Elucidating the functional evolution of heat sensors among Xenopus species adapted to different thermal niches by ancestral sequence reconstruction

Abstract

Ambient temperature fluctuations are detected via the thermosensory system which allows animals to seek preferable thermal conditions or escape from harmful temperatures. Evolutionary changes in thermal perception have thus potentially played crucial roles in niche selection. The genus Xenopus (clawed frog) is suitable for investigating the relationship between thermal perception and niche selection due to their diverse latitudinal and altitudinal distributions. Here we performed comparative analyses of the neuronal heat sensors TRPV1 and TRPA1 among closely related Xenopus species (X. borealis, X. muelleri, X. laevis, and X. tropicalis) to elucidate their functional evolution and to assess whether their functional differences correlate with thermal niche selection among the species. Comparison of TRPV1 among four extant Xenopus species and reconstruction of the ancestral TRPV1 revealed that TRPV1 responses to repeated heat stimulation were specifically altered in the lineage leading to X. tropicalis which inhabits warmer niches. Moreover, the thermal sensitivity of TRPA1 was lower in X. tropicalis than the other species, although the thermal sensitivity of TRPV1 and TRPA1 was not always lower in species that inhabit warmer niches than the species inhabit cooler niches. However, a clear correlation was found in species differences in TRPA1 activity. Heat‐evoked activity of TRPA1 in X. borealis and X. laevis, which are adapted to cooler niches, was significantly higher than in X. tropicalis and X. muelleri which are adapted to warmer niches. These findings suggest that the functional properties of heat sensors changed during Xenopus evolution, potentially altering the preferred temperature ranges among species.

Evolution of Transient Receptor Potential (TRP) Ion Channels in Antarctic Fishes (Cryonotothenioidea) and Identification of Putative Thermosensors

“…Physiological processes, such as sensation, are expected to evolve via structural rather than regulatory evolution ( Rosati and McKinnon 2009 ). Adapting to cold environments seems to require mutations to the primary amino acid sequence that result in changes to desensitization, activity, kinetics, and/or shifted dynamic range ( Lynch et al 2015 ; Laursen et al 2016 ; Saito et al 2016 ; Matos-Cruz et al 2017 ; Saito and Tominaga 2017 ; Luo et al 2019 ; Saito et al 2019 ; Hori and Saitoh 2020 ; Yang et al 2020 ). Our comparison of ranked TRP expression between Antarctic H. antarcticus and tropical A. burtoni demonstrates that our top candidates for thermosensation have similar ranked expression between the two species in support of the hypothesis that it is primarily structural evolution of existing thermosensors that underlies adaptation to new thermal environments.…”

Diverse sensitivities of TRPA1 from different mosquito species to thermal and chemical stimuli

“…TRPA1 orthologues in rodents were first reported to be involved in cold-evoked events 2 , although their temperature sensitivity is currently controversial. However, many poikilotherm TRPA1s were reported to be activated by warm temperatures 14,29 . Even though these four mosquito species seem closely related, we readily observed differences in TRPA1 properties.…”

“…During evolution animals adapt to habitats with different environmental factors, and even closely related species possess distinct optimal temperature ranges for survival 11–14 . Mosquitoes are crucial vectors for transmission of epidemic diseases in tropical and subtropical areas.…”

Human and Mouse TRPA1 Are Heat and Cold Sensors Differentially Tuned by Voltage

“…The temperature sensitivity of TRPA1, on the other hand, has been reported to be a less evolutionarily conserved activation mode or alternatively occurring at the expense of chemical sensitivity [2,4]. The physiological role of this channel as a heat sensor has likely changed during evolution, potentially altering the preferred temperature ranges among species [5,6] or enabling some of them to detect and transduce infrared signals [4]. In invertebrates and ancestral vertebrates, TRPA1 acts as a heat-sensing ion channel [4,[7][8][9][10][11][12].…”