Environmental Stress Increases the Magnitude of Nonadditive Genetic Variation in Offspring Fitness in the FrogCrinia georgiana

Abstract

When organisms encounter heterogeneous environments, selection may favor the ability of individuals to tailor their phenotypes to suit the prevailing conditions. Understanding the genetic basis of plastic responses is therefore vital for predicting whether susceptible populations can adapt and persist under new selection pressures. Here, we investigated whether there is potential for adaptive plasticity in development time in the quacking frog Crinia georgiana, a species experiencing a drying climate. Using a North Carolina II breeding design, we exposed 90 family groups to two water depth treatments (baseline and low water) late in larval development. We then estimated the contribution of additive and nonadditive sources of genetic variation to early offspring fitness under both environments. Our results revealed a marked decline in larval fitness under the stressful (low water) rearing environment but also that additive genetic variation was negligible for all traits. However, in most cases, we found significant sire-by-dam interactions, indicating the importance of nonadditive genetic variation for offspring fitness. Moreover, sire-by-dam interactions were modified by the treatment, indicating that patterns of nonadditive genetic variance depend on environmental context. For all traits, we found higher levels of nonadditive genetic variation (relative to total phenotypic variation) when larvae were reared under stressful conditions, suggesting that the fitness costs associated with incompatible parental crosses (e.g., homozygous deleterious recessive alleles) will only be expressed when water availability is low. Taken together, our results highlight the need to consider patterns of nonadditive genetic variation under contrasting selective regimes when considering the resilience of species to environmental change.

Genetic benefits of extreme sequential polyandry in a terrestrial‐breeding frog

“…In a more recent study in this species (also using a North Carolina II breeding design), Rudin‐Bitterli et al. () confirmed high levels of nonadditive genetic variance for offspring fitness, and showed that levels of nonadditive genetic variation were significantly higher when offspring were reared under stressful conditions. In quacking frogs, males force copulation and multiple male amplexus imposes large fitness costs to females through reduced fertilization success (Byrne and Roberts ).…”

“…; Rudin‐Bitterli et al. ). Causes of environmental‐maternal effects are diverse, but they are typically related to variation in the degree to which females invest in offspring (Wolf and Wade ).…”

“…; Rudin‐Bitterli et al. ). Moreover, such effects have been found in the terrestrial toadlet P. guentheri (Eads et al.…”

“…Importantly, in this design the influence of environmental effects can be manipulated and minimized by raising half‐sibs in a controlled environment (Rudin‐Bitterli et al. ).…”

“…Across multiple crosses (families), variance in offspring fitness can then be precisely partitioned among additive genetic effects (good genes), nonadditive effects (compatible genes), and maternal effects (encompassing maternal genetic effects and environmental effects) (Simmons 2005). Importantly, in this design the influence of environmental effects can be manipulated and minimized by raising half-sibs in a controlled environment (Rudin-Bitterli et al 2018).…”