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Comparison of embryonic and adult shells of Sepia officinalis (Cephalopoda, Mollusca)

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Abstract

Development and evolution of the shell in cephalopods is difficult to establish as there is few species with a calcified shell that could be fossilized (stable in geological time). Internal cuttlebone of sepiids is so particular that homologies are difficult to find. The developmental sequence in embryos give some response elements by comparison with adult cuttlebone. The macro and microstructure of adult shell is well known but an approach at nanostructural level allows to determine structure and composition of the two main parts, the dorsal shield and chambered part. We evidence in the embryonic shell, mainly organic, a light calcification of the shell, which occurs directly as aragonite, as it is all along the formation of the shell and whatever the parts. In embryonic shell, the prismatic and/or lamellar layers, present in adult, are not differentiated and the dorsal shield grows progressively, from posterior to anterior. Despite microstructural differences, all layers of both chambered part and dorsal shield are composed of rounded nanogranules (between 50 and 100 nm), similar to what is found in other mollusc shells. Finally, the presence of pillars evidenced in embryo suggests either that their absence in extinct lineages of sepiids is the result of a diagenetic process or that they are a novelty in present sepiid species.

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Acknowledgements

This work was financially supported by the ATM "Interactions Minéral-Vivant" funding of the Muséum national d'Histoire naturelle (SEPIOM project). The authors thank all the members of the Max Planck Institute for Interfaces and Colloids (Golm, Germany) for their help. We thank C. Jozet-Alves and the CREC (University of Caen) for providing eggs of Sepia officinalis. LBP thanks G. Patriache and L. Largeau (CNRS-LPN) for the first tests on mineral composition of embryonic shell several years ago.

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Authors and Affiliations

  1. Institut de Systématique, Evolution, Biodiversité, UMR 7205 CNRS, Sorbonne Université, EPHE, Muséum National D’Histoire Naturelle, Paris, France

    Yannicke Dauphin

  2. Department of Biomaterials, Max-Planck-Institute of Colloids and Interfaces, Potsdam, Germany

    Yannicke Dauphin

  3. Biologie Des Organismes Et Ecosystèmes Aquatiques, UMR CNRS 7208, Sorbonne Université, IRD 207, UCN, UA, Muséum National d’Histoire Naturelle, Paris, France

    Gilles Luquet & Laure Bonnaud-Ponticelli

  4. De la Molécule Aux Nano-Objets: Réactivité, Interactions et Spectroscopies, UMR 8233 CNRS, Sorbonne Université, Paris, France

    Aline Percot

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Terminology used for the orientation of the fractures and polished sections studied using SEM and AFM (TIF 11378 kb)

435_2020_477_MOESM2_ESM.tif

Variations in morphology and structure of the chambered zone of adult and embryonic shells. A Enlargement of the basal part of a pillar of an adult shell; fracture fixed and etched (chromium sulphate pH 3.5 for 4 h.); SE - SEM. B Pillars are covered by an organic membrane (upper part); under the membrane, the granular structure of the pillar is visible; adult sample. SE - SEM. C Etched fracture trough a pillar of an adult shell showing the empty middle part (NaOH 0.5M for 4h at 100°C, pronase pH 7.6 for 6 h at 34°C, chitinase pH 5.6 for 22 h at 24°C); SE - SEM. D Etched vertical section through the pillar of an adult shell showing the different behaviour of the middle and external parts (NaOH 1 M for 4h 30 at 100°C, then 4 days at 20°C, lipase 1 mg/ml pH 9 for 28 h at 35°C); SE - SEM. E Pillars in the first septa of an adult shell. SE - SEM. F Unetched granular surface of the lateral growing edge of a larval shell; BSE - SEM. G Unetched tangential fracture showing the zig zag “wall” made by coalescent pillars in an adult shell. H-I Stage 25/26 embryonic shell after 24h in vitro incubation of the embryo in a calcein-containing sea water (30 mg/L; CNAM, Sigma) followed by 48h incubation in sea water, H Optical image, I Fluorescence image showing that calcification occurs during the growth at the distal extremities of the pillars (TIF 11950 kb)

435_2020_477_MOESM3_ESM.tif

FTIR spectra of the soluble and insoluble organic matrices extracted from the dorsal shield and ventral zone of an adult shell, showing the similarity between the insoluble matrix and the crab chitin. The dorsal shield and the ventral zone were mechanically separated in adult samples, immersed in 3% NaClO for 1 h to remove organic contaminants, rinsed with Milli-Q water, dried, and ground into powder by grinding with an electric mortar for 10 min to obtain homogeneous granulometry. Powdered samples were immersed in Milli-Q water and decalcified by progressive addition of 50% acetic acid so that the pH (automatically controlled with a titrimeter) is above 4. The entire extract was centrifuged at 21,000 g for 15 min, which separated the supernatant (soluble) and precipitated (insoluble) fractions. The soluble fraction was desalted by exchange with Milli-Q water on a Microconcentrator (Filtron) using a 3-kDa cut-off membrane and lyophilized. Powdered samples and KBr were oven-dried at 38°C overnight. Then, they were mixed (about 5% powdered samples in KBr) and loaded into the sample cup (TIF 7340 kb)

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Dauphin, Y., Luquet, G., Percot, A. et al. Comparison of embryonic and adult shells of Sepia officinalis (Cephalopoda, Mollusca). Zoomorphology 139, 151–169 (2020). https://doi.org/10.1007/s00435-020-00477-2

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