Male sea lamprey (Petromyzon marinus) release a multi-component mating pheromone, partially comprised of 3-keto petromyzonol sulfate (3kPZS), which initiates upstream movement and close-proximity spawning behaviors in ovulated females. While the chemistry, function, and potential management application of the sea lamprey mating pheromone are relatively well-studied, the evolution the sea lamprey mating pheromone system remains poorly understood. In this dissertation, I present inter- and intra-species comparisons of pheromone communication that provide insights into the evolution of pheromone communication in the sea lamprey. In Chapter 1, I provide a broad review of the chemical cues and pheromones used by the sea lamprey during reproduction, including overviews on of the sea lamprey olfactory system, chemical cues and pheromones, and potential applications to population management. In Chapter 2, I present a phylogenetic comparison of 3kPZS communication across lampreys, including male release of 3kPZS across eleven lamprey species, representing six of ten genera and two of three families, olfactory sensitivity to 3kPZS in four species native to the Laurentian Great Lakes, and sexual responses to 3kPZS in four species native to the Laurentian Great Lakes. The results indicate either independent gains or a single gain and single loss of 3kPZS communication, and represent a rare macroevolutionary investigation of a vertebrate pheromone. In Chapter 3, I provide evidence for partial overlap of the multi-component male mating pheromone across lampreys. Chemical profiling of sexually mature males from eleven species of lamprey indicated the chemical profiles of males are partially shared across species. Behavioral assays conducted with four species sympatric in the Laurentian Great Lakes indicated asymmetric female responses to heterospecific odors, where sea lamprey were attracted to male odors from all species tested but other species generally preferred only the odor of conspecifics. Electro-olfactogram recordings from sea lamprey indicated that although sea lamprey were attracted to male odors from all species, at least some of the compounds that elicited olfactory responses were different in conspecific male odors compared to heterospecific male odors. In Chapter 4, I present evidence that small male sea lamprey exhibit increased relative pheromone signaling driven by a larger pheromone-producing organ, and possible up-regulation of pheromone synthesis. Furthermore, female choice experiments in a natural environment indicate increased pheromone release in small males likely results in higher access to mates. Taken together, this dissertation provides a rare evolutionary perspective on vertebrate pheromones and describes the species-specificity of lamprey pheromones which are being considered as tools to control and restore lamprey populations throughout the world.
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