Heat tolerance during embryonic development has not diverged among populations of a widespread species (Sceloporus undulatus)

Abstract

The frequency and magnitude of heat waves have increased in recent decades, imposing additional stresses on organisms in extreme environments. Most reptilian embryos are regularly exposed to thermal stress because they develop in shallow, warm soils for weeks to months. We studied cardiac performance during warming to infer lethal temperatures for embryonic lizards in the Sceloporus undulatus complex. Embryos from four populations throughout the geographical range (New Jersey, South Carolina, Colorado, and Arizona) were warmed at a rate observed in natural nests. Embryos from all populations exhibited a similar pattern of thermal sensitivity, as follows: heart rate rose between 34 and 41°C, remained stable between 41 and 44°C, and dropped sharply between 44 and 47°C. No embryos recovered from cardiac arrest, indicating that the upper lethal temperature was ≤47°C. Despite the putative selective pressures, the thermal limit to cardiac performance seems to have been conserved during the evolution of this species.

Keywords: Critical thermal maximum; embryo; heart rate; survival; temperature; thermal tolerance.

Figure 1:

Soils in Arizona and South Carolina are warmer than those in Colorado and New Jersey. Maximal soil temperatures at a depth of 5 cm at localities closest to our populations: AZ, 33.2° N, 110.0° W; NJ, 39.8° N, 74.7° W; SC, 33.6° N, 81.9° W; and CO, 37.0° N, 105.6° W. Each datum is the mean and standard deviation of monthly maxima between 1979 and 2010, averaged over a grid of 0.312° × 0.312° (National Center for Atmospheric Research, Boulder, CO, USA).

Figure 2:

Mean heart rates of embryos at 24 (circles) and 34°C (triangles) changed slightly throughout development. Data are for lizards from Arizona (black symbols), Colorado (blue symbols), New Jersey (green symbols), and South Carolina (red symbols). Lines represent the relationships estimated from the most likely statistical model.

Figure 3:

Heart rate increased during warming until embryos reached 41–44°C and dropped sharply between 44 and 47°C. Each black line depicts the trajectory of hearts rate for a single embryo. The red lines depict relationships estimated from the most likely general additive mixed model.

Figure 4:

Embryos in natural nests experience temperatures that caused cardiac arrest in our experiment. The plot shows the distribution of maximal temperatures for nests in New Jersey (Angilletta et al., 2009); nearly 22% of the nests exceeded the critical thermal maximum for this population (median = 47°C).