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Marine Biology

, 165:167 | Cite as

High genetic differentiation and low connectivity in the coral Pocillopora damicornis type β at different spatial scales in the Southwestern Indian Ocean and the Tropical Southwestern Pacific

  • Pauline Gélin
  • Agathe Pirog
  • Cécile Fauvelot
  • Hélène Magalon
Original paper

Abstract

Studying genetic connectivity in marine populations aims to understand the dispersal of an organism through the seascape and thus its gene flow. Here, we focused on one lineage of the recently revised coral Pocillopora damicornis complex, P. damicornis type β, corresponding to Primary Species Hypothesis PSH05 in Gélin et al. (Mol Phylogenet Evol 109:430–446, 2017b): it had been hypothesized that P. damicornis type β encompasses four distinct lineages, representing Secondary Species Hypotheses (SSH05a, SSH05b, SSH05c and SSH05d). The aim of the present study was to confirm this partition and to infer the genetic structuring and connectivity among 27 populations for this widespread and common scleractinian. For this, a total of 1418 colonies were hierarchically sampled from two marine provinces of the southern parts of its distribution range, which remain largely understudied: the Western Indian Ocean and the Tropical Southwestern Pacific. Using 13 microsatellite loci and assignment tests, our findings confirmed the partition into four SSHs, each SSH splitting into clusters, suggesting that P. damicornis type β may represent a complex of cryptic species. Moreover, within each SSH, clonal propagation was evidenced in almost every population, but clonal dispersal was mostly restricted to sampling site (except in Reunion Island and northern Madagascar, where clones were found in several populations approximately 50 km apart). Nevertheless, wherever the cursor of species level is placed (one or several species), populations were highly differentiated both within the Western Indian Ocean and the Tropical Southwestern Pacific, suggesting restricted gene flow at different spatial scales (marine province, ecoregions, islands/regions), leading to diverging lineages.

Notes

Acknowledgements

Coral sampling in New Caledonia (HM) was carried out during COBELO (http://dx.doi.org/10.17600/14003700), BIBELOT (http://dx.doi.org/10.17600/13100100), and CHEST (http://dx.doi.org/10.17600/15004500) oceanographic campaigns on board of RV Alis (IRD), and in the North-East and North-West of Madagascar during MAD (http://dx.doi.org/10.17600/16004700) oceanographic campaign on board of RV Antea (IRD). Sampling in Reunion Island (HM, PG) was supported by program CONPOCINPA (LabEx CORAIL fund); in South Madagascar (HM) in collaboration with the Institut Halieutique des Sciences Marines (Tulear) and in Rodrigues Island (HM) with the collaboration of the Rodrigues Regional Assembly and the South-East Marine Protected Area supported by project Biodiversity (POCT FEDER fund); in Juan de Nova (HM) by program BIORECIE (financial supports from INEE, INSU, IRD, AAMP, FRB, TAAF, and the foundation Veolia Environnement); in Mayotte (HM) by program SIREME (FED). We acknowledge the Plateforme Gentyane of the Institut National de la Recherche Agronomique (INRA, Clermont-Ferrand, France) for guidance and technical support. The first author was financially supported by a PhD contract from the LabEx CORAIL. We thank the reviewers for their comments to improve the manuscript.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

We declare that all applicable international, national and/or institutional guidelines for sampling, care and experimental use of organisms for the study have been followed and all necessary approvals have been obtained: New Caledonia: authorization no. 2432-2012/ARR/DENV, no. 2660-2013/ARR/DENV, no. 60912-25-28-2012/JJC, no. 60455-15-25/JJC, no. 6161-37/PR. Reunion Island: authorization no. 14-2013/DEAL/SEB/UBIO. Madagascar: authorization no. 16/1040-AE/SG/DAJC/SAG/NAV/FRANCE. Rodrigues Island: authorization no. MU 140897/Regional Assembly. Mayotte: authorization no. 2016-31/DMSOI. Juan de Nova: authorization no. 2013-66/TAAF.

Supplementary material

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References

  1. Adjeroud M, Guérécheau A, Vidal-Dupiol J, Flot J-F, Arnaud-Haond S, Bonhomme F (2014) Genetic diversity, clonality and connectivity in the scleractinian coral Pocillopora damicornis: a multi-scale analysis in an insular, fragmented reef system. Mar Biol 161:531–541.  https://doi.org/10.1007/s00227-013-2355-9 CrossRefGoogle Scholar
  2. Alberto F, Gouveia L, Arnaud-Haond S, Perez-Llorens JL, Duarte CM, Serrao EA (2005) Within-population spatial genetic structure, neighbourhood size and clonal subrange in the seagrass Cymodocea nodosa. Mol Ecol 14:2669–2681.  https://doi.org/10.1111/j.1365-294X.2005.02640.x CrossRefPubMedGoogle Scholar
  3. Arnaud-Haond S, Belkhir K (2007) GENCLONE: a computer program to analyse genotypic data, test for clonality and describe spatial clonal organization. Mol Ecol Notes 7:15–17CrossRefGoogle Scholar
  4. Arnaud-Haond S, Duarte CM, Alberto F, Serrao EA (2007) Standardizing methods to address clonality in population studies. Mol Ecol 16:5115–5139.  https://doi.org/10.1111/j.1365-294X.2007.03535.x CrossRefPubMedGoogle Scholar
  5. Ayre DJ, Hughes TP, Standish RJ (1997) Genetic differentiation, reproductive mode, and gene flow in the brooding coral Pocillopora damicornis along the Great Barrier Reef, Australia. Mar Ecol Prog Ser 159:175–187CrossRefGoogle Scholar
  6. Bailleul D, Stoeckel S, Arnaud-Haond S (2016) RClone: a package to identify multiLocus clonal lineages and handle clonal datasets in R. Methods Ecol Evol.  https://doi.org/10.1111/2041-210x.12550 CrossRefGoogle Scholar
  7. Balloux F, Lehmann L, de Meeûs T (2003) The population genetics of clonal and partially clonal diploids. Genetics 164:1635PubMedPubMedCentralGoogle Scholar
  8. Conand C, Uthicke S, Hoareau T (2002) Sexual and asexual reproduction of the holothurian Stichopus chloronotus (Echinodermata): a comparison between La Réunion (Indian Ocean) and east Australia (Pacific Ocean). Invertebr Reprod Dev 41:235–242.  https://doi.org/10.1080/07924259.2002.9652756 CrossRefGoogle Scholar
  9. de Meeûs T, Prugnolle F, Agnew P (2007) Asexual reproduction: genetics and evolutionary aspects. Cell Mol Life Sci 64:1355–1372.  https://doi.org/10.1007/s00018-007-6515-2 CrossRefPubMedGoogle Scholar
  10. Dorken ME, Eckert CG (2001) Severely reduced sexual reproduction in northern populations of a clonal plant, Decodon verticillatus (Lythraceae). J Ecol 89:339–350CrossRefGoogle Scholar
  11. Dubé CE, Boissin E, Maynard JA, Planes S (2017) Fire coral clones demonstrate phenotypic plasticity among reef habitats. Mol Ecol.  https://doi.org/10.1111/mec.14165 CrossRefPubMedGoogle Scholar
  12. 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.  https://doi.org/10.1111/j.1365-294X.2005.02553.x CrossRefPubMedPubMedCentralGoogle Scholar
  13. Flot JF, Magalon H, Cruaud C, Couloux A, Tillier S (2008) Patterns of genetic structure among Hawaiian corals of the genus Pocillopora yield clusters of individuals that are compatible with morphology. C R Biol 331:239–247.  https://doi.org/10.1016/j.crvi.2007.12.003 CrossRefPubMedGoogle Scholar
  14. Gao H, Williamson S, Bustamante CD (2007) A Markov chain Monte Carlo approach for joint inference of population structure and inbreeding rates from multilocus genotype data. Genetics 176:1635–1651.  https://doi.org/10.1534/genetics.107.072371 CrossRefPubMedPubMedCentralGoogle Scholar
  15. Gélin P, Fauvelot C, Mehn V, Bureau S, Rouzé H, Magalon H (2017a) Superclone expansion, long-distance clonal dispersal and local genetic structuring in the coral Pocillopora damicornis type β in Reunion Island, South Western Indian Ocean. PLoS One 12:e0169692.  https://doi.org/10.1371/journal.pone.0169692 CrossRefPubMedPubMedCentralGoogle Scholar
  16. Gélin P, Postaire B, Fauvelot C, Hélène M (2017b) Reevaluating species number, distribution and endemism of the coral genus Pocillopora Lamarck, 1816 using species delimitation methods and microsatellites. Mol Phylogenet Evol 109:430–446.  https://doi.org/10.1016/j.ympev.2017.01.018 CrossRefPubMedGoogle Scholar
  17. Gélin P, Fauvelot C, Bigot L, Baly J, Magalon H (2018) From population connectivity to the art of striping Russian dolls: the lessons from Pocillopora corals. Ecol Evol 8:1411–1426.  https://doi.org/10.1002/ece3.3747 CrossRefPubMedGoogle Scholar
  18. Gerlach G, Jueterbock A, Kraemer P, Deppermann J, Harmand P (2010) Calculations of population differentiation based on G ST. Mol Ecol 19:3845–3852CrossRefGoogle Scholar
  19. Gorospe KD, Karl SA (2013) Genetic relatedness does not retain spatial pattern across multiple spatial scales: dispersal and colonization in the coral, Pocillopora damicornis. Mol Ecol 22:3721–3736CrossRefGoogle Scholar
  20. Gorospe KD, Karl SA (2015) Depth as an organizing force in Pocillopora damicornis: intra-reef genetic architecture. PLoS One 10:e0122127.  https://doi.org/10.1371/journal.pone.0122127 CrossRefPubMedPubMedCentralGoogle Scholar
  21. Goudet J (2001) FSTAT, a program to estimate and test gene diversities and fixation indices version 2.9. 3.2. Updated from Goudet 1995. FSTATGoogle Scholar
  22. Halkett F, Simon J-C, Balloux F (2005) Tackling the population genetics of clonal and partially clonal organisms. Trends Ecol Evol 20:194–201.  https://doi.org/10.1016/j.tree.2005.01.001 CrossRefPubMedGoogle Scholar
  23. Highsmith RC (1982) Reproduction by fragmentation in corals. Mar Ecol Prog Ser 7:207–226CrossRefGoogle Scholar
  24. Hsu C-M, de Palmas S, Kuo C-Y, Denis V, Chen CA (2014) Identification of scleractinian coral recruits using fluorescent censusing and DNA barcoding techniques. PLoS One 9:e107366.  https://doi.org/10.1371/journal.pone.0107366 CrossRefPubMedPubMedCentralGoogle Scholar
  25. Hubisz MJ, Falush D, Stephens M, Pritchard JK (2009) Inferring weak population structure with the assistance of sample group information. Mol Ecol Resour 9:1322–1332.  https://doi.org/10.1111/j.1755-0998.2009.02591.x CrossRefPubMedPubMedCentralGoogle Scholar
  26. Hunter CL (1993) Genotypic variation and clonal structure in coral populations with different disturbance histories. Evolution 47:1213–1228.  https://doi.org/10.2307/2409987 CrossRefPubMedGoogle Scholar
  27. Jombart T (2008) adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics 24:1403–1405CrossRefGoogle Scholar
  28. Jombart T, Devillard S, Balloux F (2010) Discriminant analysis of principal components: a new method for the analysis of genetically structured populations. BMC Genet 11:94.  https://doi.org/10.1186/1471-2156-11-94 CrossRefPubMedPubMedCentralGoogle Scholar
  29. Jost L (2008) G ST and its relatives do not measure differentiation. Mol Ecol 17:4015–4026CrossRefGoogle Scholar
  30. Judson OP, Normark BB (1996) Ancient asexual scandals. Trends Ecol Evol 11:41–46.  https://doi.org/10.1016/0169-5347(96)81040-8 CrossRefPubMedGoogle Scholar
  31. Kalinowski ST (2005) HP-RARE 1.0: a computer program for performing rarefaction on measures of allelic richness. Mol Ecol Notes 5:187–189.  https://doi.org/10.1111/j.1471-8286.2004.00845.x CrossRefGoogle Scholar
  32. Kivelä M, Arnaud-Haond S, Saramäki J (2015) EDENetworks: a user-friendly software to build and analyse networks in biogeography, ecology and population genetics. Mol Ecol Resour 15:117–122.  https://doi.org/10.1111/1755-0998.12290 CrossRefPubMedGoogle Scholar
  33. Klekowski EJ (1998) Mutation rates in mangroves and other plants. Genetica 102:325–331.  https://doi.org/10.1023/A:1017026907407 CrossRefGoogle Scholar
  34. Marti-Puig P, Forsman ZH, Haverkort-Yeh RD, Knapp ISS, Maragos JE, Toonen RJ (2014) Extreme phenotypic polymorphism in the coral genus Pocillopora; micro-morphology corresponds to mitochondrial groups, while colony morphology does not. Bull Mar Sci 90:211–231.  https://doi.org/10.5343/bms.2012.1080 CrossRefGoogle Scholar
  35. Mayr E (1963) Animal species and evolution. Harvard University Press, CambridgeCrossRefGoogle Scholar
  36. Meirmans PG, Van Tienderen PH (2004) GENOTYPE and GENODIVE: two programs for the analysis of genetic diversity of asexual organisms. Mol Ecol Notes 4:792–794.  https://doi.org/10.1111/j.1471-8286.2004.00770.x CrossRefGoogle Scholar
  37. Muths D, Tessier E, Bourjea J (2015) Genetic structure of the reef grouper Epinephelus merra in the West Indian Ocean appears congruent with biogeographic and oceanographic boundaries. Mar Ecol 36:447–461.  https://doi.org/10.1111/maec.12153 CrossRefGoogle Scholar
  38. Nakajima Y, Zayasu Y, Shinzato C, Satoh N, Mitarai S (2016) Genetic differentiation and connectivity of morphological types of the broadcast-spawning coral Galaxea fascicularis in the Nansei Islands, Japan. Ecol Evol 6:1457–1469.  https://doi.org/10.1002/ece3.1981 CrossRefPubMedPubMedCentralGoogle Scholar
  39. Pante E, Puillandre N, Viricel A, Arnaud-Haond S, Aurelle D, Castelin M, Chenuil A, Destombe C, Forcioli D, Valero M, Viard F, Samadi S (2015) Species are hypotheses: avoid connectivity assessments based on pillars of sand. Mol Ecol 24:525–544.  https://doi.org/10.1111/mec.13048 CrossRefPubMedGoogle Scholar
  40. Pinzón JH, Sampayo E, Cox E, Chauka LJ, Chen CA, Voolstra CR, LaJeunesse TC, Maggs C (2013) Blind to morphology: genetics identifies several widespread ecologically common species and few endemics among Indo-Pacific cauliflower corals (Pocillopora, Scleractinia). J Biogeogr 40:1595–1608.  https://doi.org/10.1111/jbi.12110 CrossRefGoogle Scholar
  41. Pirog A, Gélin P, Bédier A, Bianchetti G, Georget S, Frouin P, Magalon H (2017) Clonal structure through space and time: high stability in the holothurian Stichopus chloronotus (Echinodermata). Ecol Evol.  https://doi.org/10.1002/ece3.3285 CrossRefPubMedPubMedCentralGoogle Scholar
  42. Planes S, Parroni M, Chauvet C (1998) Evidence of limited gene flow in three species of coral reef fishes in the lagoon of New Caledonia. Mar Biol 130:361–368CrossRefGoogle Scholar
  43. Postaire B, Gélin P, Bruggemann JH, Magalon H (2017a) One species for one island? Unexpected diversity and weak connectivity in a widely distributed tropical hydrozoan. Heredity.  https://doi.org/10.1038/hdy.2016.126 CrossRefPubMedPubMedCentralGoogle Scholar
  44. Postaire B, Gélin P, Bruggemann JH, Pratlong M, Magalon H (2017b) Population differentiation or species formation across the Indian and the Pacific Oceans? An example from the brooding marine hydrozoan Macrorhynchia phoenicea. Ecol Evol.  https://doi.org/10.1002/ece3.3236 CrossRefPubMedPubMedCentralGoogle Scholar
  45. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:954–959Google Scholar
  46. R Core Team (2016) R: a language and environment for statistical computingGoogle Scholar
  47. Rozenfeld AF, Arnaud-Haond S, Hernández-García E, Eguíluz VM, Matías MA, Serrao E, Duarte CM (2007) Spectrum of genetic diversity and networks of clonal organisms. J R Soc Interface 4:1093–1102CrossRefGoogle Scholar
  48. Schmidt-Roach S, Miller KJ, Woolsey E, Gerlach G, Baird AH (2012) Broadcast spawning by Pocillopora species on the Great Barrier Reef. PLoS One 7:e50847.  https://doi.org/10.1371/journal.pone.0050847 CrossRefPubMedPubMedCentralGoogle Scholar
  49. Schmidt-Roach S, Lundgren P, Miller KJ, Gerlach G, Noreen AME, Andreakis N (2013) Assessing hidden species diversity in the coral Pocillopora damicornis from Eastern Australia. Coral Reefs 32:161–172.  https://doi.org/10.1007/s00338-012-0959-z CrossRefGoogle Scholar
  50. Schmidt-Roach S, Johnston E, Fontana S, Jury CP, Forsman Z (2014a) Daytime spawning of Pocillopora species in Kaneohe Bay, Hawai‘i. Galaxea 16:11–12CrossRefGoogle Scholar
  51. Schmidt-Roach S, Miller KJ, Lundgren P, Andreakis N (2014b) With eyes wide open: a revision of species within and closely related to the Pocillopora damicornis species complex (Scleractinia; Pocilloporidae) using morphology and genetics. Zool J Linn Soc 170:1–33.  https://doi.org/10.1111/zoj.12092 CrossRefGoogle Scholar
  52. Schneider S, Roessli D, Excoffier L (2000) Arlequin ver. 2.000: a software for population genetics data analysis. University of Geneva, GenevaGoogle Scholar
  53. Sherman CDH, Ayre DJ, Miller KJ (2006) Asexual reproduction does not produce clonal populations of the brooding coral Pocillopora damicornis on the Great Barrier Reef, Australia. Coral Reefs 25:7–18CrossRefGoogle Scholar
  54. Smith H, Epstein H, Torda G (2017) The molecular basis of differential morphology and bleaching thresholds in two morphs of the coral Pocillopora acuta. Sci Rep 7:10066.  https://doi.org/10.1038/s41598-017-10560-2 CrossRefPubMedPubMedCentralGoogle Scholar
  55. Sommerfeldt AD, Bishop JDD, Wood CA (2003) Chimerism following fusion in a clonal ascidian (Urochordata). Biol J Linn Soc 79:183–192.  https://doi.org/10.1046/j.1095-8312.2003.00179.x CrossRefGoogle Scholar
  56. Souter P, Henriksson O, Olsson N, Grahn M (2009) Patterns of genetic structuring in the coral Pocillopora damicornis on reefs in East Africa. BMC Ecol 9:19.  https://doi.org/10.1186/1472-6785-9-19 CrossRefPubMedPubMedCentralGoogle Scholar
  57. Spalding MD, Fox HE, Allen GR, Davidson N, Ferdaña ZA, Finlayson M, Halpern BS, Jorge MA, Lombana A, Lourie SA, Martin KD, McManus E, Molnar J, Recchia CA, Robertson J (2007) Marine ecoregions of the world: a bioregionalization of coastal and shelf areas. Bioscience 57:573–583.  https://doi.org/10.1641/b570707 CrossRefGoogle Scholar
  58. Stoddart JA (1983) Asexual production of planulae in the coral Pocillopora damicornis. Mar Biol 76:279–284CrossRefGoogle Scholar
  59. Stoddart JA (1984) Genetic differentiation amongst populations of the coral Pocillopora damicornis off southwestern Australia. Coral Reefs 3:149–156.  https://doi.org/10.1007/BF00301959 CrossRefGoogle Scholar
  60. Stoddart J, Black R (1985) Cycles of gametogenesis and planulation in the coral Pocillopora damicornis. Mar Ecol Prog Ser 23:153–164CrossRefGoogle Scholar
  61. Stoddart JA, Taylor JF (1988) Genotypic diversity: estimation and prediction in samples. Genetics 118:705–711PubMedPubMedCentralGoogle Scholar
  62. Torda G, Lundgren P, Willis BL, van Oppen MJ (2013a) Revisiting the connectivity puzzle of the common coral Pocillopora damicornis. Mol Ecol 22:5805–5820.  https://doi.org/10.1111/mec.12540 CrossRefPubMedGoogle Scholar
  63. Torda G, Lundgren P, Willis BL, van Oppen MJH (2013b) Genetic assignment of recruits reveals short and long distance larval dispersal in Pocillopora damicornis on the Great Barrier Reef. Mol Ecol 22:5821–5834.  https://doi.org/10.1111/mec.12539 CrossRefPubMedGoogle Scholar
  64. Vekemans X, Hardy OJ (2004) New insights from fine-scale spatial genetic structure analyses in plant populations. Mol Ecol 13:921–935.  https://doi.org/10.1046/j.1365-294X.2004.02076.x CrossRefPubMedGoogle Scholar
  65. Ward S (1992) Evidence for broadcast spawning as well as brooding in the scleractinian coral Pocillopora damicornis. Mar Biol 112:641–646.  https://doi.org/10.1007/BF00346182 CrossRefGoogle Scholar
  66. Weir B, Cockerham C (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370PubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.UMR ENTROPIE (Université de La Réunion, IRD, CNRS), Université de La Réunion, Faculté des Sciences et TechnologiesSt Denis Cedex 09France
  2. 2.UMR ENTROPIE (IRD, Université de La Réunion, CNRS), centre IRD de NouméaNouméaFrance
  3. 3.Université Côte d’Azur, CNRS, FRE, 3729 ECOMERS, Parc ValroseNiceFrance
  4. 4.Laboratoire d’excellence-CORAILPerpignanFrance

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