Behavioural flexibility might help animals cope with costs of genetic variants
under selection, promoting genetic adaptation. However, it has proven challenging
to experimentally link behavioural flexibility to the predicted compensation
of population-level fitness. We tested this prediction using the field cricket
Teleogryllus oceanicus. In Hawaiian populations, a mutation silences males and
protects against eavesdropping parasitoids. To examine how the loss of this critical
acoustic communication signal impacts offspring production and mate location,
we developed a high-resolution, individual-based tracking system for low-light,
naturalistic conditions. Offspring production did not differ significantly in replicate
silent versus singing populations, and fitness compensation in silent conditions
was associated with significantly increased locomotion in both sexes. Our results
provide evidence that flexible behaviour can promote genetic adaptation via
compensation in reproductive output and suggest that rapid evolution of animal
communication systems may be less constrained than previously appreciated.