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Responses of round goby (Neogobius melanostomus) olfactory epithelium to steroids released by reproductive males

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Abstract

The wild perciform teleost Neogobius melanostomus (the round goby) originated from the Ponto-Caspian region and is now a highly successful invasive species in the Laurentian Great Lakes. Males may attract females into their nests for spawning by releasing reproductive pheromones, and it has been previously shown that reproductive males synthesize and release the 5β-reduced and 3α-hydroxyl steroids 3α-hydroxy-5β-androstane-11,17-dione (11-oxo-etiocholanolone; 11-O-ETIO) and 3α-hydroxy-5β-androstane-11,17-dione 3-sulfate (11-oxo-etiocholanolone-3-sulfate; 11-O-ETIO-3-s) and 3α,17β-dihydroxy-5β-androstan-11-one 17-sulfate. In this study, we investigated properties of these released steroids by recording field potential responses from the olfactory epithelium (electro-olfactogram, EOG). The steroid 3α,17β-dihydroxy-5β-androstan-11-one 17-sulfate did not elicit olfactory responses while both 11-O-ETIO and 11-O-ETIO-3-s stimulated olfactory field potentials in the round goby, but not in the goldfish. Cross-adaptation analysis demonstrated that round gobies discriminated between11-O-ETIO and 11-O-ETIO-3-s (as well as etiocholanolone, ETIO) at the sensory level. Second messenger cascades depending on both cAMP and IP3 were inferred for steroids from pharmacological inhibition studies, while the canonical teleost odors taurocholic acid (a bile acid) and l-alanine (an amino acid) used only cAMP and IP3, respectively. The round goby presents itself as an excellent species for the study of olfactory function of fish in the wild, given its possible use of these released steroids as pheromones.

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Abbreviations

ETIO:

Etiocholanolone

ETIO-G:

Etiocholanolone glucosiduronate

11-O-ETIO:

11-Oxo-etiocholanolone

11-O-ETIO-3-s:

11-Oxo-etiocholone-3-sulfate

TCA:

Taurocholic acid

17α,20β-P:

17α,20β-dihydroxy-4-pregnen-3-one

EOG:

Electro-olfactogram

RM:

Reproductive male

RF:

Reproductive female

NRF:

Non-reproductive female

NRM:

Non-reproductive male

OSN:

Olfactory sensory neuron

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Acknowledgments

The authors wish to thank Dr. S.J. Loeb for performing the mass spectrometry. For technical support and advice: Dr. Alexander P. Scott, Dr. Huiming Zhang, Dr. Yogesh Katare and Warren Green. Many students helped with the collection and care of fish, but particularly Jeff Zeyl, Ashley Kasurak, Sarah Hanik and Touba Warsi. All animal collection, housing and experimental procedures were in accordance with the guidelines of the Canadian Council on Animal Care. Funding sources: NSERC Strategic Project STPGP 322217-05, and NSERC Discovery Grant to BZ, Ontario Graduate Scholarship to AL, and the Faculty of Graduate studies at the University of Windsor.

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  1. Department of Biological Sciences, University of Windsor, Windsor, ON, Canada

    Alyson J. Laframboise & Barbara S. Zielinski

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  1. Alyson J. Laframboise
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  2. Barbara S. Zielinski
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Correspondence to Barbara S. Zielinski.

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Laframboise, A.J., Zielinski, B.S. Responses of round goby (Neogobius melanostomus) olfactory epithelium to steroids released by reproductive males. J Comp Physiol A 197, 999–1008 (2011). https://doi.org/10.1007/s00359-011-0662-5

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