Evidence that male sea lamprey increase pheromone release after perceiving a competitor

Abstract

Sexual signals evolve via selective pressures arising from male-male competition and female choice, including those originating from unintended receivers that detect the signal. For example, males can acquire information from other males signaling to females and alter their own signal. Relative to visual and acoustic signals, less is known about how such communication networks influence chemical signaling among animals. In sea lamprey (Petromyzon marinus), chemical communication system is essential for reproduction, offering a useful system to study a pheromone communication network that includes signalers and both intended and unintended receivers. Male sea lamprey aggregate on spawning grounds where individuals build nests and signal to females using sex pheromones. We examined how exposure to a major component of the male pheromone, 3keto-petromyzonol sulfate (3kPZS), influenced male pheromone signaling, and whether females had a preference for males that altered their signal. Exposure to 3kPZS, at a concentration of 5x10−10 M, simulated the presence of other male(s) and led to increased 3kPZS release rates within 10 min, followed by a return to baseline levels within 30 min. Exposure also led to increases in hepatic synthesis and circulatory transport of pheromone components. In behavioral assays, females preferred the odor of males that had been exposed to 3kPZS; therefore, males likely benefit from upregulating 3kPZS release after detecting competition for mates. Here, we define how a specific pheromone component influences chemical signaling during intrasexual competition, and show a rare example of how changes in chemical signaling strategies resulting from male competition may influence mate choice.

Plasma metabolomic profiles reveal sex- and maturation-dependent metabolic strategies in sea lamprey (Petromyzon marinus)

“…Intersexual selection through female choice is generally regarded the most important driver of signal evolution (Andersson and Iwasa, 1996;Ord et al, 2001). Indeed, OF prefer higher pheromone levels on spawning grounds (Johnson et al, 2009;Fissette et al, 2020). In addition, SM increases 3kPZS release virtually instantaneously upon detection of 3kPZS, indicating presence of competitor males (Fissette et al, 2020).…”

“…Indeed, OF prefer higher pheromone levels on spawning grounds (Johnson et al, 2009;Fissette et al, 2020). In addition, SM increases 3kPZS release virtually instantaneously upon detection of 3kPZS, indicating presence of competitor males (Fissette et al, 2020). Male signals are typically costly to produce, and thus display frequency may provide a measure of male attractiveness (Davie et al, 2010).…”

“…High inter-male variation in 3kPZS release and female preference for pheromone plumes with higher 3kPZS concentrations indicate 3kPZS likely guides female mate choice (Buchinger et al, 2017;Fissette et al, 2020;Johnson et al, 2009). Indeed, biosynthesis of 3kPZS and possible precursors appears to be under sexual selection (Buchinger et al, 2019).…”

Bile acid production is life-stage and sex dependent and affected by primer pheromones in the sea lamprey

“…Chemical communication is important for sea lampreys to complete their life cycle, including the prespawning migration aided by migratory pheromones released from larvae ( Bjerselius et al, 2000 ; Dvornikovs et al, 2006 ; Hoye et al, 2007 ; Li et al, 2018a ; Sorensen et al, 2005 ), and reproduction facilitated by sex pheromones released from spermiating males ( Buchinger et al, 2017 ; Chung-Davidson et al, 2013a ; Li et al, 2002 ; Scott et al, 2019 ; Siefkes et al, 2005 ). The pheromonal bile salt 3-keto petromyzonol sulfate (3kPZS) released by spermiating males induces sex-dependent reproductive behaviors in spawning adults ( Buchinger et al, 2013 , 2017 ; Li et al, 2002 ; Siefkes et al, 2005 ), and increases immediate 3kPZS release and hepatic production in spermiating males upon detection ( Fissette et al, 2020 ). However, another primer pheromone released by spermiating males, 3-keto allocholic acid (3kACA), seems to antagonize the neuroendocrine effects of 3kPZS in prespermiating males.…”

Circles in the sea: annual courtship “torus” behaviour of basking sharks Cetorhinus maximus identified in the eastern North Atlantic Ocean

“…released by competing males(Fissette et al, 2020). If such sexual signalling occurs in basking sharks, it could also act to increase the chemical signals emanating from a torus that attracts other individuals.…”