A pheromone antagonist liberates female sea lamprey from a sensory trap to enable reliable communication

Abstract

The evolution of male signals and female preferences remains a central question in the study of animal communication. The sensory trap model suggests males evolve signals that mimic cues used in nonsexual contexts and thus manipulate female behavior to generate mating opportunities. Much evidence supports the sensory trap model, but how females glean reliable information from both mimetic signals and their model cues remains unknown. We discovered a mechanism whereby a manipulative male signal guides reliable communication in sea lamprey (Petromyzon marinus). Migratory sea lamprey follow a larval cue into spawning streams; once sexually mature, males release a pheromone that mimics the larval cue and attracts females. Females conceivably benefit from the mimetic pheromone during mate search but must discriminate against the model cue to avoid orienting toward larvae in nearby nursery habitats. We tested the hypothesis that spawning females respond to petromyzonol sulfate (PZS) as a behavioral antagonist to avoid attraction to the larval cue while tracking the male pheromone despite each containing attractive 3-keto petromyzonol sulfate (3kPZS). We found 1) PZS inhibited electrophysiological responses to 3kPZS and abated preferences for 3kPZS when mixed at the same or greater concentrations, 2) larvae released more PZS than 3kPZS whereas males released more 3kPZS than PZS, and 3) mixtures of 3kPZS and PZS applied at ratios measured in larval and male odorants resulted in the discrimination observed between the natural odors. Our study elucidates how communication systems that arise via deception can facilitate reliable communication.

Chemical cues for intraspecific chemical communication and interspecific interactions in aquatic environments: applications for fisheries and aquaculture

“…The sex pheromones of sea lampreys appear to have evolved from their migratory pheromone cueing pathway (Buchinger et al 2013(Buchinger et al , 2020Brant et al 2016a). Initially, 3kPZS was one of the by-products derived from bile acids in larvae of sea lamprey.…”

Sensory trap leads to reliable communication without a shift in nonsexual responses to the model cue

“…However, ovulated females searching for mates encounter 3kPZS from both males and larvae, as larvae reside in habitats immediately downstream of and sometimes interspersed with spawning grounds. Consistent with the presumed costs of confusing larval odor (the model cue) and the male pheromone (the mimetic signal; see Dalziell and Welbergen 2016 for a general discussion on mimicry), ovulated females discriminate against larval odor and orient only toward the male pheromone during spawning ( Buchinger et al 2020 ). A mechanism underlying this discrimination is a pheromone antagonist, petromyzonol sulfate (PZS), which abates ovulated female preference for 3kPZS when mixed at equal or greater concentrations than 3kPZS and which larvae, but not males, release at higher rates than 3kPZS ( Figure 1A ; Buchinger et al 2020 ).…”

“…Despite the deceptive origin of 3kPZS signaling, ovulated female sea lamprey evolved to use the male pheromone for reliable sexual communication ( Buchinger et al 2020 ). Sea lamprey die after a single spawning season, and ovulated females have only a few days to a week to find males and spawn ( Applegate 1950 ; Johnson et al 2015 ).…”

Pedigree analysis and estimates of effective breeding size characterize sea lamprey reproductive biology

“…The Ocqueoc River has had an electric barrier in place since 1951 (Smith & Tibbles, 1980 ), with a permanent barrier installed since 1999. The area upstream of the barrier is the site of annual experiments that involve the release of thousands of adult female sea lamprey (Buchinger et al, 2020 ; Johnson et al, 2014 ; Wagner et al, 2018 ). Adult males are not included in experimental releases, so no successful spawning was expected in the system.…”