Within-generation and transgenerational social plasticity interact during rapid adaptive evolution

The effects of within-generation plasticity vs. transgenerational plasticity on trait expression are poorly understood, but important for evaluating plasticity's evolutionary consequences. We tested how genetics, within-generation plasticity, and transgenerational plasticity jointly shape traits influencing rapid evolution in the field cricket Teleogryllus oceanicus. In Hawaiian populations attacked by acoustically orienting parasitoid flies, a protective, X-linked variant ("flatwing") eliminates male acoustic sexual signals. Silent males rapidly spread to fixation, dramatically changing the acoustic environment. First, we found evidence supporting flatwing-associated pleiotropy in juveniles: pure-breeding flatwing males and females exhibit greater locomotion than those with normal-wing genotypes. Second, within-generation plasticity caused homozygous-flatwing females developing in silence, which mimics all-flatwing populations, to attain lower adult body condition and reproductive investment than those experimentally exposed to song. Third, maternal song exposure caused transgenerational plasticity in offspring, affecting adult, but not juvenile, size, condition, and reproductive investment. This contrasted with behavioral traits, which were only influenced by within-generation plasticity. Fourth, we matched and mismatched maternal and offspring social environments and found that transgenerational plasticity sometimes interacted with within-generation plasticity and sometimes opposed it. Our findings stress the importance of evaluating plasticity of different traits and stages across generations when evaluating its fitness consequences and role in adaptation.