Regional genetic differentiation among populations of Cladocora caespitosa in the Western Mediterranean

Abstract

Cladocora caespitosa is the only reef-forming zooxanthellate scleractinian in the Mediterranean Sea. This endemic coral has suffered severe mortality events at different Mediterranean sites owing to anomalous summer heat waves related to global climate change. In this study, we assessed genetic structure and gene flow among four populations of this species in the Western Mediterranean Sea: Cape Palos (SE Spain), Cala Galdana (Balearic Islands), Columbretes Islands, and L’Ametlla (NE Spain). The results obtained from Bayesian approaches, F ST statistics, and Bayesian analysis of migration rates suggest certain levels of genetic differentiation driven by high levels of self-recruitment, a fact that is supported by egg-retention mechanisms. Conversely, genetic connectivity among distant populations, even if generally low, seems to be related to sporadic dispersal events through regional surface currents linked to the spawning period that occurs at the end of summer-beginning of autumn. These features, together with a certain isolation of the Columbretes Islands, could explain the regional genetic differentiation found among populations. These results help to better understand population structure and connectivity of the species and will serve as an approach for further studies on different aspects of the biology and ecology of C. caespitosa.

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References

  1. Adjeroud M, Penin L, Carroll A (2007) Spatio-temporal heterogeneity in coral recruitment around Moorea, French Polynesia: implications for population maintenance. J Exp Mar Bio Ecol 341:204–218

    Article  Google Scholar 

  2. Aguirre J, Jiménez AP (1998) Fossil analogues to present-day Cladocora caespitosa coral banks: sedimentary setting, dwelling community, and taphonomy (Late Pliocene, W Mediterranean). Coral Reefs 17:203–213

    Article  Google Scholar 

  3. Augier H (1982) Inventory and classification of marine benthic biocenoses of the Mediterranean. Council of Europe (ed) Nature and Environmental Series 25:1–57

  4. Baums IB (2008) A restoration genetics guide for coral reef conservation. Mol Ecol 17:2796–2811

    PubMed  Article  Google Scholar 

  5. Baums IB, Miller MW, Hellberg ME (2005) Regionally isolated populations of an imperiled Caribbean coral, Acropora palmata. Mol Ecol 14:1377–1390

    CAS  PubMed  Article  Google Scholar 

  6. Bernasconi MP, Corselli C, Carobene L (1997) A bank of the scleractinian coral Cladocora caespitosa in the Pleistocene of the Crati Valley (Calabria, Southern Italy): growth versus environmental conditions. Bollettino-Società Paleontologica Italiana 36:53–61

    Google Scholar 

  7. Belkhir K, Borsa P, Chikhi L, Raufaste N, Bonhomme F (2004) GENETIX 4.05, Logiciel sous windows TM pour la génétique des populations. CNRS UMR 5000. Université de Montpellier II, Montpellier: Laboratoire Génome, Populations, Interactions

  8. Brookfield JFY (1996) A simple method for estimating null allele frequency from heterozyogote deficiency. Mol Ecol 5:453–455

    CAS  PubMed  Article  Google Scholar 

  9. Caley MJ, Carr MH, Hixon MA, Hughes TP, Jones GP, Menge BA (1996) Recruitment and the local dynamics of open marine populations. Annu Rev Ecol Syst 27:477–500

    Article  Google Scholar 

  10. Casado-Amezúa P, Goffredo S, Templado J, Machordom A (2012) Genetic assessment of population structure and connectivity in the threatened Mediterranean coral Astroides calycularis (Scleractinia, Dendrophyllidae) at different spatial scales. Mol Ecol 21:3671–3685

    PubMed  Article  Google Scholar 

  11. Casado-Amezúa P, García-Jiménez R, Kersting DK, Templado J, Coffroth MA, Merino P, Acevedo I, Machordom A (2011) Development of microsatellite markers as a molecular tool for conservation studies of the Mediterranean reef-builder coral Cladocora caespitosa (Anthozoa, Scleractinia). J Hered 5:622–626

    Article  Google Scholar 

  12. Cerrano C, Bavestrello G, Bianchi CN, Cattaneo-vietti R, Bava S, Morganti C, Morri C, Picco P, Sara G, Schiaparelli S, Siccardi A, Sponga F (2000) A catastrophic mass-mortality episode of gorgonians and other organisms in the Ligurian Sea (Northwestern Mediterranean), summer 1999. Ecol Lett 3:284–293

    Article  Google Scholar 

  13. Chapuis M, Estoup A (2007) Microsatellite null alleles and estimation of population differentiation. Mol Biol Evol 24:621–631

    CAS  PubMed  Article  Google Scholar 

  14. Cibrián- Jaramillo A, Daly AC, Brenner E, Desalle R, Marler TE (2010) When North and South don´t mix: genetic connectivity of a recently endangered oceanic cycad, Cycas micronesica, in Guam using EST-microsatellites. Mol Ecol 19:2364–2379

    PubMed  Google Scholar 

  15. Connell JH, Hughes TP, Wallace CC (1997) A 30-year study of coral abundance, recruitment, and disturbance at several scales in space and time. Ecol Monogr 67:461–488

    Article  Google Scholar 

  16. Cornuet JM, Piry S, Luikart G, Estoup A, Solignac M (1999) New methods employing multilocus genotypes to select or exclude populations as origins of individuals. Genetics 153:1989–2000

    CAS  PubMed Central  PubMed  Google Scholar 

  17. DiBacco C, Levin LA, Sala E (2006) Connectivity in marine ecosystems: the importance of larval and spore dispersal. In: Crooks KR, Sanjayan M (eds) Connectivity conservation. Cambridge University Press, Cambridge, pp 185–211

    Google Scholar 

  18. Earl DA, von Holdt BM (2012) STRUCTURE HARVESTER: a web site and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4:359–361

    Article  Google Scholar 

  19. Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620

    CAS  PubMed  Article  Google Scholar 

  20. Excoffier L, Estoup A, Cornuet JM (2005) Bayesian analysis of an admixture model with mutations and arbitrarily linked markers. Genetics 169:1727–1738

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  21. Font J, Salat J, Julià A (1990) Marine circulation along the Ebro continental margin. Mar Geol 95:165–177

    Article  Google Scholar 

  22. Font J, Garcialadona E, Gorriz EG (1995) The seasonality of mesoscale motion in the northern current of the western Mediterranean- several years of evidence. Oceanologica Acta 18:207–219

    Google Scholar 

  23. Fornós JJ, Barón A, Pons GX (1996) Arrecifes de coral hermatípicos (Cladocora caespitosa) en el relleno Holoceno de la zona de Es Grau (Menorca, Mediterráneo Occidental). Geogaceta 20:303–306

    Google Scholar 

  24. Garrabou J, Coma R, Bensoussan N, Bally M, Chevaldonné P, Cigliano M, Diaz D, Harmelin JG, Gambi MC, Kersting DK, Ledoux JB, Lejeusne C, Linares C, Marschal C, Pérez T, Ribes J, Romano C, Serrano E, Teixido N, Torrents O, Zabala M, Zuburer F, Cerrano S (2009) Mass mortality in North-western Mediterranean rocky benthic communities: effects of the 2003 heat wave. Glob Chang Biol 15:1090–1103

    Article  Google Scholar 

  25. Grosberg R, Cunningham CW (2001) Genetic structure in the sea: from populations to communities. In: Bertness MD, Gaines S, Hay ME (eds) Marine community ecology. Sinauer Associates, Sunderland, MA, pp 61–84

    Google Scholar 

  26. Hellberg ME (2007) Footprints on water: the genetic wake of dispersal among reefs. Coral Reefs 26:463–473

    Article  Google Scholar 

  27. Hellberg ME, Burton RS, Neigel JE, Palumbi SR (2002) Genetic assessment of connectivity among marine populations. Biol Bull 70:273–290

    Google Scholar 

  28. Holm S (1979) A simple sequentially rejective multiple test procedure. Scand J Stat 6:65–70

    Google Scholar 

  29. Hubisz M, Falush D, Stephens M, Pritchard J (2009) Inferring weak population structure with the assistance of sample group information. Mol Ecol Res 9:1322–1332

    Article  Google Scholar 

  30. Jakobsson M, Rosenberg N (2007) CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23:1801–1806

    CAS  PubMed  Article  Google Scholar 

  31. Jensen JL, Bohonak AJ, Kelley ST (2005) Isolation by distance, web service. BMC Genet 6:13. V3.21. http://ibdws.sdsu.edu/

  32. Kalinowsky ST (2005) HP-RARE: a computer program for performing rarefaction on measures of allelic diversity. Mol Ecol Notes 5:539–543

    Google Scholar 

  33. Kersting DK, Linares C (2012) Cladocora caespitosa bioconstructions in the Columbretes Islands Marine Reserve (Spain, NW Mediterranean): distribution, size structure and growth. Mar Ecol 33:427–436

    Article  Google Scholar 

  34. Kersting DK, Bensoussan N, Linares C (2013a) Long-term responses of the endemic reef-builder Cladocora caespitosa to Mediterranean warming. PLoS One 8:e70820

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  35. Kersting DK, Teixidó N, Linares C (2014a) Recruitment and mortality of the temperate coral Cladocora caespitosa: implications for the recovery of endangered populations. Coral Reefs 33:403–407

    Article  Google Scholar 

  36. Kersting DK, Casado C, López-Legentil S, Linares C (2013b) Unexpected patterns in the sexual reproduction of the Mediterranean scleractinian coral Cladocora caespitosa. Mar Ecol Prog Ser 486:165–171

    Article  Google Scholar 

  37. Kersting DK, Ballesteros E, De Caralt S, Linares C (2014b) Invasive macrophytes in a marine reserve (Columbretes Islands, NW Mediterranean): spread dynamics and interactions with the endemic scleractinian coral Cladocora caespitosa. Biol Invasions 16:1599–1610

    Google Scholar 

  38. Kružić P, Benković L (2008) Bioconstructional features of the coral Cladocora caespitosa (Anthozoa, Scleractinia) in the Southern Adriatic Sea. Coral Reefs 27:125–139

    Google Scholar 

  39. Kružic P, Zuljevic A, Nokolic V (2008a) Spawning of the colonial coral Cladocora caespitosa (Anthozoa, Scleractinia) in the Southern Adriatic Sea. Coral Reefs 27:337–341

    Article  Google Scholar 

  40. Kružić P, Zuljevic A, Nikolic V (2008b) The highly invasive alga Caulerpa racemosa var. cylindracea poses a new threat to the banks of the coral Cladocora caespitosa in the Adriatic Sea. Coral Reefs 27:441

    Article  Google Scholar 

  41. Kružić P, Sršen P, Benković L (2012) The impact of seawater temperature on coral growth parameters of the colonial coal Cladocora caespitosa (Anthozoa, Scleracinia) in the Eastern Adriatic Sea. Facies 58:477–491

    Article  Google Scholar 

  42. Kühlman DHH, Chitiroglou H, Koutsoubas D, Koukouras A (1991) Korallenriffe im Mittelmeer? Naturwiss Rundsch 44:316

    Google Scholar 

  43. Laborel J (1961) Sur un cas particulier de concrétionnement animal. Concrétionnement à Cladocora caespitosa L. dans le Golfe de Talante. Rápp. pv Réun. CIESM 16:429–432

    Google Scholar 

  44. Latch EK, Dharmarajan G, Glaubitz JC, Rhodes OE Jr (2006) Relative performance of Bayesian clustering software for inferring population substructure and individual assignment at low level of population differentiation. Conserv Genet 7:295–302

    Article  Google Scholar 

  45. La Violette PE, Tintoré J, Font J (1990) The surface circulation of the Balearic Sea. J Geophys Res 95:1559–1568

    Article  Google Scholar 

  46. Lejeusne C, Chevaldonné P, Pergent-Martini C, Boudouresque CF, Pérez T (2009) Climate change effects on a miniature ocean: the highly diverse, highly impacted Mediterranean Sea. Trends Ecol Evol 25:250–260

    PubMed  Article  Google Scholar 

  47. Luikart G, England PR, Tallmon D, Jordan S, Taberlet P (2003) The power of population genomics: from genotyping to genome typing. Nat Rev Genet 4:981–994

    CAS  PubMed  Article  Google Scholar 

  48. Mokhtar-Jamaï K, Pascual M, Ledoux JB, Coma R, Féral JP, 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. Mol Ecol 20:3291–3305

    PubMed  Article  Google Scholar 

  49. Morri C, Peirano A, Bianchi CN, Sassarini M (1994) Present day bioconstructions of the hard coral, Cladocora caespitosa (L.) (Anthozoa, Scleractinia), in the Eastern Ligurian Sea (NW Mediterranean). Biologia Marina Mediterranea 1:371–373

    Google Scholar 

  50. Özalp HB, Alparslan M (2011) The first record of Cladocora caespitosa (Linnaeus, 1767) (Anthozoa, Scleractinia) from the marmara Sea. Turk Zool Derg 35:701–705

    Google Scholar 

  51. Peakal R, Smouse PE (2006) GENEALEX 6: Genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295

    Article  Google Scholar 

  52. Peirano A, Morri C, Bianchi CN (1999) Skeleton growth and density patterns of the temperature, zooxanthellate scleractinain Cladocora caespitosa from the Ligurian Sea (NW Mediterranean). Mar Ecol Prog Ser 185:195–201

    Article  Google Scholar 

  53. Peirano A, Kružić P, Mastronuzzi G (2009) Growth of Mediterranean reef of Cladocora caespitosa (L.) in the Late Quaternary and climate inferences. Facies 55:325–333

    Article  Google Scholar 

  54. Perez T, Garrabou J, Sartoretto S, Harmelin JG, Francour P, Vacelet J (2000) Mass mortality of marine invertebrates: an unprecedented event in the Northwestern Mediterranean. C R Acad Sci III 323:853–865

    CAS  PubMed  Article  Google Scholar 

  55. Pineda J, Hare JA, Sponaugle SU (2007) Larval transport and dispersal in the coastal ocean and consequences for population connectivity. Oceanography 20:22–39

    Article  Google Scholar 

  56. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959

    CAS  PubMed Central  PubMed  Google Scholar 

  57. Raymond M, Rousset F (1995) Genepop (version 1.2): population genetics software for exact tests and ecumenicism. J Hered 86:248–249

    Google Scholar 

  58. Rodolfo-Metalpa R, Bianchi CN, Peirano A, Morri C (2005) Tissue necrosis and mortality of the temperate coral Cladocora caespitosa. Ital J Zool 72:271–276

    Article  Google Scholar 

  59. Rosenberg NA (2004) DISTRUCT: a program for the graphical display of population structure. Mol Ecol Notes 4:137–138

    Article  Google Scholar 

  60. Rousset F (1997) Genetic differentiation and estimation of gene flow from F-statistics under isolation by distance. Genetics 145:1219–1228

    CAS  PubMed Central  PubMed  Google Scholar 

  61. Ryman N, Palm S (2006) POWSIM: a computer program for assessing statistical power when testing for genetic differentiation. Mol Ecol Notes 6:600–602

    Article  Google Scholar 

  62. Ruiz S, Pascual A, Garau B, Faugère Y, Alvarez A, Tintoré J (2009) Mesoscale dynamics of the Balearic front integrating glider, ship and satellite data. J Mar Syst 78:S3–S16

    Article  Google Scholar 

  63. Sams MA, Keough MJ (2013) Effects of early recruits on temperate sessile marine community composition depend on other species recruiting at the time. Oecologia 173:259–268

    PubMed  Article  Google Scholar 

  64. Schiller CH (1993) Ecology of the symbiotic coral Cladocora caespitosa (L.) (Faviidae, Scleractinia) in the Bay of Piran (Adriatic Sea): I. Distribution and biometry. Mar Ecol 14:205–219

    Article  Google Scholar 

  65. Schunter C, Carreras-Carbonell J, Macpherson E, Tintore J, Vidal-Vijande E, Pascual A, Guidetti P, Pascual M (2011) Matching genetics with oceanography: directional gene flow in a Mediterranean fish species. Mol Ecol 20:5167–5181

    CAS  PubMed  Article  Google Scholar 

  66. Slatkin M (1993) Isolation by distance in equilibrium and nonequilibrium populations. Evolution 47:264–279

    Article  Google Scholar 

  67. Slatkin M (2005) Seeing ghosts: the effect of unsampled populations on migration rates estimated for sampled populations. Mol Ecol 14:67–73

    PubMed  Article  Google Scholar 

  68. Sokal RR, Rohlf FJ (1981) Biometry, 2nd edn. WH Freeman & Co., New York

    Google Scholar 

  69. Templado J (2014) Future trends of Mediterranean biodiversity. In: Goffredo S, Dubinsky Z (eds) The Mediterranean Sea: Its history and present challenges. Springer, New York, pp 479–498

    Google Scholar 

  70. van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P (2004) MICROCHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538

    Article  Google Scholar 

  71. Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370

    Article  Google Scholar 

  72. Wilson GA, Rannala B (2003) Bayesian inference of recent migration rates using multilocus genotypes. Genetics 163:1177–1191

    PubMed Central  PubMed  Google Scholar 

  73. Yoshioka PM (1996) Variable recruitment and its effects on the population and community structure of shallow-water gorgonians. Bull Mar Sci 59:433–443

    Google Scholar 

  74. Zibrowius H (1980) Nouvelles données sur la distribution de quelques scléractiniaires “méditerranéens” à l’est et à l’ouest du détroit de Gibraltar. Rapports et Procès- Verbaux des Réunions-Commission Internationale pour l’Exploration Scientifique de la Mer Mediterranée Monaco 28:307–309

    Google Scholar 

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Acknowledgments

We want to acknowledge A. Luque, M. Taviani, P. Montagna, J. Fayos, E. Serrano and A. Addamo for their help either in the field work or providing samples, and M.H. Nielsen for help on data analysis. We thank S. Young and M. Hara for English revision of grammar and style. C. Papetti helped us to improve the manuscript with suggestions on the analyses. Two anonymous reviewers and S. Swearer help to improve this manuscript. We thank the Secretaría General de Pesca Marítima (MAGRAMA) and the Columbretes Islands Marine Reserve staff for their logistical support. We thank the Spanish authorities for Environment and Fisheries, Valencia Autonomous Community and Balearic Islands Regional Government the permits for collecting the samples. This study was supported by the Autonomous Organism of National Parks (Spanish Ministry of Environment) and projects CGL2011-23306 from the Spanish Ministry of Science and Innovation, and COCONET—“Towards COast to COast NETworks of marine protected areas (from the shore to the high and deep sea), coupled with sea-based wind energy potential”—from the VII FP of the European Commission. P. Casado-Amezua is currently funded by a postdoctoral internship from the Alfred Wegener Institute for Polar and Marine Research (AWI).

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Casado-Amezúa, P., Kersting, D.K., Templado, J. et al. Regional genetic differentiation among populations of Cladocora caespitosa in the Western Mediterranean. Coral Reefs 33, 1031–1040 (2014). https://doi.org/10.1007/s00338-014-1195-5

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Keywords

  • Microsatellites
  • Genetic differentiation
  • Broadcast spawning coral
  • Self-recruitment
  • Oceanographic barriers