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Two enigmas may solve each other: the oocyte coat and atresia in the common cockle, Cerastoderma edule (Linnaeus, 1758)

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Abstract

Two co-occurring, enigmatic aspects of bivalve reproduction were investigated in the common cockle Cerastoderma edule: the oocyte coat and oocyte atresia. Qualitative histology and transmission electron microscopy (TEM) of cockles collected on the French Atlantic coast revealed not only the fine structure of the oocyte coat, but also confirmed that it is secreted by the oocyte itself and composed of acid mucopolysaccharides (AMPS), known to be viscous and adhesive. Quantitative histology showed that at the peak of oogenesis, oocyte coats occupy the largest fraction (approx. 40%) of the gonad acinal volume, representing both a significant sacrifice of female gamete capacity, and a non-gamete energetic investment. Potential benefits of the coat include protection from mechanical abrasion, predation, and opportunistic microbes. Atresia (oocyte degeneration) was a known second source of reduced fecundity, with a minimum impact of approximately 50% of the total oocyte volume. It is suggested that this high proportion of atresic oocytes is related to the previously-documented genetic inviability of early post-fertilization life stages. The qualitative histological and TEM observations revealed atresic debris adhering to the exterior surface of the oocyte coats. Such an arrangement would isolate adjacent oocyte coats, enabling the oocytes to be spawned individually, rather than as an egg mass, and therefore to undergo planktonic development and dispersion. Oocyte atresia and the oocyte coat of Cerastoderma edule therefore appear to be linked in the first indication of an adaptive function in bivalves.

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Data availability

The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.

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Acknowledgements

We are grateful to Bruno Chollet (IFREMER La Tremblade) for his advice and assistance with electron microscopy processing, as well as Philippe Elies from the Plateforme d’Imagerie et de Mesures en Microscopie (UBO). We thank Thibault Besle and Stacy-Ann Gray for their help with sampling and staining; Lucie Kessler, Mathilde Clairambault and Stacy-Ann Gray for their patience and perseverance in the laboratory spawning trials. We are indebted to David Berteau and employees of Chellet-Berteau Production for their warm welcome and permission to sample on-site.

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  1. Laboratoire de Biologie Marine, Faculté des Sciences, Université de Nantes, 2 rue de la Houssinière, 44322, Nantes, France

    Daphné Chérel & Peter G. Beninger

  2. Laboratoire de Biotechnologie et Chimie Marines, Université Bretagne Sud, Rue Saint Maudé, 56321, Lorient, France

    Gaël Le Pennec

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  1. Daphné Chérel
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Correspondence to Peter G. Beninger.

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Supplementary file1 Cerastoderma edule veliger inside oocyte coat; note resistance of outer reaches to mechanical stress. (AVI 6000 kb)

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Chérel, D., Beninger, P.G. & Le Pennec, G. Two enigmas may solve each other: the oocyte coat and atresia in the common cockle, Cerastoderma edule (Linnaeus, 1758). Mar Biol 167, 104 (2020). https://doi.org/10.1007/s00227-020-03718-6

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