Positive selection acted on the extracellular transmembrane linkers of heat receptors during evolution

All organisms must maintain body temperature within a suitable range and be able to sense the environmental temperature variations. However, it remains largely unknown how thermal sensing systems have evolved in animals. The transient receptor potential cation channel (TRP) protein family acts as warm/heat or cool/cold receptors by changing the probability of channel opening in response to thermal stimulation. Here, we examined the selective pressures acting on the transmembrane region of six segments (S1~S6) of thermo-TRP family members. Our results showed that there exist positive selection sites in heat receptors, but not in cold receptors. When all sequences of thermal TRP channels were pooled together, more significant selection pressures were found in the linker region between the transmembrane segments at the external side of the cellular membrane. Moreover, the P-loop region between S5 and S6 contains the most selected sites, indicating their importance in the thermal sense. Our study suggests that the heat receptor is more evolutionarily diverse than the cold receptor. This is consistent with the idea that hot environments usually have high heterogeneity, and that it is of great biological importance for animals to choosewarm basking places or escape harsh environments which are hot and dangerous such as forest fires.