Diel Patterns of Pheromone Release By Male Sea Lamprey

2021 ◽  
Author(s):  
Skye D Fissette ◽  
Ugo Busy ◽  
Belinda Huerta ◽  
Cory O Brant ◽  
Ke Li ◽  
...  
Keyword(s):  
Biological Rhythms ◽  
Sea Lamprey ◽  
Behavioral Activity ◽  
Sexual Signals ◽  
Pheromone Communication ◽  
Spawning Activity ◽  
Tissue Samples ◽  
Selective Pressures ◽  
Pheromone Release ◽  
Petromyzonol Sulfate

Abstract Costs to producing sexual signals can create selective pressures on males to invest signaling effort in particular contexts. When the benefits of signaling vary consistently across time, males can optimize signal investment to specific temporal contexts using biological rhythms. Sea lamprey, Petromyzon marinus, have a semelparous life history, are primarily nocturnal, and rely on pheromone communication for reproduction; however, whether male investment in pheromone transport and release matches increases in spawning activity remains unknown. By measuring 1) 3keto-petromyzonol sulfate (3kPZS, a main pheromone component) and its biosynthetic precursor petromyzonol sulfate (PZS) in holding water and tissue samples at 6 points over the course of 24 hours, and 2) 3kPZS release over the course of several days, we demonstrate that 3kPZS release exhibits a consistent diel pattern across several days with elevated pheromone release just prior to sunset and at night. Trends in hepatic concentrations and circulatory transport of PZS and 3kPZS were consistent with patterns of 3kPZS release and suggest the possibility of direct upregulation in pheromone transport and release rather than observed release patterns being solely a byproduct of increased behavioral activity. Our results suggest males evolved a signaling strategy that synchronizes elevated pheromone release with nocturnal increases in sea lamprey behavior. This may be imperative to ensure that male signaling effort is not wasted in a species having a single, reproductive event.

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

2021 ◽  
pp. jeb.229476
Author(s):  
Yu-Wen Chung-Davidson ◽  
Ugo Bussy ◽  
Skye D. Fissette ◽  
Anne M. Scott ◽  
Weiming Li
Keyword(s):  
Bile Salt ◽  
Bile Salts ◽  
Life Stage ◽  
Sea Lamprey ◽  
Life Stages ◽  
Pheromone Production ◽  
Primer Pheromone ◽  
Petromyzonol Sulfate ◽  
Sea Lampreys ◽  
Primer Pheromones

Pheromonal bile salts are important for sea lampreys (Petromyzon marinus Linnaeus) to complete their life cycle. The synthesis and release of a releaser/primer pheromone 3-keto petromyzonol sulfate (3kPZS) by spermiating males have been well characterized. 3kPZS evokes sexual behaviors in ovulatory females, induces immediate 3kPZS release in spermiating males, and elicits neuroendocrine responses in prespawning adults. Another primer pheromone released by spermiating males, 3-keto allocholic acid (3kACA), antagonizes the neuroendocrine effects of 3kPZS in prespermiating males. However, the effects of 3kACA and 3kPZS on pheromone production in prespawning adults is unclear. To understand the foundation of pheromone production, we examined sea lamprey bile salt levels at different life stages. To investigate the priming effects of 3kACA and 3kPZS, we exposed prespawning adults with vehicle or synthetic 3kACA or 3kPZS. We hypothesized that endogenous bile salt levels were life-stage and sex-dependent, and differentially affected by 3kACA and 3kPZS in prespawning adults. Using ultra-performance liquid chromatography tandem mass spectrometry, we found that sea lampreys contained distinct mixtures of bile salts in the liver and plasma at different life stages. Males usually contained higher amounts of bile salts than females. Petromyzonamine disulfate was the most abundant C27 bile salt and petromyzonol sulfate was the most abundant C24 bile salt. Waterborne 3kACA and 3kPZS exerted differential effects on bile salt production in the liver and gill, their circulation and clearance in the plasma, and their release into water. We conclude that bile salt levels are life-stage and sex-dependent and differentially affected by primer pheromones.

scholarly journals The olfactory system of migratory adult sea lamprey (Petromyzon marinus) is specifically and acutely sensitive to unique bile acids released by conspecific larvae.

1995 ◽  
Vol 105 (5) ◽  
pp. 569-587 ◽  
Author(s):  
W Li ◽  
P W Sorensen ◽  
D D Gallaher
Keyword(s):  
Bile Acids ◽  
Olfactory System ◽  
High Performance ◽  
Sea Lamprey ◽  
Sulfate Ester ◽  
Mature Adults ◽  
Freshwater Streams ◽  
Petromyzonol Sulfate ◽  
Receptor Sites ◽  
Cross Adaptation

Larval sea lamprey inhabit freshwater streams and migrate to oceans or lakes to feed after a radical metamorphosis; subsequently, mature adults return to streams to spawn. Previous observations suggested that lamprey utilize the odor of conspecific larvae to select streams for spawning. Here we report biochemical and electrophysiological evidence that this odor is comprised of two unique bile acids released by larvae. High performance liquid chromatography and mass spectrometry demonstrated that larval sea lamprey produce and release two unique bile acids, allocholic acid (ACA) and petromyzonol sulfate (PS). Electro-olfactogram (EOG) recording also demonstrated that the olfactory system of migratory adult sea lamprey is acutely and specifically sensitive to ACA and PS; detection thresholds for these compounds were approximately 10(-12) M. ACA and PS were the most potent of 38 bile acids tested and cross-adaptation experiments suggested that adult sea lamprey have specific olfactory receptor sites associated with independent signal transduction pathways for these bile acids. These receptor sites specifically recognize the key substituents of ACA and PS such as a 5 alpha-hydrogen, three axial hydroxyls, and a C-24 sulfate ester or carboxyl. In conclusion, the unique lamprey bile acids, ACA and PS, are potent and specific stimulants of the adult olfactory system, strongly supporting the hypothesis that these unique bile acids function as migratory pheromones in lamprey.

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

2020 ◽  
Vol 117 (13) ◽  
pp. 7284-7289 ◽  
Author(s):  
Tyler J. Buchinger ◽  
Anne M. Scott ◽  
Skye D. Fissette ◽  
Cory O. Brant ◽  
Mar Huertas ◽  
...  
Keyword(s):  
Communication Systems ◽  
Animal Communication ◽  
Sea Lamprey ◽  
Reliable Communication ◽  
Female Behavior ◽  
Petromyzonol Sulfate ◽  
Electrophysiological Responses ◽  
Sensory Trap ◽  
Nursery Habitats ◽  
Mating Opportunities

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.

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

2020 ◽  
Vol 223 (13) ◽  
pp. jeb226647 ◽  
Author(s):  
Skye D. Fissette ◽  
Ugo Bussy ◽  
Belinda Huerta ◽  
Tyler J. Buchinger ◽  
Weiming Li
Keyword(s):  
Sea Lamprey ◽  
Pheromone Release

Pheromone Communication in Sea Lampreys (Petromyzon marinus): Implications for Population Management

1980 ◽  
Vol 37 (11) ◽  
pp. 2123-2132 ◽  
Author(s):  
John Teeter
Keyword(s):  
Insect Pest ◽  
Petromyzon Marinus ◽  
Sea Lamprey ◽  
Population Management ◽  
Spawning Migration ◽  
Mass Trapping ◽  
Pheromone Communication ◽  
Physiological Factors ◽  
Sea Lampreys ◽  
Opposite Sex

The results of recent preference tests indicate that both male and female landlocked sea lampreys (Petromyzon marinus), after reaching a specific stage of sexual maturation, release pheromones which attract conspecifics of the opposite sex. In addition, sexually immature males, captured at the beginning of a spawning migration, exhibit a preference for water in which sea lamprey larvae have been held, suggesting that chemical signals, originating from populations of sea lamprey larvae in a river, may aid migrating adults in selecting a suitable spawning stream. The possible influence of a number of environmental and physiological factors on pheromone communication in sea lampreys is discussed. Synthetic pheromones have been utilized in insect pest management programs as lures for mass-trapping one or both sexes and for disrupting normal pheromone communication. Similar strategies may be applicable in an integrated program of sea lamprey population management.Key words: pheromones, reproduction, spawning migration, sea lampreys, population management, preference behavior

scholarly journals Sexual attractiveness and reproductive performance in ageing females of a coccoid insect

2018 ◽  
Vol 14 (7) ◽  
pp. 20180262 ◽  
Author(s):  
Jun Tabata ◽  
Mayumi Teshiba
Keyword(s):  
Reproductive Success ◽  
Reproductive Performance ◽  
Sexual Conflict ◽  
Communication System ◽  
Rapid Decline ◽  
Sexual Attractiveness ◽  
Sexual Signals ◽  
Pheromone Communication ◽  
Female Age ◽  
Pheromone Communication System

Female age strongly influences reproductive success in various animals. Males are, therefore, expected to show preferential responses to sexual signals released from females of ages suitable for reproduction. Here, however, we report an unexpected and contradictory effect of ageing on sexual attractiveness and reproductive performance in a coccoid insect: the pheromone-based attractiveness of females increased with ageing, though their reproductive performance was in rapid decline. Surprisingly, senescent females continued releasing relatively high amounts of pheromone and maintained their sexual attractiveness, even at ages when they had almost completely lost fertility, with reduced densities of endosymbionts to support their physiology. Our dataset suggests a potential sexual conflict within a pheromone communication system, where females benefit at males' expense through deceptive signals of fertility.

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