Abstract
Temperature is one of the most critical environmental factors affecting survival, and thus species that inhabit different thermal niches have evolved thermal sensitivities suitable for their respective habitats. During the process of shifting thermal niches, various types of genes expressed in diverse tissues, including those of the peripheral to central nervous systems, are potentially involved in the evolutionary changes in thermosensation. To elucidate the molecular mechanisms behind the evolution of thermosensation, thermal responses were compared between two species of clawed frogs (Xenopus laevis and Xenopus tropicalis) adapted to different thermal environments. X. laevis was much more sensitive to heat stimulation than X. tropicalis at the behavioral and neural levels. The activity and sensitivity of the heat-sensing TRPA1 channel were higher in X. laevis compared with those of X. tropicalis The thermal responses of another heat-sensing channel, TRPV1, also differed between the two Xenopus species. The species differences in Xenopus TRPV1 heat responses were largely determined by three amino acid substitutions located in the first three ankyrin repeat domains, known to be involved in the regulation of rat TRPV1 activity. In addition, Xenopus TRPV1 exhibited drastic species differences in sensitivity to capsaicin, contained in chili peppers, between the two Xenopus species. Another single amino acid substitution within Xenopus TRPV1 is responsible for this species difference, which likely alters the neural and behavioral responses to capsaicin. These combined subtle amino acid substitutions in peripheral thermal sensors potentially serve as a driving force for the evolution of thermal and chemical sensation.
Highlights
Animals have evolved sophisticated physiological systems for sensing ambient temperatures, as fluctuations in environmental temperature significantly affect various biological processes
Behavioral and Sensory Neural Responses to Heat Stimulation Differ between the Two Xenopus Species—To compare the thermal responses between X. tropicalis and X. laevis, heat stimulation was systemically applied to frogs, and nocifensive behaviors were observed
We reported previously that TRPV1 and TRPA1 from X. tropicalis are activated by heat stimulation and are highly co-expressed in most of the heat-sensitive dorsal root ganglion (DRG) neurons (ϳ85%) [11]
Summary
Comparative analyses among closely related species with similar ecological and physiological traits, but that inhabit different thermal environments, are required for investigating the evolutionary processes of thermal adaptation. X. laevis inhabits cooler regions compared with X. tropicalis, found in Africa, and these two Xenopus species have adapted to different thermal niches [17]. There were no detectable differences in the thermal responses of TRPM8 between the two Xenopus species [8]. We attempted to compare the thermal responses between X. laevis and X. tropicalis at the behavioral, sensory neuron, and temperature receptor levels. Thermal responses of both TRPA1 and TRPV1 differed between the two Xenopus species. We found that three amino acid substitutions are largely responsible for the species differences in TRPV1 heat responses. We were able to show that the sensitivity of TRPV1 to capsaicin differs between the two Xenopus species, and this is dictated by another single amino acid substitution. Subtle amino acid changes in thermoTRP channels altered their functional properties, and this may have contributed to the evolutionary shift in thermal and chemical sensation
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