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

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 signalling 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 signalling with the mating pheromone 3‐keto petromyzonol sulphate (3k PZS ) may exploit a nonsexual attraction to juvenile‐released 3k PZS that guides migration into productive rearing habitat. Here, we infer the distribution of male signalling with 3k PZS using a phylogenetic comparison comprising six of 10 genera and two of three families. Our results indicate that only P. marinus and Ichthyomyzon castaneus release 3k PZS at high rates. Olfactory and behavioural assays with P. marinus, I. castaneus and a subset of three other species that do not use 3k PZS as a sexual signal indicate that male signalling might have driven the evolution of female adaptations to detect 3k PZS with specific olfactory mechanisms and respond to 3k PZS with targeted attraction relevant during mate search. We postulate that 3k PZS communication evolved independently in I. castaneus and P. marinus , but cannot eliminate the alternative that other species lost 3k PZS communication. Regardless, our results represent a rare macroevolutionary investigation of a vertebrate pheromone and provide insight into the evolutionary mechanisms underlying pheromone communication.