Spermine in semen of male sea lamprey acts as a sex pheromone

• Published in: PLoS biology Vol. 17; no. 7; p. e3000332
• Main Authors: Scott, Anne M, Zhang, Zhe, Jia, Liang, Li, Ke, Zhang, Qinghua, Dexheimer, Thomas, Ellsworth, Edmund, Ren, Jianfeng, Chung-Davidson, Yu-Wen, Zu, Yao, Neubig, Richard R, Li, Weiming
• Format: Journal Article
• Language: English
• Published: United States Public Library of Science 09-07-2019; Public Library of Science (PLoS)
• Subjects: Animal behavior; Animal reproduction; Animals; Biology and Life Sciences; Chromatography; Earth Sciences; Ecology and Environmental Sciences; Eggs; Epithelium; Female; Females; Fertilization; Fish; Fish eggs; Fisheries; Fitness; HEK293 Cells; Hormones; Humans; Life sciences; Male; Males; Mass spectrometry; Medicine and Health Sciences; Olfactory epithelium; Olfactory system; Petromyzon - metabolism; Petromyzon - physiology; Petromyzon marinus; Pharmacology; Pheromones; Pheromones - metabolism; Physical Sciences; Physiological aspects; Physiology; Plasma; Polyamines; Reproduction (biology); Reproduction - physiology; Scientific imaging; Sea lamprey; Semen; Semen - metabolism; Sex Attractants - metabolism; Sex pheromone; Sexual reproduction; Spawning; Sperm; Spermatozoa - metabolism; Spermatozoa - physiology; Spermine; Spermine - metabolism; Toxicology; Trends; Vertebrates; United States; East Lansing Michigan; United States > US; China; Michigan
• ISSN: 1545-7885; 1544-9173; 1545-7885
• DOI: 10.1371/journal.pbio.3000332

Semen is fundamental for sexual reproduction. The non-sperm part of ejaculated semen, or seminal plasma, facilitates the delivery of sperm to the eggs. The seminal plasma of some species with internal fertilization contains anti-aphrodisiac molecules that deter promiscuity in post-copulatory females, conferring fitness benefits to the ejaculating male. By contrast, in some taxa with external fertilization such as fish, exposure to semen promotes spawning behaviors. However, no specific compounds in semen have been identified as aphrodisiac pheromones. We sought to identify a pheromone from the milt (fish semen) of sea lamprey (Petromyzon marinus), a jawless fish that spawns in lek-like aggregations in which each spermiating male defends a nest, and ovulatory females move from nest to nest to mate. We postulated that milt compounds signal to ovulatory females the presence of spawning spermiating males. We determined that spermine, an odorous polyamine initially identified from human semen, is indeed a milt pheromone. At concentrations as low as 10-14 molar, spermine stimulated the lamprey olfactory system and attracted ovulatory females but did not attract males or pre-ovulatory females. We found spermine activated a trace amine-associated receptor (TAAR)-like receptor in the lamprey olfactory epithelium. A novel antagonist to that receptor nullified the attraction of ovulatory females to spermine. Our results elucidate a mechanism whereby a seminal plasma pheromone attracts ready-to-mate females and implicates a possible conservation of the olfactory detection of semen from jawless vertebrates to humans. Milt pheromones may also have management implications for sea lamprey populations.