Olfactory sensitivity to steroid glucuronates in Mozambique tilapia suggests two distinct and specific receptors for pheromone detection

Keller‐Costa, Tina; Canário, Adelino V.M.; Hubbard, Peter C.

doi:10.1242/jeb.111518

Cited by 12 publications

(13 citation statements)

References 42 publications

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“…Although spermine elicits distinct sex specific behavioral responses, both male and female sea lampreys detect spermine at the olfactory level with comparable potencies. This phenomenon is consistent with those responses observed for sex pheromones in sea lamprey [19, 31], goldfish [32, 33], tilapia [34, 35], and some insects [36].…”

Section: Discussionsupporting

confidence: 89%

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

et al. 2019

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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.

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Section: Discussionsupporting

confidence: 89%

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

et al. 2019

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“…6). 107 Females exposed to male urine increase release of the oocyte-maturation hormone 17,20β-P. 106 NMR and comparisons with the analogues indicated the compounds were two stereoisomers of the steroid pregnanetriol 3glucuronate, 5β-pregnane-3α,17α,20α-triol-3α-glucuronate (20α-PG, 28) and 5β-pregnane-3α,17α,20β-triol-3α-glucuronate (20β-PG, 29). Synthetic copies from the precursor 3α, 17-dihydroxy-5βpregnan-20-one showed the same retention time on LC-MS and chemical shifts on NMR spectra, confirming the proposed structures.…”

mentioning

confidence: 99%

Discovery and characterization of natural products that act as pheromones in fish

Buchinger

2018

Nat. Prod. Rep.

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Covering: up to 2018 Fish use a diverse collection of molecules to communicate with conspecifics. Since Karlson and Lüscher termed these molecules 'pheromones', chemists and biologists have joined efforts to characterize their structures and functions. In particular, the understanding of insect pheromones developed at a rapid pace, set, in part, by the use of bioassay-guided fractionation and natural product chemistry. Research on vertebrate pheromones, however, has progressed more slowly. Initially, biologists characterized fish pheromones by screening commercially available compounds suspected to act as pheromones based upon their physiological function. Such biology-driven screening has proven a productive approach to studying pheromones in fish. However, the many functions of fish pheromones and diverse metabolites that fish release make predicting pheromone identity difficult and necessitate approaches led by chemistry. Indeed, the few cases in which pheromone identification was led by natural product chemistry indicated novel or otherwise unpredicted compounds act as pheromones. Here, we provide a brief review of the approaches to identifying pheromones, placing particular emphasis on the promise of using natural product chemistry together with assays of biological activity. Several case studies illustrate bioassay-guided fractionation as an approach to pheromone identification in fish and the unexpected diversity of pheromone structures discovered by natural product chemistry. With recent advances in natural product chemistry, bioassay-guided fractionation is likely to unveil an even broader collection of pheromone structures and enable research that spans across disciplines.

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“…Olfactory responses at such high dilution are not unusual; rather, they are common to odourants considered "pheromones" (Rosenblum et al 1991;Moore and Waring 1996;Stacey 2003). Responses to pheromones may occur at dilutions as high as 1 × 10 −12 mol/L (Li et al 1995;Keller-Costa et al 2014). We are not suggesting that nucleobases are pheromones (i.e., species-specific signals), but we do leave open the possibility that nucleobases are effective at high dilution and may evoke physiological responses.…”

Section: Physiological Responses To Nucleobasesmentioning

confidence: 80%

Nucleobase-containing compounds evoke behavioural, olfactory, and transcriptional responses in model fishes

Shamchuk

Blunt

Lyons

et al. 2018

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The sensory system of animals detects a massive and unknown array of chemical cues that evoke a diversity of physiological and behavioural responses. One group of nitrogen-containing carbon ring chemicals—nucleobases—are thought to be involved in numerous behaviours yet have received little attention. We took a top-down approach to examine responses evoked by nucleobases at behavioural, tissue, and gene expression levels. Fish generally avoided nucleobases, and this behaviour, when observed, was driven by purines but not pyrimidines. At the tissue level, olfactory neuron generator potential responses tended to be concentration specific and robust at concentrations lower than amino acid detection ranges. In terms of gene expression, more than 2000 genes were significantly upregulated following nucleobase exposure, some of which were expected (e.g., genes involved in purine binding) and some of which were not (e.g., tubulin-related genes). Humanized RNA pathway analysis showed that we had exposed the animal to a nucleobase. Our data indicate that responses to nucleobase-containing compounds may be highly structure based and are evident from changes in behaviour to mRNA expression. Many of these responses were surprising, and all provide numerous routes for further research endeavour.

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Olfactory sensitivity to steroid glucuronates in Mozambique tilapia suggests two distinct and specific receptors for pheromone detection

Cited by 12 publications

References 42 publications

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

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

Discovery and characterization of natural products that act as pheromones in fish

Nucleobase-containing compounds evoke behavioural, olfactory, and transcriptional responses in model fishes

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