• adaptation;
  • additive genetic variation;
  • Amphibia;
  • evolvability;
  • heritable variation;
  • NCII;
  • quantitative genetics;
  • water potential

Environmental change often requires evolutionary responses, and therefore understanding the genetic architecture of susceptible populations is essential for predicting their capacity to respond adaptively. However, quantitative genetic studies are rarely targeted at populations considered vulnerable to such environmental perturbations. Here, we assess the level of heritable variation in the ability of embryos to tolerate desiccation stress in Pseudophryne guentheri, a terrestrial-breeding frog that is currently experiencing a drying climate. We applied a North Carolina II breeding design to identify sources of genetic and environmental variance, and genotype-by-environment interactions (GEIs), underlying the expression of embryo survival, hatching times, hatchling mass, size, and shape. Our analysis revealed highly significant effects of water potential and maternal effects on all measured traits, while additive genetic effects were significant for hatchling shape, and nonadditive effects were observed for embryo survival. Interestingly, GEIs, including for some traits complex three-way sire-by-dam-by-environment interactions, were significant, indicating that progeny from certain male–female crosses were more tolerant to water stress than others. These findings suggest a limited capacity of P. guentheri to respond to a drying climate, but also reveal that the detrimental effects of nonviable male–female crosses (i.e., genetic incompatibility) can be masked in benign environments.