Thermal sensitivity of lizard embryos indicates a mismatch between oxygen supply and demand at near‐lethal temperatures

Abstract

Aspects of global change create stressful thermal environments that threaten biodiversity. Oviparous, non‐avian reptiles have received considerable attention because eggs are left to develop under prevailing conditions, leaving developing embryos vulnerable to increases in temperature. Though many studies assess embryo responses to long‐term (i.e., chronic), constant incubation temperatures, few assess responses to acute exposures which are more relevant for many species. We subjected brown anole (Anolis sagrei) eggs to heat shocks, thermal ramps, and extreme diurnal fluctuations to determine the lethal temperature of embryos, measure the thermal sensitivity of embryo heart rate and metabolism, and quantify the effects of sublethal but stressful temperatures on development and hatchling phenotypes and survival. Most embryos died at heat shocks of 45°C or 46°C, which is ~12°C warmer than the highest constant temperatures suitable for successful development. Heart rate and O2 consumption increased with temperature; however, as embryos approached the lethal temperature, heart rate and CO2 production continued rising while O2 consumption plateaued. These data indicate a mismatch between oxygen supply and demand at high temperatures. Exposure to extreme, diurnal fluctuations depressed embryo developmental rates and heart rates, and resulted in hatchlings with smaller body size, reduced growth rates, and lower survival in the laboratory. Thus, even brief exposure to extreme temperatures can have important effects on embryo development, and our study highlights the role of both immediate and cumulative effects of high temperatures on egg survival. Such effects must be considered to predict how populations will respond to global change.

Spatial and temporal variation in phenotypes and fitness in response to developmental thermal environments

“…For example, different components of thermal fluctuations such as maximum (Hall & Warner, 2019), minimum (Pruett et al., 2019) and variance in temperature (Du & Shine, 2010) can affect different aspects of development in reptiles, making it difficult to determine which component is inducing the observed effect. Thus, while thermal fluctuations are more ecologically relevant (Hall & Warner, 2020; Les et al., 2007), these conditions in an experiment like ours with eight temperature treatments and four populations would be difficult to interpret.…”

“…Incubators were checked daily for hatchlings, and when found they were weighed, measured (snout–vent length [SVL] and tail length [TL]), given a unique toe clip for identification, and housed individually in a cage (21 cm long × 16.5 cm wide × 11 cm high). Importantly, our body size measurements have previously been shown to be influenced by incubation temperature (Hall & Warner, 2020; Pearson & Warner, 2018) and are associated with survival (Warner & Lovern, 2014; but see Pearson & Warner, 2018). Hatchlings were kept under common thermal conditions that fluctuated daily from about 26–30ºC (due to the 12 hr cycle of overhead lights), watered daily and fed five fruit flies twice weekly while in captivity.…”

“…We provide two possible explanations for this disparity in our laboratory study of embryo development and field studies of maternal nesting behaviour. First, constant incubation temperatures used in the current study may generate reaction norms with peaks at relatively low temperatures compared to a natural fluctuating regime because there is no relief from warmer, thermally stressful conditions (Hall & Warner, 2020). Consequently, we would expect the optimal incubation temperature for hatching success to be slighter higher than that reported here had eggs experienced naturally fluctuating conditions, which would correspond with the observed maternal choices of nest microhabitat by Pruett et al.…”

“…Similarly, warmer temperatures produce hatchlings with better performance (e.g. sprint speed, endurance; Hall & Warner, 2020; Pearson & Warner, 2016) that could increase maternal fitness even if hatching success is slightly decreased. In support of these patterns, we also show that the optimal temperature for post‐hatching survival is greater than that for hatching success; this pattern is discussed further below.…”

Thermal stress induces positive phenotypic and molecular feedback loops in zebrafish embryos

“…High temperatures also accelerate the embryonic development in zebrafish embryos as shown by the 2.8-fold increase in somitogenesis frequency across a 20-30°C range or the twice faster development at 33°C compared to 26°C (Hallare et al, 2005;Long et al, 2012;Schröter et al, 2008). Repeated exposure to sublethal temperatures, however, may depress development (Hall & Warner, 2020a). At the molecular level, heat stress leads to numerous molecular effects from the accumulation of reactive oxygen species (ROS) (Madeira et al, 2016;Vinagre et al, 2012) to changes in global gene expression patterns (Logan & Buckley, 2015;Long et al, 2012;Ribas et al, 2017) along the hypothalamic-pituitary-interrenal (HPI) axis (Alsop & Vijayan, 2009).…”