Abstract
Clonality and genetic structure of the coral Pocillopora damicornis sensu lato were assessed using five microsatellites in 12 populations from four islands of the Society Archipelago (French Polynesia) sampled in June 2008. The 427 analysed specimens fell into 132 multilocus genotypes (MLGs), suggesting that asexual reproduction plays an important role in the maintenance of these populations. A haploweb analysis of ITS2 sequences of each MLG was consistent with all of them being conspecific. Genetic differentiation was detected both between and within islands, but when a single sample per MLG was included in the analyses, the populations turned out to be nearly panmictic. These observations provide further evidence of the marked variability in reproductive strategies and genetic structure of P. damicornis throughout its geographic range; comparison with results previously obtained for the congeneric species Pocillopora meandrina underlines the importance of life history traits in shaping the genetic structure of coral populations.
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References
Adjeroud M, Tsuchiya M (1999) Genetic variation and clonal structure in the scleractinian coral Pocillopora damicornis in the Ryukyu Archipelago, southern Japan. Mar Biol 134:753–760
Adjeroud M, Chancerelle Y, Schrimm M, Perez T, Lecchini D, Galzin R, Salvat B (2005) Detecting the effects of natural disturbances on coral assemblages in French Polynesia: a decade survey at multiple scales. Aquat Living Resour 18:111–123
Adjeroud M, Michonneau F, Edmunds PJ, Chancerelle Y, Penin L, Vidal-Dupiol J, Salvat B, Galzin R (2009) Recurrent disturbances, recovery trajectories, and resilience of coral assemblages on a south Central Pacific reef. Coral Reefs 28:775–780
Almany GR, Connolly SR, Heath DD, Hogan JD, Jones GP, McCook LJ, Mills M, Pressey RL, Williamson DH (2009) Connectivity, biodiversity conservation and the design of marine reserve networks for coral reefs. Coral Reefs 28:339–351
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 7:15–17
Arnaud-Haond S, Duarte CM, Alberto F, Serrão EA (2007) Standardizing methods to address clonality in population studies. Mol Ecol 16:5115–5139
Arnaud-Haond S, Vonau V, Rouxel C, Bonhomme F, Prou J, Goyard E, Boudry P (2008) Genetic structure at different spatial scales in the pearl oyster (Pinctada margaritifera cumingii) in French Polynesian lagoons: beware of sampling strategy and genetic patchiness. Mar Biol 155:147–157
Ayre DJ, Hughes TP (2000) Genotypic diversity and gene flow in brooding and spawning corals along the Great Barrier Reef, Australia. Evolution 54:1590–1605
Ayre DJ, Miller KJ (2004) Where do clonal coral larvae go? Adult genotypic diversity conflicts with reproductive effort in the brooding coral Pocillopora damicornis. Mar Ecol Prog Ser 277:95–105
Ayre DJ, Willis BL (1988) Population structure in the coral Pavona cactus: clonal genotypes show little phenotypic plasticity. Mar Biol 99:495–505
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 159:175–187
Becheler R, Diekmann O, Hily C, Moalic Y, Arnaud-Haond S (2010) The concept of population in clonal organisms: mosaics of temporally colonized patches are forming highly diverse meadows of Zostera marina in Brittany. Mol Ecol 19:2394–2407
Belkhir K, Borsa P, Chikhi L, Raufaste N, Bonhomme F (1996) Genetix 4.05, Logiciel sous Windows pour la Génétique des Populations. Laboratoire Génome, Populations, Interactions, CNRS UMR 5000, Université de Montpellier II, Montpellier, France
Bell G (1982) The masterpiece of nature: the evolution and genetics of sexuality. Croon Helm, London
Bellwood DR, Hughes TP, Folke C, Nyström M (2004) Confronting the coral reef crisis. Nature 429:827–833
Bellwood DR, Hoey AS, Ackerman JL, Depczynski M (2006) Coral bleaching, reef fish community phase shifts and the resilience of coral reefs. Global Chang Biol 12:1587–1594
Benzie JAH, Haskell A, Lehman H (1995) Variation in the genetic composition of coral (Pocillopora damicornis and Acropora palifera) populations from different reef habitats. Mar Biol 121:731–739
Botsford LW, White JW, Coffroth MA, Paris CB, Planes S, Shearer TL, Thorrold SR, Jones GP (2009) Connectivity and resilience of coral reef metapopulations in marine protected areas: matching empirical efforts to predictive needs. Coral Reefs 28:327–337
Carlon DB (1999) The evolution of mating systems in tropical reef corals. Trends Ecol Evol 14:491–495
Combosch DJ, Vollmer SV (2011) Population genetics of an ecosystem-defining reef coral Pocillopora damicornis in the Tropical Eastern Pacific. PLoS One 6:e21200
David P, Berthou P, Noel P, Jarne P (1997) Patchy recruitment patterns in marine invertebrates: a spatial test of the density-dependent hypothesis in the bivalve Spisula ovalis. Oecologia 111:331–340
De Meeus T, Balloux F (2005) F-statistics of clonal diploids structured in numerous demes. Mol Ecol 14:2695–2702
Doyle JJ (1995) The irrelevance of allele tree topologies for species delimitation, and a non-topological alternative. Syst Bot 20:574–588
Duarte CM (2007) Marine ecology warms up to theory. Trends Ecol Evol 22:332–334
Elmhirst T, Connolly SR, Hughes TP (2009) Connectivity, regime shifts and resilience of coral reefs. Coral Reefs 28:949–957
Faurby S, Barber PH (2012) Theoretical limits to the correlation between pelagic larval duration and population genetic structure. Mol Ecol 21:3419–3432
Figueiredo J, Baird A, Cohen M, Flot J-F, Kamiki T, Meziane T, Tsuchiya M, Yamasaki H (2012) Ontogenetic change in the lipid and fatty acid composition of scleractinian coral larvae. Coral Reefs 31:613–619
Flot J-F (2007a) Towards a molecular taxonomy of corals of the genus Pocillopora. PhD Thesis, Muséum National d’Histoire Naturelle, Paris
Flot J-F (2007b) Champuru 1.0: a computer software for unraveling mixtures of two DNA sequences of unequal lengths. Mol Ecol Notes 7:974–977
Flot J-F (2010) SeqPHASE: a web tool for interconverting PHASE input/output files and FASTA sequence alignments. Mol Ecol Resour 10:162–166
Flot J-F, Tillier S (2006) Molecular phylogeny and systematics of the scleractinian coral genus Pocillopora in Hawaii. In: Proceedings of the 10th International Coral Reef Symposium, vol 1, p 24–29
Flot J-F, Tillier A, Samadi S, Tillier S (2006) Phase determination from direct sequencing of length-variable DNA regions. Mol Ecol Notes 6:627–630
Flot J-F, 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
Flot J-F, Couloux A, Tillier S (2010) Haplowebs as a graphical tool for delimiting species: a revival of Doyle’s “field for recombination” approach and its application to the coral genus Pocillopora in Clipperton. BMC Evol Biol 10:372
Fukami H, Budd AF, Levitan DR, Jara J, Kersanach R, Knowlton N (2004) Geographic differences in species boundaries among members of the Montastraea annularis complex based on molecular and morphological markers. Evolution 38:324–337
Gaffney PM, Scott TM, Koehn RK, Diehl WJ (1990) Interrelationships of heterozygosity, growth rate and heterozygote deficiencies in the coot clam, Mulina lateralis. Genetics 124:687–699
Gardner TA, Côté IM, Gill JA, Grant A, Watkinson AR (2003) Long-term region-wide declines in Caribbean corals. Science 301:958–960
Glynn PW, Gassman NJ, Eakin CM, Cortes J, Smith DB, Guzman HM (1991) Reef coral reproduction in the eastern Pacific: Costa Rica, Panama, and Galapagos Islands (Ecuador). I. Pocilloporidae. Mar Biol 109:355–368
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. doi:10.1111/mec.12335
Harii S, Yamamoto M, Hoegh-Guldberg O (2010) The relative contribution of dinoflagellate photosynthesis and stored lipids to the survivorship of symbiotic larvae of the reef-building corals. Mar Biol 157:1215–1224
Harrison PL (2011) Sexual reproduction of scleractinian corals. In: Dubinsky Z, Stambler N (eds) Coral reefs: an ecosystem in transition, Part 3. Springer, Berlin, pp 59–85
Hedgecock D, Barber PH, Edmands S (2007) Genetic approaches to measuring connectivity. Oceanography 20:70–79
Heyward AJ, Negri AP (2012) Turbulence, cleavage, and the naked embryo: a case for coral clones. Science 335:1064
Hoegh-Guldberg O (2009) Climate change and coral reefs: Trojan horse or false prophecy? Coral Reefs 28:569–575
Hoegh-Guldberg O, Mumby PJ, Hooten AJ, Steneck RS, Greenfield P, Gomez E, Harvell CD, Sale PF, Edwards AJ, Caldeira K, Knowlton N, Eakin CM, Iglesias-Prieto R, Muthiga N, Bradbury RH, Dubi A, Hatziolos ME (2007) Coral reefs under rapid climate change and ocean acidification. Science 318:1737–1742
Hughes TP, Baird AH, Bellwood DR, Card M, Connolly SR, Folke C, Grosberg R, Hoegh-Guldberg O, Jackson JBC, Kleypas J, Lough JM, Marshall P, Nyström M, Palumbi SR, Pandolfi JM, Rosen B, Roughgarden J (2003) Climate change, human impacts, and the resilience of coral reefs. Science 301:929–933
Hunter CL (1993) Genotypic variation and clonal structure in coral populations with different disturbance histories. Evolution 47:1213–1228
Johnson MS, Black R (1984) Pattern beneath the chaos: the effect of recruitment on genetic patchiness in an intertidal limpet. Evolution 38:1371–1383
Jones GP, Almany GR, Russ GR, Sale PF, Steneck RS, van Oppen MJH, Willis BL (2009) Larval retention and connectivity among populations of corals and reef fishes: history, advances and challenges. Coral Reefs 28:307–325
Lesser MP (2004) Experimental biology of coral reef ecosystems. J Exp Mar Biol Ecol 300:217–252
Magalon H, Samadi S, Richard M, Adjeroud M, Veuille M (2004) Development of coral and zooxanthella-specific microsatellites in three species of Pocillopora (Cnidaria, Scleractinia) from French Polynesia. Mol Ecol Notes 4:206–208
Magalon H, Adjeroud M, Veuille M (2005) Patterns of genetic variation do not correlate with geographical distance in the reef-building coral Pocillopora meandrina in the South Pacific. Mol Ecol 14:1861–1868
McManus JW, Polsenberg JF (2004) Coral-algal phase shifts on coral reefs: ecological and environmental aspects. Prog Oceanogr 60:263–279
Miller KJ, Ayre DJ (2008) Protection of genetic diversity and maintenance of connectivity among reef corals within marine protected areas. Conserv Biol 22:1245–1254
Moberg F, Folke C (1999) Ecological goods and services of coral reef ecosystems. Ecol Econ 29:215–233
Mora C, Andréfouët S, Costello MJ, Kranenburg C, Rollo A, Veron J, Gaston KJ, Myers RA (2006) Coral reefs and the global network of marine protected areas. Science 312:1750–1751
Nishikawa A, Katoh M, Sakai K (2003) Larval settlement rates and gene flow of broadcast-spawning (Acropora tenuis) and planula-brooding (Stylophora pistillata) corals. Mar Ecol Prog Ser 256:87–97
Nozawa Y, Harrison PL (2008) Temporal patterns of larval settlement and survivorship of two broadcast-spawning acroporid corals. Mar Biol 155:347–351
O’Connor MI, Bruno JF, Gaines SD, Halpern BS, Lester SE, Kinlan BP, Weiss JM (2007) Temperature control of larval dispersal and the implications for marine ecology, evolution, and conservation. Proc Natl Acad Sci USA 104:1266–1271
Palumbi SR (1994) Genetic divergence, reproductive isolation, and marine speciation. Annu Rev Ecol Syst 25:547–572
Pandolfi JM, Bradbury RH, Sala E, Hughes TH, Bjorndal KA, Cooke RG, McArdle D, McClenachan L, Newman MJH, Paredes G, Warner RR, Jackson JBC (2003) Global trajectories of the long-term decline of coral reef ecosystems. Science 301:955–958
Parsons KE (1996) The genetic effects of larval dispersal depend on spatial scale and habitat characteristics. Mar Biol 126:403–414
Paz-García DA, Chávez-Romo HE, Correa-Sandoval F, Reyes-Bonilla H, López-Pérez A, Medina-Rosas P, Hernández-Cortés MP (2012) Genetic connectivity patterns of corals Pocillopora damicornis and Porites panamensis (Anthozoa: Scleractinia) along the west coast of Mexico. Pac Sci 66:43–61
Pinzón JH, LaJeunesse TC (2011) Species delimitation of common reef corals in the genus Pocillopora using nucleotide sequence phylogenies, population genetics and symbiosis ecology. Mol Ecol 20:311–325
Pinzón JH, Reyes-Bonilla H, Baums IB, LaJeunesse TC (2012) Contrasting clonal structure among Pocillopora (Scleractinia) communities at two environmentally distinct sites in the Gulf of California. Coral Reefs 31:765–777
Richmond RH (1987) Energetics, competency, and long-distance dispersal of planula larvae of the coral Pocillopora damicornis. Mar Biol 93:527–533
Richmond RH, Jokiel PL (1984) Lunar periodicity in larva release in the reef coral Pocillopora damicornis at Enewetak and Hawaii. Bull Mar Sci 34:280–287
Riginos C, Douglas KE, Jin Y, Shanahan DF, Treml EA (2011) Effects of geography and life history traits on genetic differentiation in benthic marine fishes. Ecography 34:566–575
Sale PF, Cowen RK, Danilowicz BS, Jones GP, Kritzer JP, Lindeman KC, Planes S, Polunin NVC, Russ GR, Sadovy YJ, Steneck RS (2005) Critical science gaps impede use of no-take fishery reserves. Trends Ecol Evol 20:74–80
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(12):e50847
Schmidt-Roach S, Lundgren P, Miller K, Gerlach G, Noreen A, Andreakis N (2013) Assessing hidden species diversity in the coral Pocillopora damicornis from Eastern Australia. Coral Reefs 32:161–172
Selkoe KA, Toonen RJ (2011) Marine connectivity: a new look at pelagic larval duration and genetic metrics of dispersal. Mar Ecol Prog Ser 436:291–305
Selkoe KA, Watson JR, White C, Ben Horin T, Iachhei M, Mitarai S, Siegel DA, Gaines SD, Toonen RJ (2010) Taking the chaos out of genetic patchiness: seascape genetics reveals ecological and oceanographic drivers of genetic patterns in three temperate reef species. Mol Ecol 19:708–3726
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 25:7–18
Souter P (2010) Hidden genetic diversity in a key model species of coral. Mar Biol 157:875–885
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
Souter P, Willis BL, Bray LK, Caley MJ, Muirhead A, van Oppen MJH (2010) Location and disturbance affect population genetic structure in four coral species of the genus Acropora on the Great Barrier Reef. Mar Ecol Prog Ser 416:35–45
Starger CJ, Yeoh SSR, Dai CF, Baker AC, Desalle R (2008) Ten polymorphic STR loci in the cosmopolitan reef coral, Pocillopora damicornis. Mol Ecol Resour 8:619–621
Starger CJ, Barber PH, Ambariyanto, Baker AC (2010) The recovery of coral genetic diversity in the Sunda Strait following the 1883 eruption of Krakatau. Coral Reefs 29:547–565
Stephens M, Smith NJ, Donnelly P (2001) A new statistical method for haplotype reconstruction from population data. Am J Hum Genet 68:978–989
Stoddart JA (1983) Asexual production of planulae in the coral Pocillopora damicornis. Mar Biol 76:279–284
Stoddart JA (1984a) Genetic structure within populations of the coral Pocillopora damicornis. Mar Biol 81:19–30
Stoddart JA (1984b) Genetic differentiation amongst populations of the coral Pocillopora damicornis of southwestern Australia. Coral Reefs 3:149–156
Stoeckel S, Grange J, Fernández-Manjarres JF, Bilger I, Frascaria-Lacoste N, Mariette S (2006) Heterozygote excess in a self-incompatible and partially clonal forest tree species—Prunus avium L. Mol Ecol 15:2109–2118
Treml EA, Roberts JJ, Chao Y, Halpin PN, Possingham HP, Riginos C (2012) Reproductive output and duration of the pelagic larval stage determine seascape-wide connectivity of marine populations. Integr Comp Biol 52:525–537
Underwood JN, Smith LD, van Oppen MJH, Gilmour JP (2007) Multiple scales of genetic connectivity in a brooding coral on isolated reefs following catastrophic bleaching. Mol Ecol 16:771–784
Underwood JN, Smith LD, van Oppen MJH, Gilmour JP (2009) Ecologically relevant dispersal of corals on isolated reefs: implications for managing resilience. Ecol Appl 19:18–29
Veron JEN (2000) Corals of the world. The Australian Institute of Marine Science, Townsville
Veron JEN, Pichon M (1976) Scleractinia of Eastern Australia Part I. Australian Institute of Marine Science, Canberra
Weir B, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370
Whitaker K (2006) Genetic evidence for mixed modes of reproduction in the coral Pocillopora damicornis and its effect on population structure. Mar Ecol Prog Ser 306:115–124
Wilkinson C (2008) Status of coral reefs of the world: 2008. Global Coral Reef Monitoring Network and Reef and Rainforest Research Center, Townsville
Williams GC (1975) Sex and evolution. Princeton University Press, Princeton
Wright S (1950) Genetical structure of populations. Nature 166:247–249
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Some samples were collected with the help of Pauline Bosserelle from the CRIOBE USR 3278 CNRS-EPHE. The samples were genotyped at the IFR 119 “Montpellier Environnement Biodiversité”. We would particularly like to thank Marie-Thérèse Augé, Érick Desmarais, Frédérique Cerqueira and Nicolas Bierne for their help in data acquisition and analysis. This paper is a contribution to the ANR “ADACNI” (ANR-12-ADAP-0016).
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Communicated by C. Riginos.
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Adjeroud, M., Guérécheau, A., Vidal-Dupiol, J. et al. 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 (2014). https://doi.org/10.1007/s00227-013-2355-9
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DOI: https://doi.org/10.1007/s00227-013-2355-9