Chemical discrimination by tongue-flicking in lizards: A review with hypotheses on its origin and its ecological and phylogenetic relationships

Tongue-flicking is a synapomorphy of squamate reptiles functioning to sample chemicals for vomerolfactory analysis, which became possible in primitive squamates when ducts opened from the vomeronasal organs to the roof of the mouth. Extant iguanian lizards in families that do not use the tongue to sample chemical prey cues prior to attack partially protrude it in two feeding contexts: during capture by lingual prehension and after oral contact with prey. These lizards do not exhibit strike-induced chemosensory searching. Lingual prey prehension is present in iguanian lizards and inSphenodon, the sister taxon of Squamata. During attempts to capture prey, the tongues of primitive squamates inevitably made incidental contact with environmental substrates bearing chemicals deposited by prey, conspecifics, and predators. Such contact presumably induced selection for tongue-flicking and ability to identify biologically important chemicals. Most iguanian lizards are ambush foragers that use immobility as a major antipredatory defense. Because tongue-flicking at an ambush post would not allow chemical search beyond the vicinity of the head and would render them easier for predators and prey to detect, typical iguanians tongue-flick neither while foraging nor to identify predators. They do detect pheromones by tongue-flicking. Scleroglossan lizards are typically active foragers that rely on speed to escape. Being freer to move the tongue, they have evolved lingual sampling allowing detection of chemical cues of conspecifics, predators, and prey, as well as strike-induced chemosensory searching, some can follow pheromone trails by tongue-flicking. Some families have lingual morphology and behavior specialized for chemosensory sampling. In varanids and snakes, the taxa showing the greatest lingual specialization, additional prey-related chemosensory behaviors have evolved. In iguanian and scleroglossan families that have secondarily adopted the foraging mode typical of the other taxon, prey chemical discrimination involving tongue-flicking and strike-induced chemosensory searching are typical for the foraging mode rather than the taxon. Because foraging mode and state of prey chemical discrimination are stable within squamate families and to a large extent in higher taxa, both features have been retained from the ancestral condition in most families. However, in three cases in which foraging mode has changed from its ancestral state, the state of prey chemical discrimination has also changed, indicating that prey chemical discrimination is adaptively adjusted to foraging mode. Indeed, acquisition of lingually mediated prey chemical discrimination may have made feasible the evolution of active foraging, which in turn appears to have profoundly influenced the further evolution of squamate chemosensory structures and behavior, placing a selective premium on features enhancing the tongue's efficiency as a chemical sampling device. The advent of tongue-flicking to sample prey chemicals and thus detect hidden prey may have allowed generalist (cruise) or ambush foragers, if early squamates were such, to become specialists in active foraging. Alternatively, if the common ancestors of squamates were active foragers, the adoption of ambush foraging would have selected against participation of the tongue in locating prey. Acting jointly, tongue-flicking and active foraging have had momentous consequences for squamate diversification. Specialization for active foraging would appear to have had ramifying effects on antipredatory defenses, body form, territoriality, mating systems, and reproductive physiology.