Unexpected loss of TAS1R1-TAS1R3 umami taste receptor function in carnivorous Lyncodontini mustelids

Lyncodon patagonicus (Patagonian weasel), Galictis cuja (lesser grison), and Galictis vittata (greater grison) are the only extant species of Lyncodontini, a relatively poorly known Neotropical tribe of the mustelid subfamily Ictonychinae within the mammalian order Carnivora. Here, we report molecular evidence indicating that the TAS1R1-TAS1R3 umami (savory) taste receptor lost its function in the Lyncodontini's stem lineage (∼3 to 9.5 million years ago) and is therefore nonfunctional in all crown Lyncodontini. This finding is unexpected and intriguing because all extant Lyncodontini apparently need this receptor (they are terrestrial carnivores with diets high in umami-eliciting compounds, including purine 5'-monophosphate ribonucleotides, the main agonists of TAS1R1-TAS1R3 in carnivorans). We argue that the common ancestor of extant Lyncodontini that first lost TAS1R1-TAS1R3 function was semiaquatic and predated mainly on fish and/or aquatic invertebrates (tissues of living or recently dead fish and aquatic invertebrates are low in purine 5'-monophosphate ribonucleotides). This hypothesis is consistent with the idea that loss of taste receptor function is caused by feeding specializations that restrict access to the compounds that a particular receptor detects. Our hypothesis effectively suggests a prolonged semiaquatic episode in the evolutionary history of the Lyncodontini's stem lineage because loss of TAS1R1-TAS1R3 function is achieved by a stochastic process continuing over evolutionary time. Whether the extant Lyncodontini evolved a mechanism to compensate for the loss of TAS1R1-TAS1R3 function is currently unknown and requires further research.