Early Developmental Decline in HSP Expression Affects Subsequent Response to Transient Heat Exposure

Understanding physiological responses to short-term changes in temperature is of growing interest considering the rising frequency and severity of transient temperatures such as heat waves. During the embryonic development of egg-laying vertebrates, inducible physiological responses to transient heat are likely critical to short-term survival but may also be energetically costly or disruptive to development. Inducible heat-shock proteins (HSPs) are conserved molecular chaperones which act to safeguard cellular protein homeostasis during transient stress. However, experiments in ectotherms have shown that overexpression of HSPs can increase embryonic mortality and reduce later thermotolerance. Yet, few studies have explored natural developmental patterns of HSP expression and heat inducibility in embryos of egg-laying ectothermic vertebrates. Using the red-eared slider turtle (Trachemys scripta), we characterized the response of five HSP genes in embryonic trunks following repeated 3-d transient heat wave exposures. Interestingly, we found that the expression of most HSPs naturally declined during early development and that warm temperatures amplified this decline, while also accelerating developmental rate. Only in a few instances did we observe induction of certain HSP genes during heat wave exposures, though this depended on the thermal history of the embryo. Specifically, induction of these genes during a particular heat wave was reduced in embryos that had already experienced two recent prior exposures relative to those experiencing it for the first or second time, suggesting repeated heat exposures can attenuate subsequent responses. The observed changes in HSP expression and inducibility may relate to an individual's need to balance thermotolerance alongside extensive cellular differentiation and proliferation during early development. The effects of incubation temperature on these changes could also have important implications for how turtle embryos deal with subsequent heat stress and may be similarly present in other ectothermic vertebrates. Our study demonstrates the importance of considering ontogenetic changes in physiological responses to temperature even across embryonic development.