of benefit of using the receptor's gustatory function. We propose that this process may be accelerated by abiotic environmental conditions or decelerated/stopped because of extragustatory functions of the receptor's protein(s). As test case we used evolution of the sweet (TAS1R2+TAS1R3) and umami (TAS1R1+TAS1R3) receptors in Carnivora (dogs, cats, and kin). We predicted these receptors' absence/presence using data on presence/absence of inactivating mutations in these receptors' genes and data from behavioral sweet/umami preference tests. We identified 20 evolutionary events of sweet (11) or umami (9) receptor loss. These events affected species with feeding specializations predicted to favor sweet/umami receptor loss (27 and 22 species, respectively). All species with feeding habits predicted to favor sweet/umami receptor retention (11 and 24, respectively) were found to retain that receptor. Six species retained the sweet (5) or umami (1) receptor despite feeding specialization predicted to favor loss of that receptor, which can be explained by the time dependence of sweet/umami receptor loss process and the possible decelerating effect of TAS1R extragustatory functions so that the sweet/umami receptor process is ongoing in these species. Our findings support the idea that feeding specialization leads to taste receptor loss and is the main if not only triggering factor for evolutionary loss of taste receptors.