Skip to main content
SpringerLink
Log in

Historical biogeography and mitogenomics of two endemic Mediterranean gorgonians (Holaxonia, Plexauridae)

  • Original Article
  • Published:
Organisms Diversity & Evolution Aims and scope Submit manuscript

Abstract

Among the Mediterranean plexaurids, four species are endemic and despite their ecological importance, comprehensive studies on the evolution and biogeography of these organisms are lacking. Here, we explore the mitogenomic variability of two endemic, ecologically important Mediterranean Paramuricea species. We assess their phylogenetic relationships and provide first insights into their evolution and biogeography. Complete mitogenome sequences of Paramuricea clavata and Paramuricea macrospina were obtained using long-range PCR, primer-walking and Sanger sequencing. For an enlarged sample of Paramuricea species, maximum likelihood and Bayesian phylogenetic trees of the mitochondrial gene mtMutS were obtained and used to study the biogeographic history of Paramuricea through a statistical Dispersal-Vicariance (S-DIVA) method and a Dispersal Extinction Cladogenesis (DEC) model. Divergence time was estimated under strict and relaxed molecular clock models in BEAST using published octocoral mutation rates. Our results revealed high nucleotide diversity (2.6%) among the two Mediterranean endemics; the highest mutation rates were found in the mtMutS, Nad4 and Nad5. In addition, we found length polymorphisms in several intergenic regions and differences in mitochondrial genome size. The red gorgonian P. clavata was closely related to the Eastern Atlantic Paramuricea grayi rather than its Mediterranean congener, P. macrospina. Our biogeographic results provide evidence for the independent speciation of the Mediterranean species and point to a Miocene origin of the two endemics, highlighting the role played by the Messinian Salinity Crisis in the evolutionary history of Mediterranean organisms.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Alderslade, P., Althaus, F., Mcennulty, F., Gowlett-Holmes, K., & Williams, A. (2014). Australia’s deep-water octocoral fauna: historical account and checklist, distributions and regional affinities of recent collections. Zootaxa, 3796, 435–452.

    Article  Google Scholar 

  • Aljanabi, S. M., & Martinez, I. (1997). Universal and rapid salt-extraction of high quality genomic DNA for PCR-based techniques. Nucleic Acids Research, 25, 4692–4693.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Agell, G., Rius, M., & Pascual, M. (2009). Isolation and characterization of eight olymorphic microsatellite loci for the Mediterranean gorgonian Paramuricea clavata. Conservation Genetics, 10, 2025–2027.

    Article  CAS  Google Scholar 

  • Angeletti, L., Taviani, M., Canese, S., Foglini, F., Mastrototaro, F., Argnani, A., Trincardi, F., Bakran-Petricioli, T., Ceregato, A., Chimienti, G., Macić, V., & Poliseno, A. (2014). New deep-water cnidarian sites in the southern Adriatic Sea. Mediterranean Marine Science, 15, 263–273.

    Article  Google Scholar 

  • Bas, C. (2009). The Mediterranean: a synoptic overview. Contributions to Science, 5, 25–39.

    Google Scholar 

  • Bayer, F. M. (1956). Octocorallia. In R. C. Moore (Ed.), Treatise of invertebrate paleontology, part F Coelenterata (pp. 167–231). Kansas: Geological Society of America and University of Kansas Press.

    Google Scholar 

  • Bayer, F. M. (1961). The shallow-water Octocorallia of the West Indian region. A manual for marine biologists. Studies of the Fauna of Curaçao and other Caribbean Islands, 12, 1–373.

  • Bianchi, C., & Morri, C. (2000). Marine biodiversity of the Mediterranean Sea: situation, problems and prospects for future research. Marine Pollution Bulletin, 40, 367–376.

    Article  CAS  Google Scholar 

  • Bo, M., Canese, S., Spaggiari, C., Pusceddu, A., Bertolino, M., Angiolillo, M., Giusti, M., Loreto, M. F., Salvati, E., Greco, S., & Bavestrello, G. (2012). Deep coral oases in the South Tyrrhenian Sea. PloS One, 7(11), e49870. doi:10.1371/journal.pone.0049870.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bouckaert, R. (2010). DensiTree: making sense of sets of phylogenetic trees. Bioinformatics, 26, 1372–1373.

    Article  CAS  PubMed  Google Scholar 

  • Bouckaert, R., Heled, J., Kühnert, D., Vaughan, T., Wu, C. H., Xie, D., Suchard, M. A., Rambaut, A., & Drummond, A. J. (2014). BEAST 2: a software platform for Bayesian evolutionary analysis. PLoS Computational Biology, 10(4), e1003537. doi:10.1371/journal.pcbi.1003537.

    Article  PubMed  PubMed Central  Google Scholar 

  • Boudouresque, C. F. (2004). Marine biodiversity in the Mediterranean: status of species, populations and communities. Scientific Report of Port-Cros National Park, 20, 97–146.

    Google Scholar 

  • Boury-Esnault, N., Pasini, M., & Uriz, M. J. (1992). A new Discorhabdella (Porifera, Demospongiae), a new Tethyan relict of pre-Messinian biota? Journal of Natural History, 26, 1–7.

  • Brockman, S. A., & McFadden, C. S. (2012). The mitochondrial genome of Paraminabea aldersladei (Cnidaria: Anthozoa: Octocorallia) supports intramolecular recombination as the primary mechanism of gene rearrangement in octocoral mitochondrial genomes. Genome Biology and Evolution, 4, 994–1006.

    Article  PubMed  Google Scholar 

  • Carpine, C., & Grasshoff, M. (1975). Les Gorgonaires de la Méditerranée. Bulletin de l’Institut Océanographique de Monaco, 71, 1–140.

    Google Scholar 

  • Carreras-Carbonell, J., Macpherson, E., & Pascual, M. (2005). Rapid radiation and cryptic speciation in Mediterranean triplefin blennies (Pisces: Tripterygiidae) combining multiple genes. Molecular Phylogentics and Evolution, 37, 751–761.

    Article  CAS  Google Scholar 

  • Coll, M., Piroddi, C., Steenbeek, J., Kaschner, K., Ben Rais Lasram, F., Aguzzi, J., Ballesteros, E., Nike Bianchi, C., Corbera, J., Dailianis, T., Danovaro, R., Estrada, M., Froglia, C., Galil, B. S., Gasol, J. M., Gertwagen, R., Gil, J., Guilhaumon, F., Kesner-Reyes, K., Kitsos, M. S., Koukouras, A., Lampadariou, N., Laxamana, E., López-Fé de la Cuadra, C. M., Lotze, H. K., Martin, D., Mouillot, D., Oro, D., Raicevich, S., Rius-Barile, J., Saiz-Salina, J. I., San Vicente, S., Somot, S., Templado, J., Turon, X., Vafidis, D., Villanueva, R., & Voultsiadou, E. (2010). The biodiversity of the Mediterranean Sea: estimates, patterns, and threats. PloS One, 5(8), e11842. doi:10.1371/journal.pone.0011842.

    Article  PubMed  PubMed Central  Google Scholar 

  • Costantini, F., Carlesi, L., & Abbiati, M. (2013). Quantifying spatial genetic structuring in mesophotic populations of the precious coral Corallium rubrum. PloS One, 8(4), e61546. doi:10.1371/journal.pone.0061546.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Danovaro, R., Dinet, A., Duinevel, G., & Tselepides, A. (1999). Benthic response to particulate fluxes in different trophic environments: a comparison between the Gulf of Lions–Catalan Sea (western-Mediterranean) and the Cretan Sea (eastern-Mediterranean). Progress in Oceanography, 44, 287–312.

    Article  Google Scholar 

  • Darriba, D., Taboada, G. L., Doallo, R., & Posada, D. (2012). jModelTest 2: more models, new heuristics and parallel computing. Nature Methods, 9, 772.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Doughty, C., Quattrini, A. M., & Cordes, E. E. (2014). Insights into the population dynamics of the deep-sea coral genus Paramuricea in the Gulf of Mexico. Deep Sea Research Part II: Topical Studies in Oceanography, 99, 71–82.

    Article  Google Scholar 

  • Domingues, V. S., Bucciarelli, G., Almada, V. C., & Bernardi, G. (2005). Historical colonization and demography of the Mediterranean damselfish, Chromis chromis. Molecular Ecology, 14, 4051–4063.

    Article  PubMed  Google Scholar 

  • Dov Por, F. (2009). Tethys returns to the Mediterranean: success and limits of tropical re-colonization. BioRisk, 3, 5–19.

    Article  Google Scholar 

  • Doyle, J. J., & Doyle, J. L. A. (1987). Rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochemical Bulletin, 19, 11–15.

    Google Scholar 

  • Edgar, R. C. (2004). MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research, 32, 1792–1797.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Erpenbeck, D., Voigt, O., Wörheide, G., & Lavrov, D. V. (2009). The mitochondrial genomes of sponges provide evidence for multiple invasions by repetitive hairpin-forming elements (RHE). BMC Genomics, 10, 591. doi:10.1186/1471-2164-10-591.

    Article  PubMed  PubMed Central  Google Scholar 

  • France, S. C., & Hoover, L. L. (2002). DNA sequences of the mitochondrial COI gene have low levels of divergence among deep-sea octocorals (Cnidaria: Anthozoa). Hydrobiologia, 471, 149–155.

    Article  Google Scholar 

  • Garcia-Castellanos, D., Estrada, F., Jiménez-Munt, I., Gorini, C., Fernàndez, M., Vergés, J., & De Vicente, R. (2009). Catastrophic flood of the Mediterranean after the Messinian salinity crisis. Nature, 10, 778–781.

    Article  Google Scholar 

  • Gouy, M., Guindon, S., & Gascuel, O. (2010). SeaView version 4: a multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Molecular Biology and Evolution, 27, 221–224.

    Article  CAS  PubMed  Google Scholar 

  • Grasshoff, M. (1977). Die Gorgonarien des östlichen Nordatlantik und des Mittelmeeres. III Die Familie Paramuriceidae (Cnidaria, Anthozoa). Meteor Forschungsergebnisse, 27, 5–76.

    Google Scholar 

  • Grasshoff, M. (1992). Die Flachwasser-Gorgonarien von Europa und Westafrika (Cnidaria, Anthozoa). Courier Forschungsinsitut Senckenberg, 149, 1–135.

    Google Scholar 

  • Hsü, K. J., Ryan, W. B. F., & Cita, M. B. (1973). Late Miocene dessication of the Mediterranean. Nature, 242, 240–244.

    Article  Google Scholar 

  • Kearse, M., Moir, R., Wilson, A., Stones-Havas, S., Cheung, M., Sturrock, S., Buxton, S., Cooper, A., Markowitz, S., Duran, C., Thierer, T., Ashton, B., Mentjies, P., & Drummond, A. (2012). Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics, 28, 1647–1649.

    Article  PubMed  PubMed Central  Google Scholar 

  • Lavrov, D. V. (2010). Rapid proliferation of repetitive palindromic elements in mtDNA of the endemic Baikalian sponge Lubomirskia baicalensis. Molecular Biology and Evolution, 27, 757–760.

    Article  CAS  PubMed  Google Scholar 

  • Lepard, A. (2003). Analysis of variation in the mitochondrial encoded msh1 in the genus Leptogorgia (Cnidaria: Octocorallia) and implications for population and systematic studies. MS thesis, University of Charleston, Charleston, SC.

  • Lessios, H. A., & Robertson, D. R. (2006). Crossing the impassable: genetic connections in 20 reef fishes across the Eastern Pacific Barrier. Proceedings of the Royal Society B, 273, 2201–2208.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Librado, P., & Rozas, J. (2009). DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics, 25, 1451–1452.

    Article  CAS  PubMed  Google Scholar 

  • McFadden, C. S., & Hutchinson, M. B. (2004). Molecular evidence for the hybrid origin of species in the soft coral genus Alcyonium (Cnidaria: Anthozoa: Octocorallia). Molecular Ecology, 13, 1495–1505.

    Article  CAS  PubMed  Google Scholar 

  • McFadden, C. S., France, S. C., Sanchez, J. A., & Alderslade, P. (2006). A molecular phylogenetic analysis of the Octocorallia (Cnidaria: Anthozoa) based on mitochondrial protein coding sequences. Molecular Phylogenetics and Evolution, 41, 513–527.

    Article  CAS  PubMed  Google Scholar 

  • McFadden, C. S., Benayahu, Y., Pante, E., Thoma, J. N., Nevarez, P. A., & France, S. C. (2011). Limitations of mitochondrial gene barcoding in Octocorallia. Molecular Ecology Resources, 11, 19–31.

    Article  CAS  PubMed  Google Scholar 

  • Mokhtar-Jamaï, K., Pascual, M., Ledoux, J. B., Coma, R., Féral, J. P., Garrabou, J., & Aurelle, D. (2011). From global to local genetic structuring in the red gorgonian Paramuricea clavata: the interplay between oceanographic conditions and limited larval dispersal. Molecualar ecology, 20, 3291–3305.

    Article  Google Scholar 

  • Pante, E., Abdelkrim, J., Viricel, A., Gey, D., France, S. C., Boisselier, M. C., & Samadi, S. (2015). Use of RAD sequencing for delimiting species. Heredity, 114, 450–459.

    Article  CAS  PubMed  Google Scholar 

  • Park, E., Song, J. I., & Won, Y. J. (2011). The complete mitochondrial genome of Calicogorgia granulosa (Anthozoa: Octocorallia): potential gene novelty in unidentified ORFs formed by repeat expansion and segmental duplication. Gene, 486, 81–87.

    Article  CAS  PubMed  Google Scholar 

  • Pérès, J. M. (1985). History of the Mediterranean biota and the colonization of the depth. In R. Margalef (Ed.), Western Mediterranean (pp. 200–234). London: Pergamon Press.

    Google Scholar 

  • Pérès, J. M., & Picard, J. (1964). Nouveau manuel de bionomie benthique de la mer Méditerranée. Recueil des Travaux de la Station Marine d’Endoume, 31, 1–137.

    Google Scholar 

  • Pinardi, N., Arneri, E., Crise, A., Ravaioli, M., & Zavatarelli, M. (2006). The physical, sedimentary and ecological structure and variability of shelf areas in the Mediterranean Sea. In A. R. Robinson & K. Brink (Eds.), The sea (pp. 1243–1330). Cambridge: Harvard University Press.

    Google Scholar 

  • Pratlong, M., Haguenauer, A., Chabrol, O., Klopp, C., Pontarotti, P., & Aurelle, D. (2015). The red coral (Corallium rubrum) transcriptome: a new resource for population genetics and local adaptation studies. Molecular Ecology Resources, 15, 1205–1215.

    Article  CAS  PubMed  Google Scholar 

  • Rambaut, A., Drummond, A. J. (2009). Tracer—MCMC trace analysis tool. Ver. 1. 5. Edinburgh: University of Edinburgh.

  • Ree, R. H., & Smith, S. A. (2008). Maximum likelihood inference of geographic range evolution by dispersal, local extinction, and cladogenesis. Systematic Biology, 57(1), 4–14.

    Article  PubMed  Google Scholar 

  • Ronquist, F. (1997). Dispersal-vicariance analysis: a new approach to the quantification of historical biogeography. Systematic Biology, 46, 195–203.

    Article  Google Scholar 

  • Ronquist, F. (2001). DIVA—computer program for MacOS and Win32. Ver 1. 2. Uppsala: Evolutionary Biology Centre, Uppsala University.

  • Sánchez, J. A., McFadden, C. S., France, S. C., & Lasker, H. R. (2003). Molecular phylogenetic analyses of shallow-water Caribbean octocorals. Marine Biology, 142, 975–987.

    Article  Google Scholar 

  • Sanna, D., Cossu, P., Dedola, G. L., Scarpa, F., Maltagliati, F., Castelli, A., Franzoi, P., Lai, T., Cristo, B., Curini-Galletti, M., Francalacci, P., & Casu, M. (2013). Mitochondrial DNA reveals genetic structuring of Pinna nobilis across the Mediterranean Sea. PloS One, 8(6), e67372. doi:10.1371/journal.pone.0067372.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sarà, M. (1985). Ecological factors and their biogeographic consequences in the Mediterranean ecosystems. In M. M. Apostolopoulou & V. Kiortsis (Eds.), Mediterranean marine ecosystems NATO conference series (pp. 1–18). London: Plenum Press.

    Chapter  Google Scholar 

  • Stamatakis, A. (2006). RAxML-VI-HPC: maximum likelihood based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics, 22, 2688–2690.

    Article  CAS  PubMed  Google Scholar 

  • Stamatakis, A., Hoover, P., & Rougemont, J. (2008). A rapid bootstrap algorithm for the RAxML Web servers. Systematic Biology, 57, 758–771.

    Article  PubMed  Google Scholar 

  • Tanhua, T., Hainbucher, D., Schroeder, K., Cardin, V., Alvarez, M., & Civitarese, G. (2013). The Mediterranean Sea system: a review and an introduction to the special issue. Ocean Science, 9, 789–803.

    Article  Google Scholar 

  • Thoma, J. N., Pante, E. G., Brugler, M. R., & France, S. C. (2009). Deep-sea octocorals and antipatharians show no evidence of seamount-scale endemism in the NW Atlantic. Marine Ecology Progress Series, 397, 25–35.

    Article  CAS  Google Scholar 

  • Topçu, E. N., & Öztürk, B. (2015). Composition and abundance of octocorals in the sea of Marmara, where the Mediterranean meets the Black Sea. Scientia Marina, 79, 125–135.

    Article  Google Scholar 

  • Tougard, C., Folly, J., & Berrebi, P. (2014). New light on the evolutionary history of the common goby (Pomatoschistus microps) with an emphasis on colonization processes in the Mediterranean Sea. PloS One, 9(3), e91576. doi:10.1371/journal.pone.0091576.

    Article  PubMed  PubMed Central  Google Scholar 

  • Vafidis, D. (2010) Checklist of class Anthozoa (Phylum Cnidaria). In Coll, M., et al. (2010). The biodiversity of the Mediterranean Sea: estimates, patterns, and threats. PLoS ONE, 5(8), e11842. doi:10.1371/journal.pone.0011842.

  • Vargas, S., Eitel, M., Breedy, O., & Schierwater, B. (2010). Molecules match morphology: mitochondrial DNA supports Bayer’s Lytreia–Bebryce–Heterogorgia (Alcyonacea: Octocorallia) clade hypothesis. Invertebrate Systematics, 24, 23–31.

    Article  Google Scholar 

  • Vargas, S., Guzman, H. M., Breedy, O., & Wörheide, G. (2014). Molecular phylogeny and DNA barcoding of tropical eastern Pacific shallow-water gorgonian octocorals. Marine Biology, 161, 1027–1038.

    Article  Google Scholar 

  • Vertino, A., Stolarski, J., Bosellini, F. R., & Taviani, M. (2014). Mediterranean corals through time: from Miocene to present. In S. Goffredo & Z. Dubinsky (Eds.), The Mediterranean Sea: its history and present challenges (pp. 257–274). Dordrecht: Springer.

    Chapter  Google Scholar 

  • Williams, G. C., & Chen, J. (2014). Illustrated key to the shallow-water gorgonians and pennatulaceans of the Verde Island Passage, northern Philippines, including synopses of the taxa and a glossary of terms (Cnidaria: Anthozoa: Octocorallia). In G. C. Williams & T. M. Gosliner (Eds.), The coral triangle—the Hearst Philippine Biodiversity Expedition 2011 (pp. 67–128). San Francisco: California Academy of Sciences.

    Google Scholar 

  • Wirshing, H. H., Messing, C. G., Douady, C. J., Reed, J., Stanhope, M. J., & Shivji, M. S. (2005). Molecular evidence for multiple lineages in the gorgonian family Plexauridae (Anthozoa: Octocorallia). Marine Biology, 147, 497–508.

    Article  CAS  Google Scholar 

  • Wirshing, H. H., & Baker, A. C. (2015). Molecular and morphological species boundaries in the gorgonian octocoral genus Pterogorgia (Octocorallia: Gorgoniidae). PloS One, 10(7), e0133517. doi:10.1371/journal.pone.0133517.

    Article  PubMed  PubMed Central  Google Scholar 

  • Yan, Y., Harris, A. J., & Xingjin, H. (2010). S-DIVA (Statistical Dispersal-Vicariance Analysis): a tool for inferring biogeographic histories. Molecular Phylogenetics and Evolution, 56, 848–850.

    Article  Google Scholar 

  • Yu, Y., Harris, A.J., He, X.J. (2014) RASP (Reconstruct Ancestral State in Phylogenies). Ver. 3. 0. Available at http://mnh.scu.edu.cn/soft/blog/RASP.

Download references

Acknowledgements

We thank Andromede Océanologie and Thibault Rauby for help with sampling and to José Aldrey and Marie-Noëlle de Casamajor for sending part of the samples. We would also like to thank an anonymous reviewer for the insightful comments on the paper. This study was possible thanks to the generous support of the LMU München Junior Research Funds to SV through the German Excellence Initiative. SV is indebted to N. Villalobos, M. Vargas, S. Vargas and S. Vargas for their constant support during the realization of this study.

Author information

Authors and Affiliations

  1. Department of Earth and Environmental Sciences, Palaeontology and Geobiology, Ludwig-Maximilians-Universität München, Richard-Wagner-Straße 10, 80333, Munich, Germany

    Angelo Poliseno, Gert Wörheide & Sergio Vargas

  2. INSUB, Zemoria 12, 20013, San Sebastián, Spain

    Alvaro Altuna

  3. Department of Life and Environmental Sciences (DiSVA), Marche Polytechnic University, Via Brecce Bianche, 60131, Ancona, Italy

    Carlo Cerrano

  4. GeoBio-Center, Ludwig-Maximilians-Universität München, Richard-Wagner-Straße 10, 80333, Munich, Germany

    Gert Wörheide

  5. Bayerische Staatssammlung für Paläontologie und Geologie, Richard-Wagner-Straße 10, 80333, Munich, Germany

    Gert Wörheide

Authors
  1. Angelo Poliseno
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Alvaro Altuna
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Carlo Cerrano
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Gert Wörheide
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Sergio Vargas
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Sergio Vargas.

Electronic supplementary material

ESM 1

(PDF 898 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Poliseno, A., Altuna, A., Cerrano, C. et al. Historical biogeography and mitogenomics of two endemic Mediterranean gorgonians (Holaxonia, Plexauridae). Org Divers Evol 17, 365–373 (2017). https://doi.org/10.1007/s13127-017-0322-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13127-017-0322-x

Keywords

Search

Navigation