Female sea lamprey use seminal pheromones to discriminate among potential mates

Abstract

Females’ ability to select mates that can fertilize eggs directly impacts their fitness, but the secondary sexual traits that often guide mate choice may not be directly correlated with male fertility. In externally fertilizing species, such as many fish species, chemical cues in ejaculates may allow females to assess male fertilization capacity. However, chemical cues associated with sperm release have only been described in a few species, and evidence that females use these cues to discriminate among males remains limited. Female sea lamprey, Petromyzon marinus, use several chemical cues to find and interact with potential mates, including a sex pheromone released by males across their gill epithelia and a second sex pheromone released in their semen. Unlike males of many fish species that control pheromone release via urinary pulses, male sea lamprey continually broadcast the gill pheromone once they are sexually mature. This presents a potentially costly scenario for females because attraction to males that are not actively spawning or that are sperm-depleted likely wastes time and energy. We tested the hypothesis that female sea lamprey use pheromones present in seminal plasma to discriminate among potential mates. In-stream behavioural assays revealed that females (1) preferred seminal plasma + male-conditioned water (containing gill-released pheromones) over male-conditioned water alone, (2) preferred male-conditioned water + 2× seminal plasma over male-conditioned water + 1× seminal plasma and (3) oriented towards seminal plasma over large distances and when no male-conditioned water was applied. Taken together, our results indicate that female sea lamprey use seminal pheromones to find and remain near males with immediate fertilization capacity, thereby reducing the risk of wasting time and energy during their single, reproductive window. Finally, our study highlights the importance of multiple cues in mate choice.