Evolutionary Tuning of Transient Receptor Potential Ankyrin 1 Underlies the Variation in Heat Avoidance Behaviors among Frog Species Inhabiting Diverse Thermal Niches

Abstract

Environmental temperature is a critical factor for all forms of life, and thermal tolerance defines the habitats utilized by a species. Moreover, the evolutionary tuning of thermal perception can also play a key role in habitat selection. Yet, the relative importance of thermal tolerance and perception in environmental adaptation remains poorly understood. Thermal conditions experienced by anuran tadpoles differ among species due to the variation in breeding seasons and water environments selected by parental frogs. In the present study, heat tolerance and avoidance temperatures were compared in tadpoles from five anuran species that spatially and temporally inhabit different thermal niches. These two parameters were positively correlated with each other and were consistent with the thermal conditions of habitats. The species difference in avoidance temperature was 2.6 times larger than that in heat tolerance, suggesting the importance of heat avoidance responses in habitat selection. In addition, the avoidance temperature increased after warm acclimation, especially in the species frequently exposed to heat in their habitats. Characterization of the heat-sensing TRPA1 ion channel revealed an amphibian-specific alternatively spliced variant containing a single valine insertion relative to the canonical alternative spliced variant of TRPA1, and this novel variant altered the response to thermal stimuli. The two alternatively spliced variants of TRPA1 exhibited different thermal responses in a species-specific manner, which are likely to be associated with a difference in avoidance temperatures among species. Together, our findings suggest that the functional change in TRPA1 plays a crucial role in thermal adaptation processes.

Understanding the role of environmental temperature on sex determination through comparative studies in reptiles and amphibians

“…Among thermosensitive TRP channels, TRPA1 and TRPV1 have been an active area of research at elucidating the physiology and evolution of thermal sensitivity in non-model and wild organisms (Oda et al, 2019;Ohkita et al, 2012;Saito et al, 2012Saito et al, , 2016Saito et al, , 2019Saito et al, , 2022. Both TRPA1 and TRPV1 have been reported as heat-sensitive channels in most species studied investigated, with the exception of TRPA1 in mammals and Caenorhabditis elegans (Chatzigeorgiou et al, 2010;Saito et al, 2014).…”

“…In amphibians, where sex determination occurs during or after the larval stage, thermal perception through TRP channels may indirectly influence their own sex by inducing thermoregulatory behaviors. Behavioral assays have shown that a TRPA1 agonist sensitizes heat avoidance behavior in the Japanese stream tree frog ( Buergeria japonica ) and Buerger's frog ( B. buergeri ), implying that TRPA1 also functions as a nociceptive heat sensor in these amphibians (Saito et al, 2022). The relationship between thermal effects on sex determination and thermoregulatory behaviors remains essential and warrants further investigation to comprehend the significance of temperature perception in amphibian sex determination.…”