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bioRxiv · 10.1101/2025.03.31.646411

Evolutionary Adaptations of TRPA1 Thermosensitivity and Skin Thermoregulation in Vertebrates

Bertolesi, G. E.·Heshami, N.·McFarlane, S.
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Abstract

Altering skin color and reflectance is crucial for temperature regulation in poikilothermic vertebrates, while less so in homeotherms like birds and mammals, which evolved feathers, fur, and other insulation for endothermy. Heat-sensing in vertebrates relies primarily on Transient Receptor Potential (TRP) channels, with certain channels (TRPA1) shifting thermosensitivity over evolution and others retaining heat sensitivity (TRPV1). Exploration of a role for TRP channels in skin physiology has largely focused on human pigmentation and overlooked the evolution of different thermoregulatory structures in the integument of distinct vertebrates. For instance, colour/reflector pigment cells in ectotherms, fur and feathers in endotherms, hairless skin in hominids, and blubber in marine mammals. Therefore, we investigated whether a TRP channel mediates skin darkening induced by heat in the ectotherm Xenopus laevis and then explored the evolution of TRPA1 thermal sensitivity and its link with skin physiology. We find Trpa1 mediates heat-induced melanosome dispersion, darkening skin under warmer conditions. In contrast, TRPA1 is known to mediate cold sensation in rodents and UV-induced tanning in humans, leading us to investigate the co-evolution of TRPA1 and skin thermoregulation. Our findings reveal TRPA1 is a heat sensor in ectotherms with uncovered integuments. In mammals, we suggest TRPA1 was thermally insensitive in Euarchontoglires but became cold-sensitive in several rodent lineages. TRPA1 shows reduced selection pressure for thermosensitivity in aquatic mammals (manatees, whales) that depend on blubber for insulation as compared to their terrestrial relatives. These findings emphasize adaptive evolution of TRPA1 in vertebrates, linking thermal sensitivity to the evolution of skin physiology.

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Bertolesi, G. E., Heshami, N., McFarlane, S.. 2025-04-04. Evolutionary Adaptations of TRPA1 Thermosensitivity and Skin Thermoregulation in Vertebrates. https://doi.org/10.1101/2025.03.31.646411

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