Bile Acid Secreted by Male Sea Lamprey That Acts as a Sex Pheromone

Li, Weiming; Scott, Alexander P.; Siefkes, Michael J.; Yan, Honggao; Liu, Qin; Yun, Sang-Seon; Gage, Douglas A.

doi:10.1126/science.1067797

Cited by 330 publications

(306 citation statements)

References 21 publications

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“…Studies of pheromone-mediated behavior of vertebrates in natural habitats have been limited both because relatively few vertebrate pheromones have been chemically identified (3) and because field research on this topic is often constrained by the ecology and behavior of vertebrates (4). Nonetheless, studies of the sea lamprey (Petromyzon marinus), an ancestral vertebrate and destructive invader of the Laurentian Great Lakes (5), indicate that spermiated males release a pheromone, 7␣, 12␣, 24-trihydroxy-5␣-cholan-3-one 24-sulfate (3kPZS) (6), that induces predictable movements in ovulated females in spawning streams (7). We reasoned that the sea lamprey offers a uniquely advantageous model for determining possible applications of pheromones in vertebrate pest control.…”

mentioning

confidence: 99%

A synthesized pheromone induces upstream movement in female sea lamprey and summons them into traps

Johnson

Yun

Thompson

et al. 2009

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

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166

170

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Female insect pheromone blends induce robust tracking responses in males and direct them into traps. In vertebrates, pheromones that induce strong and precise tracking responses in natural habitats have rarely been described. Here, we show in the sea lamprey (Petromyzon marinus), a vertebrate invader of the Laurential Great Lakes, that a synthesized component of the male mating pheromone, 7␣, 12␣, 24-trihydroxy-5␣-cholan-3-one 24-sulfate (3kPZS), when released into a stream to reach concentrations of 10 ؊14 , 10 ؊13 , 10 ؊12 ,10 ؊11 , or 10 ؊10 M, triggers robust upstream movement in ovulated females drawing Ϸ50% into baited traps. Experiments conducted in diverse stream segments demonstrate the level of behavioral response was not affected by habitat conditions and is effective over hundreds of meters. 3kPZS is equally effective at luring ovulated females as the whole pheromone blend released by males between 10 ؊14 and 10 ؊11 M. 3kPZS diverts ovulated females away from and disrupts orientation to male washings when applied at concentrations higher than washings. Indeed, a single pheromone compound is able to redirect female sea lampreys away from a natural pheromone source and lure them into traps, which should be more effective than targeting males when applied in population control. Our findings may spur the discovery of other potent and environmentally benign agents to combat biological invasion, a process accelerated by globalization, exacerbated by climate change, and costing the global economy US$ 1.4 trillion of damage annually.invasive species ͉ odorant tracking ͉ pest control ͉ odorant disruption ͉ jawless vertebrate

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mentioning

confidence: 99%

A synthesized pheromone induces upstream movement in female sea lamprey and summons them into traps

Johnson

Yun

Thompson

et al. 2009

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

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166

170

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“…Significantly, eels seem to have a markedly higher olfactory sensitivity to bile salts than either goldfish or tilapia. Therefore bile salts are good candidates for sex pheromones in this species, as has been previously shown in the sea lamprey (Li et al, 2002;Sorensen et al, 2005). Differences in the composition of the bile fluid between the sexes are also apparent in both the goldfish and tilapia, although they are much less marked than in the eel.…”

Section: Putative Biological Roles Of Olfactory Sensitivity To Bile Amentioning

confidence: 65%

“…Although the biological function of this phenomenon is unclear, with the notable exception of the sea lamprey Petromyzon marinus (Li et al, 2002;Polkinghorne et al, 2001;Sorensen et al, 2005), the stability and water solubility of the bile salt molecule makes it an ideal candidate for a role in chemical communication (Rosenthal and Lobel, 2006). We have recently shown that the odour of bile from the European eel (Anguilla anguilla) depends not only on the sex, but also changes with sexual maturity (Huertas et al, 2007), suggesting a possible role for bile salts as sex pheromones in teleosts.…”

Section: Introductionmentioning

confidence: 99%

Olfactory sensitivity to bile fluid and bile salts in the European eel (Anguilla anguilla), goldfish (Carassius auratus) and Mozambique tilapia (Oreochromis mossambicus) suggests a `broad range' sensitivity not confined to those produced by conspecifics alone

Huertas

Hagey

Hofmann

et al. 2010

Journal of Experimental Biology

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SUMMARYTeleosts have high olfactory sensitivity to bile salts. To assess whether this phenomenon is involved in intra-specific chemical communication alone, or is part of a more 'broad range' sensitivity to bile salts produced by heterospecifics, we investigated possible differences in the odour of bile between the sexes and among different species -the eel (Anguilla anguilla), goldfish (Carassius auratus) and Mozambique tilapia (Oreochromis mossambicus) -using the electro-olfactogram (EOG). We also identified the main bile constituents by liquid chromatography and mass spectrometry. There were marked differences in olfactory response of the eel to thin-layer chromatography fractions of bile from both sexes, and mature and immature conspecifics. Smaller differences were seen in the potency of fractions of bile from male and female goldfish and tilapia. Eels, goldfish and tilapia demonstrated similar olfactory sensitivity to bile from a range of different species, with no apparent correlation between the olfactory potency of bile and a phylogenetic closeness and/or similarity of diet of the donor to the receiver. The three species were able to detect odorants in thin-layer chromatography fractions of heterospecific bile even in the absence of activity in conspecific bile. Eels, goldfish and tilapia responded to both sulphated C 27 bile salts (5-scymnol-sulphate and 5-cyprinol sulphate) and to taurine-conjugated C 24 bile salts (taurochenodeoxycholic acid, taurolithocholic acid and taurocholic acid), irrespective of whether these bile salts were present in conspecific bile. Together, these results suggest that teleosts have a broad-range olfactory sensitivity to bile salts, with potential roles in both intra-specific chemical communication and in inter-specific interactions.

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“…Many fish species release steroids or prostaglandins as sex pheromones (2)(3)(4)(5)(6)(7)(8)(9), as demonstrated in the goldfish (Carassius auratus) (4,5). These pheromones are broadly termed ''hormonal pheromones'' because they or their precursors act as hormones in fishes (10).…”

mentioning

confidence: 99%

l -Kynurenine, an amino acid identified as a sex pheromone in the urine of ovulated female masu salmon

Yambe

Kudoh

Kamio

et al. 2006

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

127

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Many animals employ sex pheromones to find mating partners during their reproductive seasons. However, most sex pheromones of vertebrates remain to be identified. Over the past 20 years, steroids and prostaglandins have been identified as sex pheromones in several fishes. These pheromones are broadly termed “hormonal pheromones” because they or their precursors act as hormones in these fishes. Hitherto, no other type of sex pheromone has been unambiguously identified in teleost fish. Here we report the identification of a “nonhormonal pheromone” in teleost fish. The urine of the reproductively mature female masu salmon ( Oncorhynchus masou ) contains a male-attracting pheromone. Bioassay-guided fractionation yielded an active compound that was identical to l -kynurenine in spectral and chromatographic properties. l -Kynurenine is a major metabolite of l -tryptophan in vertebrates. This pheromone elicits a male-specific behavior at even picomolar concentrations; its electrophysiological threshold is 10 −14 M. l -Kynurenine is a reasonable substance for female masu salmon to advertise their readiness for mating.

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Bile Acid Secreted by Male Sea Lamprey That Acts as a Sex Pheromone

Cited by 330 publications

References 21 publications

A synthesized pheromone induces upstream movement in female sea lamprey and summons them into traps

A synthesized pheromone induces upstream movement in female sea lamprey and summons them into traps

Olfactory sensitivity to bile fluid and bile salts in the European eel (Anguilla anguilla), goldfish (Carassius auratus) and Mozambique tilapia (Oreochromis mossambicus) suggests a `broad range' sensitivity not confined to those produced by conspecifics alone

l -Kynurenine, an amino acid identified as a sex pheromone in the urine of ovulated female masu salmon

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