Dead Spadefoot Tadpoles Adaptively Modify Development in Future Generations: A Novel Form of Nongenetic Inheritance?

Nongenetic inheritance—involving epigenetic, behavioral, or environmental factors—is increasingly viewed as being important in development and evolution. Here, we describe a possible novel form of nongenetic inheritance in the tadpoles of the Mexican Spadefoot (Spea multiplicata): the transmission of information about the environment from dead individuals to living individuals of a later cohort or generation. When we exposed live tadpoles to the remains of desiccated conspecifics from a naturally occurring dry pond, we found that they used phenotypic plasticity to adjust their development in ways that would increase their chances of escaping a drying pond. Specifically, compared to their siblings that were reared with soil lacking tadpole remains, those reared with soil containing desiccated conspecifics grew larger, developed faster, and were more likely to express an alternative, environmentally induced phenotype—a distinctive carnivore morph that is favored in rapidly drying ponds. We also found evidence of underlying genetic variation in the plasticity to produce carnivores, suggesting that this plasticity could mediate adaptive evolution when populations experience different environmental conditions. Such a tendency of living individuals to respond to cues associated with dead individuals from a previous generation may be vital in giving each generation a head start in their environment.