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.

Synchronized Expansion and Contraction of Olfactory, Vomeronasal, and Taste Receptor Gene Families in Hystricomorph Rodents

“…Therefore, it is possible that the T1R1 gene has undergone pseudogenization in the common gundi genome, although we cannot rule out the possibility of assembly errors. In this regard, it is noteworthy that certain mammals, such as carnivores, cetaceans, and bats, have lost one or more T1R genes in response to changes in diet, feeding habitats, or environmental conditions ( Jiang et al 2012 ; Zhao et al 2012 ; Antinucci and Risso 2017 ; Wolsan and Sato 2022 ).…”

Insights to Study, Understand and Manage Extruded Dry Pet Food Palatability

“…These discrepancies between cats and dogs are congruent with the obligate carnivorous diet of cats, allowing for a more refined appreciation of amino acids from meat without interference from sugars [21,35]. Indeed, while dogs possess the sweet taste receptor heterodimer TAS1R2 + TAS1R3, cats do not have the capacity to encode the TAS1R2 protein, resulting in the loss of the sweet taste receptor [36,67]. There is a debated hypothesis on the absence of sweet taste receptors in some Carnivora that relates it to specific feeding specializations such as obligate carnivore.…”

“…Indeed, this feeding specialization would have no benefit from having such a taste receptor [68,69]. Recently, Wolsan and Sato [67] supported this hypothesis by predicting the presence or absence of the sweet taste receptor using data on genetics and behavioral taste preference tests. Carnivora with an obligate carnivore diet studied here, such as cats, all lost their sweet taste receptors, with few exceptions for which the loss is hypothesized to be ongoing.…”

“…Concerning palatability, olfaction is considered essential in food selection and preference for cats and dogs [7,33,36,42,56,67,75]. Regarding its physiology, the mammalian olfactory system is similar for most species, including these two companion animals.…”