In one species of vocalizing fish, the plainfin midshipman (Porichthys notatus), large, nest-guarding males ('type I') use striated muscles to produce acoustic communication signals that include short duration (< 1 s) 'burps' important in agonistic encounters and long duration (in the order of minutes) 'hums' which function in attracting females to nest sites during the breeding season. Females, and a second group of smaller reproductively active males ('type II') that 'sneak' spawn, do not generate hums, although they produce burps. Differences in vocal behavior are paralled by a relative increase of 6-fold in the sonic muscle of type I males. Inter- and intrasexual dimorphisms in sonic muscle mass were matched by those in the cross-sectional area of sonic motor axons, but not by those in number of axons. Thus, axon size was 2- to 3-fold larger in type I males than in females, type II males, or juveniles, none of which differed significantly from each other. Axon number was similar between type I males and females of a similar body size, despite the extreme dimorphism in sonic muscle mass. Axon number, however, was slightly greater (0.1-fold) in type I males and females compared to the smaller-sized juveniles and type II males. Type II males, in comparison to the non-reproductive juvenile males, have gonads that are about 20-fold larger and produce mature sperm. Nevertheless, the two groups resemble each other in body and swimbladder size, as well as sonic motor axon size and number. This suggests that type II males represent a subset of juvenile males that undergo precocious gonadal hypertrophy and spermiogenesis, but retain juvenile-like nongonadal traits. The results are discussed within the context of the development of vertebrate motor systems as well as the evolution of alternative reproductive tactics among teleost fishes.