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Complex genetic structure of a euryhaline marine fish in temporarily open/closed estuaries from the wider Gulf of Aden

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Abstract

Temporarily open/closed estuaries (TOCEs) are major ecosystems of the Indian Ocean coastal zones. Their functioning is tightly linked to climatic events such as monsoons and storms, and their mouth can close up for prolonged and variable periods of time, thus limiting their connectivity with the marine environment. Two types of genetic markers (i.e., mitochondrial cytochrome c oxidase I (COI) gene and microsatellites) were used to assess the genetic structure of 288 individuals of Terapon jarbua, a widely distributed fish species in the wider Gulf of Aden. Firstly, the hypothesis of panmixia was tested. Then, alternative hypotheses were investigated to explain the population genetic structure of T. jarbua: could it be shaped by (1) regional biogeographic barriers (i.e., Socotra Island vs. mainland Yemen) and/or (2) the particular functioning of TOCEs in relation to the species life cycle and particular physical ocean parameters? On one hand, the polymorphism of the COI inferred (1) a high haplotype diversity and a reduced nucleotide diversity over the whole data set and (2) a “star-like” shape of the haplotype network, thus suggesting a population expansion after local extinctions during the Pleistocene glaciations. On a second hand, the genotyping of eight microsatellites showed a significant genetic differentiation between T. jarbua populations in the wider Gulf of Aden (F ST = 0.035, p < 0.01), and thus, the panmixia hypothesis was rejected. Analyses of molecular variance results did not show any significant structure between Socotra Island and mainland Yemen and thus did not support the role of biogeographic barriers in structuring T. jarbua populations. Significant multi-locus deficits in heterozygotes at particular locations displaying high levels of F IS were recorded. It was suggested that a possible Wahlund effect took place in those TOCEs which could gather several cohorts of larvae stemming from different marine subpopulations over the sampled area. The present study emphasized the uniqueness of each TOCE as a potential reservoir of biodiversity and the urgent need for a better conservation program of those estuaries in the region, in order to avoid habitat fragmentation and permanent closure of those nursery areas by human activities.

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Acknowledgments

The present study was mainly funded by the Total Foundation, Paris. It was partially conducted at the Socotra Field Research Station of the Biodiversity and Climate Research Centre (BiK-F), Frankfurt a.M., based on financial support of the research-funding program “LOEWE—Landes-Offensive zur Entwicklung Wissenschaftlich-ökonomischer Exzellenz” of Hesse’s Ministry of Higher Education, Research and the Arts. Additional mobility funds were provided by scholarships from the GRADE—Goethe Graduate Academy of the Goethe University Frankfurt a.M. and the International Doctoral College of the European University of Brittany (UEB). His Excellency Eng. Abdul‐Rahman F. Al‐Eryani, former Minister of Water and Environment of the Republic of Yemen, and H. E. Eng. Mahmoud Shidiwa, Chairman of the Environment Protection Authority, are cordially acknowledged for their continued support and for granting research and sample export permits. The Socotra Conservation and Development Program (SCDP-UNDP) is thanked for providing indispensable support during the field work. We would like to thank the People of Socotra and Hadhramout, particularly the members of the coastal communities which kindly facilitated field work and provided access to the areas in their care. We wish to express our gratitude to Fouad Naseeb and Motea Sheikh Aideed for their efficient assistance in the field, to Mohamed Saeed El-Mashjary and Atta Allha Mohesen Ali of the Hadhramout University for granting the first author access to the University wet laboratory. Friedhelm Krupp, Louis Quiniou and Eric Morize are cordially acknowledged for their support of the first author’s Ph.D. project.

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Authors and Affiliations

  1. Sektion Ichthyologie, Senckenberg Forschungsinstitut und Naturmuseum, Senckenberganlage 25, 60325, Frankfurt am Main, Germany

    Edouard Lavergne & Uwe Zajonz

  2. Biodiversität und Klima Forschungszentrum (BiK-F), Senckenberganlage 25, 60325, Frankfurt am Main, Germany

    Edouard Lavergne & Uwe Zajonz

  3. Laboratoire des Sciences de l’Environnement Marin LEMAR, UMR 6539, CNRS/IRD/UBO/IFREMER, Institut Universitaire Européen de la Mer IUEM, Université de Bretagne Occidentale, Rue Dumont d’Urville, 29280, Plouzané, France

    Edouard Lavergne, Isabelle Calvès, Grégory Charrier & Jean Laroche

  4. Centre de Formation et de Recherche sur l’Environnement Méditerranéen (CEFREM), UMR 5110, CNRS/UPVD, Université de Perpignan, 52, Avenue Paul Alduy, 66860, Perpignan Cedex, France

    Anne Leila Meistertzheim

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  1. Edouard Lavergne
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  2. Isabelle Calvès
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  3. Anne Leila Meistertzheim
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  4. Grégory Charrier
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  5. Uwe Zajonz
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  6. Jean Laroche
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Correspondence to Edouard Lavergne.

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Communicated by M. I. Taylor.

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Lavergne, E., Calvès, I., Meistertzheim, A.L. et al. Complex genetic structure of a euryhaline marine fish in temporarily open/closed estuaries from the wider Gulf of Aden. Mar Biol 161, 1113–1126 (2014). https://doi.org/10.1007/s00227-014-2404-z

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