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Settled, symbiotic, then sexually mature: adaptive developmental anatomy in the deep-sea, chemosymbiotic mussel Idas modiolaeformis

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Abstract

The Bathymodiolinae are pervasive in reducing environments in the deep sea, yet data on post-larval and juvenile development and on the process of symbiont acquisition remain elusive. To understand how these opportunistic metazoans survive in ephemeral reducing habitats, individuals of the small bathymodiolin, Idas modiolaeformis, were examined histologically to trace their reproductive development, and with fluorescence and transmission electron microscopy to identify patterns of infection by their environmentally acquired bacterial symbionts. A size series of these mussels was retrieved from larval colonisation devices containing vegetative substrates, deployed for 51 weeks (November 2006–2007) in the central ‘Pockmarks’ region (site 2A) of the Nile deep-sea fan in the eastern Mediterranean (NDSF), a zone where methane seepage can occur (N 32° 31.97, E 30° 21.18, 1,693 m deep). Developmental patterns of germ cell migration, size at first maturity, and symbiont acquisition and localisation are presented for the post-larva to adult transition. The smallest mature adult was a male with shell length (SL) 2.35 mm. All larger individuals in the series were male (maximum SL 6.54 mm). Based on the absence of bacterial signals, plantigrades were asymbiotic, indicating strict heterotrophy in larvae and early post-larvae. During the early stages of dissoconch deposition, extracellular symbiont infection was non-specific. This was followed by increasing specificity on non-ciliated gill epithelia in adults. These observations on early development in I. modiolaeformis represent evolutionary adaptations to their ephemeral, reducing habitats.

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Acknowledgments

We thank Antje Boetius and Catherine Pierre for samples collected during the BIONIL (M70/2b) and MEDECO cruises with RVs Meteor and RV Pourquoi Pas? funded by the ESF EUROCORES projects: CHEMECO and EuroDEEP and by the European Commission: EU HERMES and DIWOOD programs. Additional funding and logistics were met by IFREMER, CNRS and the Max-Planck-Institut für Mikrobiologie. We thank the captains and crews of RVs Meteor and RVs Pourquoi Pas? and those teams operating Quest 4000 (MARUM, Bremen, Germany) and ROVs Victor 6000 (Ifremer, France). At UPMC, our thanks go to Ghislaine Frébourg and Géraldine Toutirais (IFR 83) for assistance with TEM analysis. This work was co-funded by UPMC, HERMIONE EC (FP7/2007-2013-n° 226354) and a MARES grant. MARES is a Joint Doctorate Programme selected under Erasmus Mundus coordinated by Ghent University (FPA 2011-0016). See www.mares-eu.org for extra information. Our thanks go to the Editor and two anonymous reviewers whose comments greatly improved the manuscript.

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  1. UMR7208 Laboratoire biologie des organismes et écosystèmes aquatiques (UPMC CNRS MNHM IRD CAEN), Sorbonne Universités, UPMC Université Paris 06, 7 quai St. Bernard, 75005, Paris, France

    Sven R. Laming, Sébastien Duperron & Sylvie M. Gaudron

  2. Departamento de Biologia and CESAM, Universidade de Aveiro, Campus Universitario de Santiago, 3810-193, Aveiro, Portugal

    Sven R. Laming & Marina R. Cunha

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Laming, S.R., Duperron, S., Cunha, M.R. et al. Settled, symbiotic, then sexually mature: adaptive developmental anatomy in the deep-sea, chemosymbiotic mussel Idas modiolaeformis . Mar Biol 161, 1319–1333 (2014). https://doi.org/10.1007/s00227-014-2421-y

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