The journey of squid sperm

Abstract

Sperm storage is common in internally fertilizing animals, but is also present in several external fertilizers, such as many cephalopods. Cephalopod males attach sperm packets (spermatangia) to female conspecifics during mating. Females of eight externally fertilizing families comprising 25% of cephalopod biodiversity have sperm-storage organs (seminal receptacles) in their buccal area, which are not in direct physical contact with the deposited spermatangia. The mechanism of sperm transmission between the implantation site and the storage organ has remained a major mystery in cephalopod reproductive biology. Here, jumbo squid females covering almost the entire life cycle, from immature to a laboratory spawned female, were used to describe the internal structure of the seminal receptacles and the process of sperm storage. Seminal fluid was present between the spermatangia and seminal receptacles, but absent in regions devoid of seminal receptacles. The sperm cellular component was formed by spermatozoa and round cells. Although spermatozoa were tracked over the buccal membrane of the females to the inner chambers of the seminal receptacles, round cells were not found inside the seminal receptacles, suggesting that spermatozoa are not sucked up by the muscular action of the seminal receptacles. This finding supports the hypothesis that spermatozoa are able to actively migrate over the female skin. Although further experimental support is needed to fully confirm this hypothesis, our findings shed light on the elusive process of sperm storage in many cephalopods, a process that is fundamental for understanding sexual selection in the sea.

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Acknowledgements

We thank Diana H. Li, Hannah Rosen, Elan Portner, Patrick C. Daniel and Timothy H. Frawley for their valuable help in the collection of jumbo squids. Thanks to Mr. J. M. Fortuño (Electron Microscopy Service, ICM) for his dedication and kindness during the SEM sessions and Mr. J. M. Anguita (ICM) for the elaboration of Fig. 2a. We thank the editor and two anonymous reviewers for their helpful comments. This study was funded by the research project CALOCEAN-2 (AGL2012-39077) from the Ministry of Economy and Competitiveness (MINECO) of Spain. FAFA was supported by two Grants (BES-2013-063551 and EEBB-I-15-09631) from MINECO. HJTH was financed by a Grant (CP1218) of the Cluster of Excellence 80 “The Future Ocean”, funded within the framework of the Excellence Initiative by the Deutsche Forschungsgemeinschaft (DFG) on behalf of the German federal and state governments. Support from Grants OCE-1338973 RAPID, IOS-142093 EAGER, OCE 0850839 and IOS-1557754 (US National Science Foundation), and N000140911054 (US Office of Naval Research) is also acknowledged.

Author contributions

FAFA, RV, HJTH and WFG conceived the study. FAFA and WFG performed the samplings. FAFA performed the histology and SEM observations. All authors contributed to the interpretation of the material, the writing of the manuscript, and its revision, and approved its final version. All the authors agree to be accountable for the content.

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Correspondence to Fernando Á. Fernández-Álvarez.

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The authors declare that they have no conflict of interest.

Ethical standards

Laboratory protocols and experimental conditions were in line with current international standards for cephalopod care and welfare reviewed by Fiorito et al. (2015).

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Fernández-Álvarez, F.Á., Villanueva, R., Hoving, H.T. et al. The journey of squid sperm. Rev Fish Biol Fisheries 28, 191–199 (2018). https://doi.org/10.1007/s11160-017-9498-6

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Keywords

  • Dosidicus gigas
  • Reproduction
  • Sexual selection
  • Sperm storage organs
  • Spermatangium
  • Squid