Increased pheromone signaling by small male sea lamprey has distinct effects on female mate search and courtship

J of Evolutionary Biology

Bussy

et al. 2017

Pheromones are among the most important sexual signals used by organisms throughout the animal kingdom. However, few are identified in vertebrates, leaving the evolutionary mechanisms underlying vertebrate pheromones poorly understood. Pre-existing biases in receivers' perceptual systems shape visual and auditory signalling systems, but studies on how receiver biases influence the evolution of pheromone communication remain sparse. The lamprey Petromyzon marinus uses a relatively well-understood suite of pheromones and offers a unique opportunity to study the evolution of vertebrate pheromone communication. Previous studies indicate that male signalling with the mating pheromone 3-keto petromyzonol sulphate (3kPZS) may exploit a nonsexual attraction to juvenile-released 3kPZS that guides migration into productive rearing habitat. Here, we infer the distribution of male signalling with 3kPZS using a phylogenetic comparison comprising six of 10 genera and two of three families. Our results indicate that only P. marinus and Ichthyomyzon castaneus release 3kPZS at high rates. Olfactory and behavioural assays with P. marinus, I. castaneus and a subset of three other species that do not use 3kPZS as a sexual signal indicate that male signalling might have driven the evolution of female adaptations to detect 3kPZS with specific olfactory mechanisms and respond to 3kPZS with targeted attraction relevant during mate search. We postulate that 3kPZS communication evolved independently in I. castaneus and P. marinus, but cannot eliminate the alternative that other species lost 3kPZS communication. Regardless, our results represent a rare macroevolutionary investigation of a vertebrate pheromone and provide insight into the evolutionary mechanisms underlying pheromone communication.

Section: Discussionmentioning

confidence: 99%

Phylogenetic distribution of a male pheromone that may exploit a nonsexual preference in lampreys

J of Evolutionary Biology

Bussy

et al. 2017

“…All behavioral assays used ovulated females or spermiated males. Procedures for 2-choice flume and in-stream behavioral assays were slightly modified from previous studies (33,34,45) and are described in SI Appendix. Natural odorants for behavior tests were collected from a captive population of ∼25,000 larvae as previously described (24) and from a group (14 or 20) of males held in 40 L water for 4 h. Synthesized 3kPZS and PZS were prepared by Bridge Organics.…”

Section: Methodsmentioning

confidence: 99%

“…We used odor-choice assays to test our prediction that ovulated females discriminate between larval odor and its partial mimic released by males. First, we used an established in-stream bioassay to test whether females track the male pheromone when it is offered alongside larval odor (26,33). This assay creates a scenario similar to that females face when navigating to males on spawning nests near patches of larval populations.…”

Section: Ovulated Females Discriminate Between Larval Odor and The Malementioning

confidence: 99%

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

Proc. Natl. Acad. Sci. U.S.A.

Scott

Fissette

et al. 2020

Self Cite

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.

“…Notably, P. marinus larvae and sexually mature males synthesize many of the same bile acids (Li et al 1995;Sorensen et al 2005;Brant et al 2013Brant et al , 2016Buchinger et al 2013). However, bile acids produced by larvae are nonsexual traits, whereas bile acids produced by sexually mature males (which do not feed and have a degenerate digestive system) are sexual traits that affect access to mates (Buchinger et al 2017a).…”

Section: Introductionmentioning

confidence: 99%

“…Although liver bile acids are not direct measures of pheromone signals, they allow useful comparisons despite the lack of specific information on pheromone identity in most lampreys. Furthermore, we reasoned that the bile acids produced in the liver are important sexual traits because (1) the liver (which synthesizes bile acids) is essentially the pheromone gland of lamprey and a major determinant of pheromone release (Buchinger et al 2017a) and (2) known liver bile acids are either sex pheromones or pheromone precursors for P. marinus (Li et al 2018b).…”

Section: Introductionmentioning

confidence: 99%

Intra- and Interspecific Variation in Production of Bile Acids That Act as Sex Pheromones in Lampreys

Physiological and Biochemical Zoology

Bussy

et al. 2019

Self Cite

Pheromones are important sexual signals in most animals, but research into their evolution is largely biased toward insects. Lampreys are a jawless fish with a relatively well-understood pheromone communication system, and they offer a useful opportunity to study pheromone evolution in a vertebrate. Once sexually mature, male sea lamprey (Petromyzon marinus) and likely other lampreys produce and release bile acids that act as sex pheromones. Spawning males do not feed and therefore produce bile acids primarily for sexual communication, whereas larvae produce the same bile acids but for digestion, offering an opportunity to compare the evolution of bile acids produced for sexual versus nonsexual functions. We profiled eight pheromonerelated bile acids in livers from larvae and males and determined the effect of life stage on intra-and interspecific variation in bile acid production. Our results indicate less variation among males than larvae within P. marinus but more variation among species for males than larvae. We postulate that bile acid production in males is shaped by directional or stabilizing selection that reduces variance within P. marinus and directional or disruptive selection that promotes diversification across species. Although our results offer support for the role of sexual selection in the evolution of lamprey pheromones, they do not eliminate possible roles of other aspects of lamprey ecology.