Organisms Diversity & Evolution

, Volume 17, Issue 2, pp 365–373 | Cite as

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

  • Angelo Poliseno
  • Alvaro Altuna
  • Carlo Cerrano
  • Gert Wörheide
  • Sergio Vargas
Original Article

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.

Keywords

Endemic species Mediterranean Mitogenomics Paramuricea Phylogeography Vicariance Octocorals 

Supplementary material

13127_2017_322_MOESM1_ESM.pdf (898 kb)
ESM 1(PDF 898 kb)

References

  1. 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.CrossRefGoogle Scholar
  2. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  3. 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.CrossRefGoogle Scholar
  4. 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.CrossRefGoogle Scholar
  5. Bas, C. (2009). The Mediterranean: a synoptic overview. Contributions to Science, 5, 25–39.Google Scholar
  6. 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
  7. 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.Google Scholar
  8. Bianchi, C., & Morri, C. (2000). Marine biodiversity of the Mediterranean Sea: situation, problems and prospects for future research. Marine Pollution Bulletin, 40, 367–376.CrossRefGoogle Scholar
  9. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  10. Bouckaert, R. (2010). DensiTree: making sense of sets of phylogenetic trees. Bioinformatics, 26, 1372–1373.CrossRefPubMedGoogle Scholar
  11. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  12. 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
  13. 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.Google Scholar
  14. 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.CrossRefPubMedGoogle Scholar
  15. Carpine, C., & Grasshoff, M. (1975). Les Gorgonaires de la Méditerranée. Bulletin de l’Institut Océanographique de Monaco, 71, 1–140.Google Scholar
  16. 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.CrossRefGoogle Scholar
  17. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  18. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  19. 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.CrossRefGoogle Scholar
  20. Darriba, D., Taboada, G. L., Doallo, R., & Posada, D. (2012). jModelTest 2: more models, new heuristics and parallel computing. Nature Methods, 9, 772.CrossRefPubMedPubMedCentralGoogle Scholar
  21. 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.CrossRefGoogle Scholar
  22. 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.CrossRefPubMedGoogle Scholar
  23. Dov Por, F. (2009). Tethys returns to the Mediterranean: success and limits of tropical re-colonization. BioRisk, 3, 5–19.CrossRefGoogle Scholar
  24. 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
  25. Edgar, R. C. (2004). MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research, 32, 1792–1797.CrossRefPubMedPubMedCentralGoogle Scholar
  26. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  27. 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.CrossRefGoogle Scholar
  28. 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.CrossRefGoogle Scholar
  29. 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.CrossRefPubMedGoogle Scholar
  30. Grasshoff, M. (1977). Die Gorgonarien des östlichen Nordatlantik und des Mittelmeeres. III Die Familie Paramuriceidae (Cnidaria, Anthozoa). Meteor Forschungsergebnisse, 27, 5–76.Google Scholar
  31. Grasshoff, M. (1992). Die Flachwasser-Gorgonarien von Europa und Westafrika (Cnidaria, Anthozoa). Courier Forschungsinsitut Senckenberg, 149, 1–135.Google Scholar
  32. Hsü, K. J., Ryan, W. B. F., & Cita, M. B. (1973). Late Miocene dessication of the Mediterranean. Nature, 242, 240–244.CrossRefGoogle Scholar
  33. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  34. 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.CrossRefPubMedGoogle Scholar
  35. 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.Google Scholar
  36. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  37. Librado, P., & Rozas, J. (2009). DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics, 25, 1451–1452.CrossRefPubMedGoogle Scholar
  38. 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.CrossRefPubMedGoogle Scholar
  39. 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.CrossRefPubMedGoogle Scholar
  40. 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.CrossRefPubMedGoogle Scholar
  41. 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.CrossRefGoogle Scholar
  42. 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.CrossRefPubMedGoogle Scholar
  43. 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.CrossRefPubMedGoogle Scholar
  44. 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
  45. 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
  46. 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
  47. 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.CrossRefPubMedGoogle Scholar
  48. Rambaut, A., Drummond, A. J. (2009). Tracer—MCMC trace analysis tool. Ver. 1. 5. Edinburgh: University of Edinburgh.Google Scholar
  49. 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.CrossRefPubMedGoogle Scholar
  50. Ronquist, F. (1997). Dispersal-vicariance analysis: a new approach to the quantification of historical biogeography. Systematic Biology, 46, 195–203.CrossRefGoogle Scholar
  51. Ronquist, F. (2001). DIVA—computer program for MacOS and Win32. Ver 1. 2. Uppsala: Evolutionary Biology Centre, Uppsala University.Google Scholar
  52. 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.CrossRefGoogle Scholar
  53. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  54. 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.CrossRefGoogle Scholar
  55. Stamatakis, A. (2006). RAxML-VI-HPC: maximum likelihood based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics, 22, 2688–2690.CrossRefPubMedGoogle Scholar
  56. Stamatakis, A., Hoover, P., & Rougemont, J. (2008). A rapid bootstrap algorithm for the RAxML Web servers. Systematic Biology, 57, 758–771.CrossRefPubMedGoogle Scholar
  57. 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.CrossRefGoogle Scholar
  58. 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.CrossRefGoogle Scholar
  59. 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.CrossRefGoogle Scholar
  60. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  61. 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.
  62. 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.CrossRefGoogle Scholar
  63. 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.CrossRefGoogle Scholar
  64. 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.CrossRefGoogle Scholar
  65. 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
  66. 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.CrossRefGoogle Scholar
  67. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  68. 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.CrossRefGoogle Scholar
  69. 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.

Copyright information

© Gesellschaft für Biologische Systematik 2017

Authors and Affiliations

  • Angelo Poliseno
    • 1
  • Alvaro Altuna
    • 2
  • Carlo Cerrano
    • 3
  • Gert Wörheide
    • 1
    • 4
    • 5
  • Sergio Vargas
    • 1
  1. 1.Department of Earth and Environmental Sciences, Palaeontology and GeobiologyLudwig-Maximilians-Universität MünchenMunichGermany
  2. 2.INSUB, Zemoria 12San SebastiánSpain
  3. 3.Department of Life and Environmental Sciences (DiSVA)Marche Polytechnic UniversityAnconaItaly
  4. 4.GeoBio-CenterLudwig-Maximilians-Universität MünchenMunichGermany
  5. 5.Bayerische Staatssammlung für Paläontologie und GeologieMunichGermany

Personalised recommendations