Ganglion-specific splicing of TRPV1 underlies infrared sensation in vampire bats

Abstract

Vampire bats (Desmodus rotundus) are obligate blood feeders that have evolved specialized systems to suit their unique sanguinary lifestyle 1–3. Chief among such adaptations is the ability to detect infrared radiation as a means of locating hot spots on warm-blooded prey. Among vertebrates, only vampire bats, boas, pythons, and pit vipers are capable of detecting infrared radiation 1,4. In each case, infrared heat is detected by trigeminal nerve fibers that innervate specialized pit organs on the animal’s face 5–10. Thus, vampire bats and snakes have taken thermosensation to the extreme by developing specialized systems for detecting infrared radiation. As such, these creatures provide a window into the molecular and genetic mechanisms underlying evolutionary tuning of thermoreceptors in a species or cell type specific manner. Previously, we have shown that snakes co-opt a non-heat sensitive channel (vertebrate TRPA1) to produce an infrared detector 6. Here we show that vampire bats tune an already heat sensitive channel (TRPV1) by lowering its thermal activation threshold to ~30°C. This is achieved through alternative splicing of TRPV1 transcripts to produce a channel with a truncated C-terminal cytoplasmic domain. Remarkably, these splicing events occur exclusively in trigeminal ganglia (TG), and not dorsal root ganglia (DRG), thereby maintaining a role for TRPV1 as a detector of noxious heat in somatic afferents. This reflects a unique organization of the bat TRPV1 gene that we show to be characteristic of Laurasiatheria mammals (cows, dogs, and moles), supporting a close phylogenetic relationship with bats. These findings reveal a unique molecular mechanism for physiological tuning of thermosensory nerve fibers.