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Identification of a New Set of Polypeptidic Sex Pheromones from Cuttlefish (Sepia officinalis)

Marine Biotechnology volume 24, pages 574–587 (2022)Cite this article

Abstract

The common English Channel cuttlefish (Sepia officinalis) reproduces every year on very localized coastal spawning areas after a west–east horizontal migration of several tens of kilometers (80–200 km). The massive arrival of spawners on the coasts of west Cotentin and the Bay of Seine is suspected to be driven by the action of sex pheromones expressed and secreted by the genitals of sexually mature females. The present study aims to verify the existence of polypeptide pheromones, of a higher molecular weight than those described above. Their size could confer them a wider range of action than that of the previously identified peptide pheromones. The implementation of an experimental strategy combining transcriptomics and proteomics with functional tests and an in silico study led to the identification of a cocktail of pheromones with molecular weights ranging between 22 and 26 kDa. Proteomic analyses combined to functional tests revealed partial pheromone release in the environment, and their accumulation in the outer capsule of the egg, suggesting the eggs as pheromone diffusers, also able to induce stimulation by contact when the eggs are handled by females.

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References

  • Anraku K, Archdale MV, Hatanaka K, Marui T (2005) Chemical stimuli and feeding behavior in octopus. Phuket Mar Biol Cent Res Bull 66:221–227

    Google Scholar 

  • Arnold J (1962) Mating behavior and social structure in Loligo pealeii. Biol Bull 123:53–57

    Article  Google Scholar 

  • Audesirk TE (1977) Chemoreception in Aplysia californica III. Evidence for pheromones influencing reproductive behavior. Behav Biol 20:235–243

    CAS  Article  PubMed  Google Scholar 

  • Begnoche V, Moore SK, Blum N et al (1996) Sign stimulus activates a peptidergic neural system controlling reproductive behavior in Alpysia. J Neurophysiol 75:2161–2166

    CAS  Article  Google Scholar 

  • Boal JG, Prosser KN, Holm JB et al (2010) Sexually mature cuttlefish are attracted to the eggs of conspecifics. J Chem Ecol 36:834–836

    CAS  Article  PubMed  Google Scholar 

  • Buresch KC, Boal JG, Nagle GT et al (2004) Experimental evidence that ovary and oviducal gland extracts influence male agonistic behavior in squids. Biol Bull 206:1–3

    Article  PubMed  Google Scholar 

  • Buresi A, Croll RP, Tiozzo S et al (2014) Emergence of sensory structures in the developing epidermis in sepia officinalis and other coleoid cephalopods. J Comp Neurol 522:3004–3019

    CAS  Article  PubMed  Google Scholar 

  • Cornet V, Henry J, Corre E et al (2014) Dual role of the cuttlefish salivary proteome in defense and predation. J Proteomics 108:209–22

  • Cummins SF, Boal JG, Buresch KC et al (2011) Extreme aggression in male squid induced by a β -MSP-like pheromone. Curr Biol 21:322–327

    CAS  Article  PubMed  Google Scholar 

  • Cummins SF, Erpenbeck D, Zou Z et al (2009a) Candidate chemoreceptor subfamilies differentially expressed in the chemosensory organs of the mollusc Aplysia. BMC Biol 7:28

    Article  PubMed  PubMed Central  Google Scholar 

  • Cummins SF, Leblanc L, Degnan BM, Nagle GT (2009b) Molecular identification of candidate chemoreceptor genes and signal transduction components in the sensory epithelium of Aplysia. J Exp Biol 212:2037–2044

    CAS  Article  PubMed  Google Scholar 

  • Cummins SF, Nichols AE, Amare A et al (2004a) Characterization of Aplysia enticin and temptin, two novel water-borne protein pheromones that act in concert with attractin to stimulate mate attraction. J Biol Chem 279:25614–25622

    CAS  Article  PubMed  Google Scholar 

  • Cummins SF, Nichols AE, Rajarathnam K, Nagle GT (2004b) A conserved heptapeptide sequence in the waterborne attractin pheromone stimulates mate attraction in Aplysia. Peptides 25:185–189

    CAS  Article  PubMed  Google Scholar 

  • Cummins SF, Nichols AE, Warso CJ, Nagle GT (2005) Aplysia seductin is a water-borne protein pheromone that acts in concert with attractin to stimulate mate attraction. Peptides 26:351–359

    CAS  Article  PubMed  Google Scholar 

  • Cummins SF, Xie F, de Vries MR et al (2007) Aplysia temptin − the ‘glue’ in the water-borne attractin pheromone complex. FEBS J 274:5425–5437

    CAS  Article  PubMed  Google Scholar 

  • DiMarco FP, Hanlon RT (2010) Agonistic behavior in the squid Loligo plei (Loliginidae, Teuthoidea): fighting tactics and the effects of size and resource value. Ethology 103:89–108

    Article  Google Scholar 

  • Enault J, Zatylny-Gaudin C, Bernay B et al (2012) A complex set of sex pheromones identified in the cuttlefish Sepia officinalis. PLoS ONE 7:e46531

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Gilly WF, Lucero MT (1992) Behavioral responses to chemical stimulation of the olfactory organ in the squid Loligo opalescens. J Exp Zool 162:209–229

    CAS  Google Scholar 

  • Graziadei P (1964) Receptors in the sucker of the cuttlefish. Nature 203:384–386

    CAS  Article  PubMed  Google Scholar 

  • Graziadei P (1962) Receptors in the suckers of octopus. Nature 195:57–59

    Article  Google Scholar 

  • Hanlon RT (1996) Evolutionary games that squids play: fighting, courting, sneaking, and mating behaviors used for sexual selection in Loligo pealei. Biol Bull 191:309–310

    CAS  Article  PubMed  Google Scholar 

  • King AJ, Adamo SA, Hanlon RT (1999) Contact with squid egg capsules increases agonistic behavior in male squid (Loligo pealei). Biol Bull 197:256–256

    CAS  Article  PubMed  Google Scholar 

  • King AJ, Adamo SA, Hanlon RT (2003) Squid egg mops provide sensory cues for increased agonistic behaviour between male squid. Anim Behav 66:49–58

    Article  Google Scholar 

  • Painter SD, Chong MG, Wong MA et al (1991) Relative contributions of the egg layer and egg cordon to pheromonal attraction and the induction of mating and egg-laying activity in Aplysia. Biol Bull 181:81–94

    CAS  Article  Google Scholar 

  • Painter SD, Cummins SF, Nichols AE et al (2004) Structural and functional analysis of Aplysia attractins, a family of water-borne protein pheromones with interspecific attractiveness. Proc Natl Acad Sci U S A 101:6929–6933

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Polese G, Bertapelle C, Di Cosmo A (2015) Role of olfaction in Octopus vulgaris reproduction. Gen Comp Endocrinol 210:55–62

    CAS  Article  PubMed  Google Scholar 

  • Polese G, Bertapelle C, Di Cosmo A (2016) Olfactory organ of Octopus vulgaris : morphology, plasticity, turnover and sensory characterization. Biol Open 5:611–619

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Scaros AT, Andouche A, Baratte S, Croll RP (2020) Histamine and histidine decarboxylase in the olfactory system and brain of the common cuttlefish Sepia officinalis (Linnaeus, 1758). J Comp Neurol 528:1095–1112

    CAS  Article  PubMed  Google Scholar 

  • Scaros AT, Croll RP, Baratte S (2018) Immunohistochemical approach to understanding the organization of the olfactory system in the cuttlefish, Sepia officinalis. ACS Chem Neurosci 9:2074–2088

    CAS  Article  PubMed  Google Scholar 

  • Wertz A, Rössler W, Obermayer M, Bickmeyer U (2006) Functional neuroanatomy of the rhinophore of Aplysia punctata. Front Zool 3:6

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Zatylny-Gaudin C, Cornet V, Leduc A et al (2016) Neuropeptidome of the cephalopod Sepia officinalis : identification, tissue mapping, and expression pattern of neuropeptides and neurohormones during egg laying. J Proteome Res 15:48–67

    CAS  Article  PubMed  Google Scholar 

  • Zatylny-Gaudin C, Henry J (2018) Egg-laying in the cuttlefish Sepia officinalis. In: Biolog Res Water InTech

  • Zatylny C, Gagnon J, Boucaud-Camou E, Henry J (2000) ILME: a waterborne pheromonal peptide released by the eggs of Sepia officinalis. Biochem Biophys Res Commun 275:217–222

    CAS  Article  PubMed  Google Scholar 

Download references

Acknowledgements

We thank the Country Council of Low Normandy that funded the thesis of Maxime Endress and the University of Caen Normandy for the financing of experimental work. We also thank Jean-Luc Blaie, the captain of fishing boat “Père Daniel,” and his crew as well as the marine station of Luc-sur-Mer (University of Caen Normandy) for providing cuttlefish.

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Authors and Affiliations

  1. Laboratoire de Biologie Des Organismes Et Ecosystèmes Aquatiques (BOREA), Université de Caen-Normandie, MNHN, SU, UA, CNRS, IRD-207, 14 000, Caen, France

    Céline Gaudin-Zatylny, Maxime Endress, Alexandre Leduc & Joël Henry

  2. Normandie Univ, UNICAEN, UMR 8067 BOREA, MNHN, SU, UA, CNRS, IRD-207, 14 000, Caen, France

    Céline Gaudin-Zatylny, Erwan Corre, Maxime Endress, Alexandre Leduc & Joël Henry

  3. CNRS, Sorbonne Université, R242429680, ABiMS, Station Biologique, 29680, Roscoff, France

    Bruno Zanuttini

  4. Normandie Univ, UNICAEN, ENSICAEN, CNRS, GREYC, 14 000, Caen, France

    Benoît Bernay, Julien Pontin & Joël Henry

  5. Normandie Univ, UNICAEN, SF ICORE 4206, US EMerode, Proteogen plateform, 14000, Caen, France

    Joël Henry

Authors
  1. Céline Gaudin-Zatylny
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  2. Erwan Corre
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  3. Bruno Zanuttini
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  4. Maxime Endress
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  5. Benoît Bernay
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  6. Julien Pontin
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  7. Alexandre Leduc
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  8. Joël Henry
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Correspondence to Joël Henry.

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Gaudin-Zatylny, C., Corre, E., Zanuttini, B. et al. Identification of a New Set of Polypeptidic Sex Pheromones from Cuttlefish (Sepia officinalis). Mar Biotechnol 24, 574–587 (2022). https://doi.org/10.1007/s10126-022-10126-y

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  • DOI: https://doi.org/10.1007/s10126-022-10126-y

Keywords

  • Sepia officinalis
  • Cephalopod
  • Reproduction
  • Proteomics
  • Oviduct gland
  • Sex pheromones