Phylogenetic distribution of a male pheromone that may exploit a nonsexual preference in lampreys

Abstract

Pheromones are among the most important sexual signals used by organisms throughout the animal kingdom. However, few are identified in vertebrates, leaving the evolutionary mechanisms underlying vertebrate pheromones poorly understood. Pre-existing biases in receivers’ perceptual systems shape visual and auditory signaling systems, but studies on how receiver biases influence the evolution of pheromone communication remain sparse. The lamprey Petromyzon marinus uses a relatively well-understood suite of pheromones and offers a unique opportunity to study the evolution of vertebrate pheromone communication. Previous studies indicate that male signaling with the mating pheromone 3-keto petromyzonol sulfate (3kPZS) may exploit a nonsexual attraction to juvenile-released 3kPZS that guides migration into productive rearing habitat. Here, we infer the distribution of male signaling with 3kPZS using a phylogenetic comparison comprising six of ten genera and two of three families. Our results indicate that only P. marinus and Ichthyomyzon castaneus release 3kPZS at high rates. Olfactory and behavioral assays with P. marinus, I. castaneus and a subset of three other species that do not use 3kPZS as a sexual signal indicate that male signaling might drive the evolution of female adaptations to detect 3kPZS with specific olfactory mechanisms and respond to 3kPZS with targeted attraction relevant during mate search. We postulate that 3kPZS communication evolved independently in I. castaneus and P. marinus , but cannot eliminate the alternative that other species lost 3kPZS communication. Regardless, our results represent a rare macroevolutionary investigation of a vertebrate pheromone and insight into the evolutionary mechanisms underlying pheromone communication.