Nonsequential developmental trajectories lead to dimorphic vocal circuitry for males with alternative reproductive tactics.

Abstract

Midshipman fish, Porichthys notatus, have two male reproductive morphs: type 1 males generate long duration advertisement calls ("hums") to attract females to a nest; type II males sneak-spawn and, like females, do not produce mate calls but generate short duration agonistic calls. A vocal pacemaker circuit includes: motoneurons in the caudal brain stem and rostral spinal cord that innervate vocal/sonic muscles; pacemaker neurons that are located ventrolateral to motoneurons and establish their fundamental discharge frequency; and a ventral medullary nucleus that couples the motoneuron-pacemaker circuit bilaterally. Transneuronal biocytin transport identified morph-specific developmental trajectories for the vocal circuit. Among nonreproductive, juvenile type I males, motoneuron soma size and motor nucleus volume increase most during a stage prior to sexual maturation. An additional increase in motoneuron size and nucleus volume is coupled to the greatest increase in pacemaker soma size at a stage coincident with the onset of sexual maturity; ventral medullary neurons show similar growth increments during both stages. Type II males (and females) mature with no or little change in cell size or motor nucleus volume. The results indicate that alternative mating tactics are paralleled by alternative developmental trajectories for the neurons that determine tactic-specific behaviors, in this case vocalizations. Together with aging data based on otolith growth, the results support the hypothesis that alternative male morphs in midshipman fish adopt nonsequential, mutually exclusive life history tactics.