A maternal effect mediates rapid population divergence and character displacement in spadefoot toads

Despite long-standing interest in character displacement, little is known of its underlying proximate causes. Here, we explore the role of maternal effects in character displacement. We specifically investigated whether differences in maternal body condition mediate divergence in the expression of resource-use traits between populations of spadefoot toads (Spea multiplicata) that occur in sympatry with a heterospecific competitor and those that occur in allopatry. In sympatry, S. multiplicata is forced by its competitor onto a less profitable resource. As a result, sympatric females mature in poorer condition and invest less into offspring. Consequently, their offspring produce a resource-use phenotype that minimizes competition with the other species and that also differs from the phenotype produced in allopatry. These differences in trait expression between allopatry and sympatry disappear once mothers are equilibrated in body condition in the laboratory. Thus, a condition-dependent maternal effect mediates population divergence and character displacement. Such effects potentially buffer populations from extinction (via competitive exclusion) while genetic changes accumulate, which produce divergent traits in the absence of the maternal effect. Maternal effects may therefore often be important in determining the initial direction and rate of evolution during the early stages of character displacement.