Inheritance of environmental variation in body size: Superparasitism of seeds affects progeny and grandprogeny body size via a nongenetic maternal effect

Maternal effects provide the most common mechanism by which environmental variation in one generation affects the phenotype of individuals in subsequent generations. In egg-laying animals, however, we typically observe that maternal effects can have large influences on early growth (egg size and early development), but these effects gradually disappear and become undetectable by the time progeny mature due to developmental plasticity in progeny. We describe a system in which an environmentally induced reduction in body size is inherited by progeny via a nongenetic maternal effect. The seed beetle, Callosobruchus maculatus, completes development inside a discrete resource package (a seed) selected by its mother. Due to superparasitism in response to low host availability, progeny frequently develop at high densities, resulting in intense larval competition and pupation at a smaller body size. Females reared at higher density (and thus emerging smaller) lay smaller eggs than females reared at lower density. Progeny from these smaller eggs mature at a smaller size than progeny reared from the larger eggs laid by females reared at lower density. Crosses between high and low density lines demonstrated that treatment differences in body size are maternally inherited, confirming that the inheritance of body size variation in part involves an environmentally based maternal effect.