Chemical Senses Vol. 30 No. suppl 1 © Oxford University
Press 2005; all rights reserved
Potential Multiple Functions of a Male Sea Lamprey Pheromone
Michigan State University, Department of Fish and Wildlife, 13 Natural Resources Building, East Lansing, MI 48824-1222, USA
Correspondence to be sent to: Weiming Li, e-mail: liweim{at}msu.edu
Key words: bile acid, gills, 3-keto-allocholic acid, 3-keto-petromyzonol sulfate, pest control, pheromone, sea lamprey
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Introduction |
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 Top Introduction Structure and function of...Production and release of...Potential application of the...AcknowledgementsReferences |
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The sea lamprey is a useful animal model for understanding the role of olfactory communication in reproduction (Teeter, 1980
;
Li et al., 2003a). Our
research has focused on characterizing the structure and function of pheromones that
signal mating readiness in adults. Sexually mature sea lampreys are virtually blind
(Manion and Hanson, 1980), cease
feeding (Larson, 1980) and likely
coordinate mating and spawning activities through chemical cues (Li et al., 2003a).
Previous studies have indicated that both male and female sea lampreys release
pheromones to attract individuals of the opposite sex (Teeter, 1980). We reasoned that the male pheromone would be
technically advantageous to isolate and identify. This pheromone has to be released in a
large quantity to be effective because males move into the spawning grounds first and
then release a pheromone to guide the females to their nests (Teeter, 1980), which are often built in rapids
where flow rates range between 0.5 and 1.5 m/s (Manion and Hanson, 1980). Further, identification of a male
sea lamprey pheromone could provide a model system for studies of male pheromone
signaling in fish. Several hormonal pheromones have been identified in female teleosts
but not in males (for a review, see
Stacey and Sorensen, 2002).
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Structure and function of male pheromone compounds |
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TopIntroductionStructure and function of...Production and release of...Potential application of the...AcknowledgementsReferences |
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Two novel bile acids, 7
,12,24-trihydroxy-3-one-5-cholan-24-sulfate (3kPZS;
Li et al., 2002;
Yun et al., 2002) and
7,12-dihydroxy-5-cholan-3-one-24-oic acid (3kACA;
Yun et al., 2003), have been
postulated to be components of the male pheromone based on several lines of evidence
(Li et al., 2003a). First,
these two compounds are released only by male lampreys after the onset of spermiation
(Yun et al., 2002, 2003;
Siefkes et al., 2003b) and
it is only spermiating males that releases the male pheromone (Li et al., 2002;
Siefkes et al., 2003a,b).
These results corroborated previous findings that sexually mature males release a
pheromone that attracts sexually mature females (Teeter, 1980) and that water washings from spermiating
males are more stimulatory to adult olfactory organs than those from pre-spermiating
males (Bjerselius et al.,
1996).
Secondly, when measured with electro-olfactogram (EOG) recording, mature female sea
lampreys detect 3kPZS and 3kACA at concentrations as low as 10–12 and
10–10 molar, respectively (Siefkes and Li, 2004). Thirdly, at 
1.7 x
10–10 molar, 3kPZS induces robust preference and search behaviors in
ovulated females placed in a two choice maze (Li
et al., 2002). These behaviors are the same as those induced by
washing of spermiating males (Li et al.,
2002;
Siefkes et al., 2003a,b). In
a natural spawning stream, it appears that 3kPZS induces upstream movement at an even
lower concentration (Siefkes and Li, unpublished). Evidently, 3kPZS is the main component
of the pheromone that is released by spermiating sea lamprey males to attract ovulated
females to their nests (Li et al.,
2002).
Another male bile acid, 3kACA, may also be a component of the male pheromone
(Li et al., 2003a;
Yun et al., 2003). The
timing of 3kACA release is synchronized with 3kPZS (Yun et al., 2002;
Siefkes et al., 2003b). The
exact role of this compound has yet to be determined. Our current hypothesis is that
3kACA may regulate the reproductive endocrine system to promote sexual maturation in
conspecific individuals and thus augment the behavioral responsiveness of adult females
to 3kPZS. There is also evidence indicating that 3kCAC functions as a minor component to
induce search behaviors typically induced by 3kPZS in ovulatory females (unpublished
results).
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Production and release of 3kPZS and 3kACA |
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TopIntroductionStructure and function of...Production and release of...Potential application of the...AcknowledgementsReferences |
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It seems that 3kPZS and 3kACA may have evolved as specialized pheromone signals (Li et al., 2002
, 2003a).
They are not needed for lipid digestion because adult lampreys do not feed (Larson, 1980). Yet, spermiating male hepatocytes
contain higher levels of immunoreactive 3kPZS and 3kACA than pre-spermiating male
hepatocytes (Siefkes et al.,
2003b). Since adult lampreys do not have bile ducts or gall bladders (they
are lost during transformation;
Youson, 1985), bile acids are not
likely released directly into intestine; rather, they are probably transported via the
bloodstream to kidney and gills where they are released into the water. Our experiments
indicate that only washings from the anterior portion of the male lamprey are
immunoreactive for male bile acids, whereas urine contained only a trace amount of 3kPZS
(Yun et al., 2002). In
addition, washing collected directly off the gills contained male bile acids and
pheromone potency (Siefkes et al.,
2003b).
The selection pressure to produce a signal that can be detected from a great distance
in rapidly flowing water may have favored the evolution of a bile acid derivative as a
pheromone—as opposed to the gonadal hormones that commonly act as pheromones in
teleost fish (Stacey and Sorensen,
2002)—since bile acids can be produced in relatively large quantities
due to the synthetic efficiency of the liver (Li
et al., 2002). This gill-based release route is potentially very
efficient and direct because the hepatic veins carry blood directly to the heart and
because all the blood from the heart goes through the gills. However, sulfated steroidal
compounds typically are excreted through the urinary tract and only unconjugated
compounds are shown to diffuse through gill epithelium (Vermeirssen and Scott, 1996). Clearly, a mechanism other
than passive diffusion must have had to evolve in lampreys to excrete a sulfated bile
acid, 3kPZS, into water via their gills. Male sea lamprey gills develop profuse glandular
cells with secretory papillae during spermiation (Siefkes et al., 2003b). These cells were first
found in European river lampreys (Lampetra fluviatis) and speculated to excrete
‘sex substances’ (Pickering,
1977). We have shown that in the sea lamprey, the ‘sex
substances’ include 3kPZS and 3kACA (Siefkes et al., 2003b). The molecular mechanism
for active transportation of male bile acids through the gills has not been elucidated.
Further, synthetic pathways for 3kPZS and 3kACA have not been studied.
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Potential application of the male lamprey pheromone |
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TopIntroductionStructure and function of...Production and release of...Potential application of the...AcknowledgementsReferences |
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A major impetus that drives the quest for identifying sea lamprey pheromones has centered on their potential applications in lamprey management (Teeter, 1980
;
Li et al., 2003b). The sea
lamprey is an invasive species in the Laurentian Great Lakes of North America where it
has caused dramatic and undesirable changes throughout the fish community (Smith and Tibbles, 1980). Our results to date
indicate that interference with the male bile acid pheromone system offers an attractive
target for selective and environmentally benign control of the sea lamprey. A recent
study indicates that traps baited with spermiating males capture up to 87% of the
ovulating females, whereas empty traps and traps baited with non-spermiating males
capture no females (Johnson et al.,
2004). This study confirms a previous report of the ‘infallible’
practice of French fishermen who use male lampreys to bait traps to capture females
(Fontaine, 1938). Whether synthetic
3kPZS and 3kACA can replicate the male washings in trapping ovulatory females has not yet
been determined. None the less, 3kPZS has been found to induce female behaviors similar
to those induced by spermiating male washings (Li
et al., 2002). |
Acknowledgements |
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TopIntroductionStructure and function of...Production and release of...Potential application of the...AcknowledgementsReferences |
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I express my appreciation to the Great Lakes Fishery Commission for its financial support of my research into the sea lamprey pheromone communications and to my collaborators A.P. Scott, M.J. Siefkes, S.-S. Yun, N. Johnson, B. Zielinski and J. Teeter.
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References |
|---|
|
TopIntroductionStructure and function of...Production and release of...Potential application of the...AcknowledgementsReferences |
|---|
Bjerselius, R., Li, W. and Sorensen, P.W. (1996) Spermiated male sea lamprey release a potent sex pheromone. In Thomas, P. and Goetz, F. (eds), Proceedings of the Fifth International Symposium on the Reproductive Physiology of Fish, Austin, TX, p. 271.
Bjerselius, R., Li, W., Teeter, J.H., Seelye, J.G., Johnsen, P.B., Maniak, P.J., Grant, G.C., Polkinghorne, C.N. and Sorensen, P.W. (2000) Direct behavioral evidence that unique bile acids released by larval sea lamprey function as a migratory pheromone. Can. J. Fish. Aquat. Sci., 57, 557–569.[CrossRef]
Fontaine, M. (1938) La lamproie marine. Sa peche et son importance economique. Bull. Sco. Oceanogr. Fr., 17, 1681–1687.
Johnson, N., Siefkes, M.J. and Li, W. (2004) Capturing Ovulating Female Sea Lampreys in Pheromone Baited Traps. North Am. J. Fish. Manag. (in press).
Larson, L.O. (1980) Physiology of adult lampreys, with special regard to natural starvation, reproduction, and death after spawning. Can. J. Fish. Aquat. Sci., 37, 1762–1779.
Li, W., Scott, A.P., Siefkes, M.J., Yan, H., Liu, Q., Yun, S. and Gage, D. (2002) Bile acid secreted by male sea lamprey that acts as a sex pheromone. Science, 296, 138–141.
Li, W., Scott, A.P., Siefkes, M.J., Yun, S.-S. and Zielinski, B. (2003a) A male pheromone in the sea lamprey (Petromyzon marinus): an overview. Comp. Physiol. Biochem., 28, 259–252.
Li, W., Siefkes, M.J., Scott, A.P. and Teeter, J.H. (2003b) Sex pheromone communication in the sea lamprey: implications for integrated management. J. Great Lakes Res., 29(Suppl. 1). 85–94.
Manion, P.J. and Hanson, L.H. (1980) Spawning behavior and fecundity of lampreys from the upper three Great lakes. Can. J. Fish. Aquat. Sci., 37, 1635–1640.
Pickering, A.D. (1977) Sexual dimorphism in the gills of the spawning river lamprey, Lampetra fluviatilis L. Cell Tissue Res., 180, 1–10.[Web of Science][Medline]
Siefkes, M.J. and Li, W. (2004) Detection and discrimination of bile acids of mature male sea lampreys (Petromyzon marinus) by the olfactory epithelium of conspecific females. J. Comp. Physiol. A, 190, 193–199.
Siefkes, M.J., Bergstedt, R.A., Twohey, M.B. and Li, W. (2003a) Chemosterilization of male sea lamprey Petromyzon marinus does not affect sex pheromone release. Can. J. Fish. Aquat. Sci., 60, 23–31.[CrossRef]
Siefkes, M.J., Zielinski, B., Scott, A.P., Yun, S.-S. and Li, W. (2003b) A novel release mechanism for a male sea lamprey sex pheromone. Biol. Reprod., 69, 125–132.
Smith, B.R. and Tibbles, J.J. (1980) Sea lamprey (Petromyzon marinus) in Lake Huron, Michigan, and Superior: history of invasion and control, 1936–78. Can. J. Fish. Aquat. Sci., 37, 1780–1801.
Stacey, N. and Sorensen, P.W. (2002) Hormonal pheromones in fish. In Pfaff, D.W., Arnold, A.P., Etgen, A.M., Fahrbach, S.E. and Rubin, R.T. (eds), Hormones, Brain and Behavior. Elsevier Science, San Diego, CA, pp. 375–434.
Teeter, J. (1980) Pheromone communication in sea lampreys (Petromyzon marinus): implications for population management. Can. J. Fish. Aquat. Sci., 37, 2123–2132.
Vermeirssen, E.L.M. and Scott, A.P. (1996) Excretion of free and conjugated steroids in rainbow trout (Oncorhynchus mykiss): evidence for branchial excretion of the maturation-inducing steroid, 17,20ß-dihydroxy-4-pregnen-3-one. Gen. Comp. Endocrinol., 101, 180–194.[CrossRef][Web of Science][Medline]
Youson, J.H. (1985) Organ development and specialization in lamprey species. In Foreman, R.E., Gorbman, A., Dodd, J.M. and Olsson, R. (eds), Evolutionary Biology of Primitive Fishes. Plenum Press, New York, pp. 141–164.
Yun, S.-S., Siefkes, M.J., Scott, A.P. and Li, W. (2002) Development and application of an ELISA for a sex pheromone released by the male sea lamprey (Petromyzon marinus L.) . Gen. Comp. Endocrinol., 129, 163–170.[CrossRef][Medline]
Yun, S.-S., Scott, A.P. and Li, W. (2003) Pheromones of the male sea lamprey, Petromyzon marinus L.: structural studies on a new compound, 3-keto allocholic acid, and 3-keto petromyzonol sulfate. Steroids, 68, 297–304.[CrossRef][Medline]
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