Synergistic behavioral antagonists of a sex pheromone reduce reproduction of invasive sea lamprey

Sex pheromones impart maximal attraction when their components are present at optimal ratios that confer balanced olfactory inputs in potential mates. Altering ratios or adding pheromone analogs to optimal mixtures may disrupt balanced olfactory antagonism and result in reduced attraction, however, tests in natural populations are lacking. We tested this hypothesis in sea lamprey (Petromyzon marinus), a fish whose male sex pheromone attracts females when two critical components, 3-keto petromyzonol sulfate (3kPZS) and petromyzonol sulfate (PZS), are present at certain ratios. Here, we report a pheromone analog, petromyzonol tetrasulfate (3sPZS), reduced female attraction to 3kPZS but not to PZS. 3sPZS mixed with additional PZS synergistically disrupted female attraction to the male pheromone and reduced spawning by 97% in a high-density population. Our results provide evidence of balanced olfactory antagonism in a vertebrate and establish a tactic to disrupt spawning of sea lamprey, a destructive invader of the Laurentian Great Lakes.