RESUMEN
We found that embryonic behavioral thermoregulation could not enhance the thermoregulatory capacity of turtle hatchlings. Our study is not only the first to provide experimental evidence regarding the impact of embryonic behavioral thermoregulation on offspring thermoregulation but also falsifies the play behavior hypothesis that suggests thermotaxis by embryos allows them to practice thermoregulatory tactics at later life stages.
RESUMEN
Temperature sensing is essential for the survival of living organisms. Some reptile embryos can reposition themselves within the egg to seek optimal temperatures, but the molecular sensors involved in this temperature detection remain unknown. Here, we show that such thermotaxic behavior is directly determined by the activation of two heat-sensitive ion channels of the turtle: the transient receptor potential ankyrin 1 (MrTRPA1) and transient receptor potential vanilloid-1 (MrTRPV1). These two TRP channels were found to exhibit distinctive distributions among turtle dorsal root ganglion (DRG) neurons. Additionally, our laser irradiation assays illustrated that the heat activation thresholds of MrTRPA1 and MrTRPV1 are consistent with the mild (28-33°C) and noxious (>33°C) heat determined by behavioral tests, respectively. Further pharmacological studies have demonstrated that ligand-induced intervention of MrTRPA1 or MrTRPV1 is sufficient to mimic heat stimuli or block temperature signaling, causing changes in embryo movement. These findings indicate that the initiation of thermotaxic response in turtle embryos relies on a delicate functional balance between the heat activation of MrTRPA1 and MrTRPV1. Our study reveals, for the first time, a unique molecular mechanism underlying thermal detection: the two TRP channels act as a physiological tandem to control the thermotaxic behavior of turtle embryos.
Asunto(s)
Tortugas , Animales , Regulación de la Temperatura Corporal , Calor , Canales Catiónicos TRPV , Temperatura , Sensación Térmica/fisiología , Tortugas/fisiologíaRESUMEN
Sessile organisms with thermally sensitive developmental trajectories are at high risk from climate change. For example, oviparous reptiles with temperature-dependent sex determination (TSD) may experience strong (potentially disastrous) shifts in offspring sex ratio if reproducing females are unable to predict incubation conditions at the time of oviposition. How then have TSD reptile taxa persisted over previous periods of extreme climatic conditions? An ability of embryos to move within the egg to select optimal thermal regimes could buffer ambient extremes, but the feasibility of behavioral thermoregulation by embryos has come under strong challenge. To test this idea, we measured thermal gradients within eggs in semi-natural nests of a freshwater turtle species with TSD, manipulated embryonic thermoregulatory ability, and modeled the effects of embryonic thermoregulation on offspring sex ratios. Behavioral thermoregulation by embryos accelerated development and influenced offspring sex ratio, expanding the range of ambient conditions under which nests produce equal numbers of male and female offspring. Model projections suggest that sex ratio shifts induced by global warming will be buffered by the ability of embryos to influence their sexual destiny via behavioral thermoregulation.