Abstract
Studying population genetic connectivity (i.e., identifying gene flow among populations and understanding their impacts on the genetic structure and diversity of populations) is first a matter of knowing what we work on, that is, accurately delimiting evolutionary units. Here, we focused on Pocillopora damicornis sensu stricto (or Pocillopora PSH04 sensu Gélin et al. in Mol Phylogenet Evol 109:430–446. http://dx.doi.org/10.1016/j.ympev.2017.01.018, 2017). From 458 colonies sampled within the tropical southwestern Pacific [Chesterfield Islands and New Caledonia (Grande Terre and Loyalty Islands)], Bayesian assignments and network analyses were conducted with 11-microsatellite loci to first evaluate the genetic partitioning of the colonies in distinct Secondary Species Hypotheses (SSHs), then in distinct clusters. Population genetic connectivity was then assessed for each cluster separately. Pocillopora PSH04 was partitioned into two highly differentiated SSHs (SSH04a and SSH04b), regularly found in sympatry. Furthermore, SSH04a was subdivided into two clusters (SSH04a-1 and SSH04a-2). This pattern of genetic structuring seems not related to clonality, but rather to the establishment of reproductive barriers. Nevertheless, considering each cluster separately, the populations appeared highly differentiated, suggesting relatively weak gene flow. This low connectivity among populations, coupled with the existence of cryptic species, brings new insights to the connectivity pattern of this understudied Pacific region.
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References
Alberto F, Gouveia L, Arnaud-Haond S, Pérez-Lloréns 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
Anderson EC, Thompson EA (2002) A model-based method for identifying species hybrids using multilocus genetic data. Genetics 160:1217–1229
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. https://doi.org/10.1111/j.1471-8286.2006.01522.x
Arnaud-Haond S, Duarte CM, Alberto F, Serrão 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
Arrigoni R, Berumen ML, Mariappan KG, Beck PSA, Hulver AM, Montano S, Pichon M, Strona G, Terraneo TI, Benzoni F (2020) Towards a rigorous species delimitation framework for scleractinian corals based on RAD sequencing: the case study of Leptastrea from the Indo-Pacific. Coral Reefs. https://doi.org/10.1007/s00338-020-01924-8
Balloux F, Lehmann L, de Meeûs T (2003) The population genetics of clonal and partially clonal diploids. Genetics 164:1635–1644
Baums IB, Miller MW, Hellberg ME (2006) Geographic variation in clonal structure in a reef-building Caribbean coral, Acropora palmata. Ecol Monogr 76:503–519. https://doi.org/10.1890/0012-9615(2006)076%5b0503:gvicsi%5d2.0.co;2
Bickford D, Lohman DJ, Sodhi NS, Ng PKL, Meier R, Winker K, Ingram KK, Das I (2007) Cryptic species as a window on diversity and conservation. Trends Ecol Evol 22:148–155. https://doi.org/10.1016/j.tree.2006.11.004
Bongaerts P, Riginos C, Ridgway T, Sampayo EM, van Oppen MJH, Englebert N, Vermeulen F, Hoegh-Guldberg O (2010) Genetic divergence across habitats in the widespread coral Seriatopora hystrix and its associated Symbiodinium. PLoS One 5:e10871. https://doi.org/10.1371/journal.pone.0010871
Boulay JN, Hellberg ME, Cortés J, Baums IB (2014) Unrecognized coral species diversity masks differences in functional ecology. Proc R Soc B Biol Sci 281:20131580. https://doi.org/10.1098/rspb.2013.1580
Bowen BW, Rocha LA, Toonen RJ, Karl SA (2013) The origins of tropical marine biodiversity. Trends Ecol Evol 28:359–366. https://doi.org/10.1016/j.tree.2013.01.018
Cowen RK, Sponaugle S (2009) Larval dispersal and marine population connectivity. Annu Rev Mar Sci 1:443–466. https://doi.org/10.1146/annurev.marine.010908.163757
Cowen RK, Gawarkiewicz G, Pineda J, Thorrold SR, Werner F (2003) Population connectivity in marine systems. Report of a workshop to develop science recommendations for the National Science Foundation. EOS Trans 84:119
Dorken ME, Eckert CG (2001) Severely reduced sexual reproduction in northern populations of a clonal plant, Decodon verticillatus (Lythraceae). J Ecol 89:339–350. https://doi.org/10.1046/j.1365-2745.2001.00558.x
Drechsler M, Frank K, Hanski I, O’Hara RB, Wissel C (2003) Ranking metapopulation extinction risk: from patterns in data to conservation management decisions. Ecol Appl 13:990–998. https://doi.org/10.1890/1051-0761(2003)13%5b990:rmerfp%5d2.0.co;2
Fišer C, Robinson CT, Malard F (2018) Cryptic species as a window into the paradigm shift of the species concept. Mol Ecol 27:613–635. https://doi.org/10.1111/mec.14486
Flot J-F, Licuanan WY, Nakano Y, Payri C, Cruaud C, Tillier S (2008) Mitochondrial sequences of Seriatopora corals show little agreement with morphology and reveal the duplication of a tRNA gene near the control region. Coral Reefs 27:789–794. https://doi.org/10.1007/s00338-008-0407-2
Forsman Z, Wellington GM, Fox GE, Toonen RJ (2015) Clues to unraveling the coral species problem: distinguishing species from geographic variation in Porites across the Pacific with molecular markers and microskeletal traits. PeerJ 3:e751. https://doi.org/10.7717/peerj.751
Gélin P, Postaire B, Fauvelot C, Magalon H (2017a) 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
Gélin P, Fauvelot C, Mehn V, Bureau S, Rouzé H, Magalon H (2017b) 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
Gélin P, Fauvelot C, Bigot L, Baly J, Magalon H (2018a) 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
Gélin P, Pirog A, Fauvelot C, Magalon H (2018b) 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. Mar Biol. https://doi.org/10.1007/s00227-018-3428-6
Goudet J (2001) FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9.3.2). http://www.unil.ch/izea/softwares/fstat.html
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
Harii S, Kayanne H, Takigawa H, Hayashibara T, Yamamoto M (2002) Larval survivorship, competency periods and settlement of two brooding corals, Heliopora coerulea and Pocillopora damicornis. Mar Biol 141:39–46. https://doi.org/10.1007/s00227-002-0812-y
Harrison PL (2011) Sexual reproduction of scleractinian corals. In: Dubinsky Z, Stambler N (eds) Coral reefs: an ecosystem in transition. Springer, Dordrecht, pp 59–85
Hatcher BG (1990) Coral reef primary productivity. A hierarchy of pattern and process. Trends Ecol Evol 5:149–155. https://doi.org/10.1016/0169-5347(90)90221-x
Highsmith RC (1982) Reproduction by fragmentation in corals. Mar Ecol Prog Ser 7:207–226. https://doi.org/10.3354/meps007207
Hughes TP, Bellwood DR, Baird AH, Brodie J, Bruno JF, Pandolfi JM (2011) Shifting base-lines, declining coral cover, and the erosion of reef resilience: comment on Sweatman et al. (2011). Coral Reefs 30:653–660. https://doi.org/10.1007/s00338-011-0787-6
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
Jost LOU (2008) GST and its relatives do not measure differentiation. Mol Ecol 17:4015–4026. https://doi.org/10.1111/j.1365-294x.2008.03887.x
Keenan K, McGinnity P, Cross TF, Crozier WW, Prodöhl PA (2013) Diversity: an r package for the estimation and exploration of population genetics parameters and their associated errors. Methods Ecol Evol 4:782–788. https://doi.org/10.1111/2041-210x.12067
Keshavmurthy S, Yang S-Y, Alamaru A, Chuang Y-Y, Pichon M, Obura D, Fontana S, De Palmas S, Stefani F, Benzoni F, MacDonald A, Noreen AME, Chen C, Wallace CC, Pillay RM, Denis V, Amri AY, Reimer JD, Mezaki T, Sheppard C, Loya Y, Abelson A, Mohammed MS, Baker AC, Mostafavi PG, Suharsono BA, Chen CA (2013) DNA barcoding reveals the coral “laboratory-rat”, Stylophora pistillata encompasses multiple identities. Sci Rep 3:1520. https://doi.org/10.1038/srep01520
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
Knowlton N (1993) Sibling species in the sea. Annu Rev Ecol Syst 24:189–216. https://doi.org/10.1146/annurev.es.24.110193.001201
Marti-Puig P, Forsman ZH, Haverkort-Yeh RD, Knapp IS, 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
Mayr E (1963) Animal species and evolution. Harvard University Press, Cambridge
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
Mills LS, Allendorf FW (1996) The one-migrant-per-generation rule in conservation and management. Conserv Biol 10:1509–1518. https://doi.org/10.1046/j.1523-1739.1996.10061509.x
Mönkkönen M, Reunanen P (1999) On critical thresholds in landscape connectivity: a management perspective. Oikos 84:302–305
Nakajima Y, Nishikawa A, Iguchi A, Nagata T, Uyeno D, Sakai K, Mitarai S (2017) Elucidating the multiple genetic lineages and population genetic structure of the brooding coral Seriatopora (Scleractinia: Pocilloporidae) in the Ryukyu Archipelago. Coral Reefs 36:415–426. https://doi.org/10.1007/s00338-017-1557-x
Palumbi SR (1992) Marine speciation on a small planet. Trends Ecol Evol 7:114–118. https://doi.org/10.1016/0169-5347(92)90144-z
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
Paulay G, Meyer C (2002) Diversification in the tropical Pacific: comparisons between marine and terrestrial systems and the importance of founder speciation. Integr Comp Biol 42:922–934. https://doi.org/10.1093/icb/42.5.922
Pinzón JH, Sampayo E, Cox E, Chauka LJ, Chen CA, Voolstra CR, LaJeunesse TC (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
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 130:361–368. https://doi.org/10.1007/s002270050256
Postaire B, Magalon H, Bourmaud CA-F, Bruggemann JH (2016) Molecular species delimitation methods and population genetics data reveal extensive lineage diversity and cryptic species in Aglaopheniidae (Hydrozoa). Mol Phylogenet Evol 105:36–49. https://doi.org/10.1016/j.ympev.2016.08.013
Postaire B, Gélin P, Bruggemann JH, Pratlong M, Magalon H (2017) Population differentiation or species formation across the Indian and the Pacific Oceans? An example from the brooding marine hydrozoan Macrorhynchia phoenicea. Ecol Evol 7:8170–8186. https://doi.org/10.1002/ece3.3236
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959
R Core Team (2016) r: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. https://www.R-project.org/
Raymond M, Rousset F (1995) GenePop: population genetics software for exact tests and ecumenism. J Hered 86:248–249. https://doi.org/10.1111/j.1558-5646.1995.tb04456.x
Richmond RH (1987) Energetics, competency, and long-distance dispersal of planula larvae of the coral Pocillopora damicornis. Mar Biol 93:527–533. https://doi.org/10.1007/bf00392790
Rousset F (2008) Genepop’007: a complete re-implementation of the genepop software for Windows and Linux. Mol Ecol Resour 8:103–106. https://doi.org/10.1111/j.1471-8286.2007.01931.x
Rozenfeld AF, Arnaud-Haond S, Hernández-García E, Eguíluz VM, Matías MA, Serrão E, Duarte CM (2007) Spectrum of genetic diversity and networks of clonal organisms. J R Soc Interface 4:1093–1102. https://doi.org/10.1098/rsif.2007.0230
Samadi S, Bottan L, Macpherson E, De Forges BR, Boisselier M-C (2006) Seamount endemism questioned by the geographic distribution and population genetic structure of marine invertebrates. Mar Biol 149:1463–1475. https://doi.org/10.1007/s00227-006-0306-4
Schmidt-Roach S, Lundgren P, Miller KJ, Gerlach G, Noreen AME, Andreakis N (2012a) 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
Schmidt-Roach S, Miller KJ, Woolsey E, Gerlach G, Baird AH (2012b) Broadcast spawning by Pocillopora species on the Great Barrier Reef. PLoS One 7:e50847. https://doi.org/10.1371/journal.pone.0050847
Schmidt-Roach S, Miller KJ, Lundgren P, Andreakis N (2014) 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
Serrano XM, Baums IB, Smith TB, Jones RJ, Shearer TL, Baker AC (2016) Long distance dispersal and vertical gene flow in the Caribbean brooding coral Porites astreoides. Sci Rep 6:21619. https://doi.org/10.1038/srep21619
Spalding MD, Fox HE, Allen GR, Davidson N, Ferdaña ZA, Finlayson MAX, Halpern BS, Jorge MA, Lombana AL, Lourie SA (2007) Marine ecoregions of the world: a bioregionalization of coastal and shelf areas. Bioscience 57:573–583. https://doi.org/10.1641/b570707
Stoddart JA (1983) Asexual production of planulae in the coral Pocillopora damicornis. Mar Biol 76:279–284. https://doi.org/10.1007/bf00393029
Sundqvist L, Keenan K, Zackrisson M, Prodöhl P, Kleinhans D (2016) Directional genetic differentiation and relative migration. Ecol Evol 6:3461–3475. https://doi.org/10.1002/ece3.2096
Thomas L, Kendrick GA, Stat M, Travaille KL, Shedrawi G, Kennington WJ (2014) Population genetic structure of the Pocillopora damicornis morphospecies along Ningaloo Reef, Western Australia. Mar Ecol Prog Ser 513:111–119. https://doi.org/10.3354/meps10893
Todd PA (2008) Morphological plasticity in scleractinian corals. Biol Rev 83:315–337. https://doi.org/10.1111/j.1469-185x.2008.00045.x
Torda G, Lundgren P, Willis BL, van Oppen MJH (2013a) 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
Torda G, Lundgren P, Willis BL, van Oppen MJH (2013b) Revisiting the connectivity puzzle of the common coral Pocillopora damicornis. Mol Ecol 22:5805–5820. https://doi.org/10.1111/mec.12540
van Oosterhout C, Hutchinson WF, Wills DP, Shipley P (2004) Micro-Checker: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538. https://doi.org/10.1111/j.1471-8286.2004.00684.x
van Oppen MJH, Bongaerts P, Underwood JN, Peplow LM, Cooper TF (2011) The role of deep reefs in shallow reef recovery: an assessment of vertical connectivity in a brooding coral from west and east Australia. Mol Ecol 20:1647–1660. https://doi.org/10.1111/j.1365-294x.2011.05050.x
Vega A, Marchesiello P, Lefêvre J (2006) Atlas hydrodynamique de la Zone Economique Exclusive de la Nouvelle-Calédonie. Laboratoire d’Etudes Géophysiques et d’Océanographie Spatiale, Nouméa, Nouvelle-Calédonie
Veron JEN (2000) Corals of the world. Australian Institute of Marine Science, Townsville
Warner PA, van Oppen MJH, Willis BL (2015) Unexpected cryptic species diversity in the widespread coral Seriatopora hystrix masks spatial-genetic patterns of connectivity. Mol Ecol 24:2993–3008. https://doi.org/10.1111/mec.13225
Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370. https://doi.org/10.1111/j.1558-5646.1984.tb05657.x
Wilkinson CR (2008) Status of coral reefs of the world: 2008. Global Coral Reef Monitoring Network and Reef and Rainforest Research Centre, Townsville
Wright S (1931) Evolution in Mendelian populations. Genetics 16:97–159
Zayasu Y, Nakajima Y, Sakai K, Suzuki G, Satoh N, Shinzato C (2016) Unexpectedly complex gradation of coral population structure in the Nansei Islands, Japan. Ecol Evol 6:5491–5505. https://doi.org/10.1002/ece3.2296
Acknowledgements
Coral sampling in New Caledonia (HM) was carried out during COBELO (http://dx.doi.org/10.17600/13100100), BIBELOT (http://dx.doi.org/10.17600/14003700), 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 the South of 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 Europa, Juan de Nova, and Glorioso Islands (HM) by program BIORECIE (financial supports from INEE, INSU, IRD, AAMP, FRB, TAAF, and the foundation Veolia Environnement); in Tromelin Island (HM) by program ORCIE (INEE), and in Mayotte (HM) by program SIREME (FED). HM thanks all the buddies who helped in photographs during diving (J. Butscher, S. Andréfouët, L. Bigot, and M. Pinault). We acknowledge the Plateforme Gentyane of the Institut National de la Recherche Agronomique (INRA, Clermont-Ferrand, France) for genotyping and technical support. PG and NO were respectively financially supported by PhD contracts from the LabEx CORAIL and the Doctoral School of Reunion Island University. We thank the reviewers for their comments to improve the manuscript.
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HM collected samples. NO, PG, and HM did lab steps and analysed the genotyping results. NO wrote the original draft and NO, PG, and HM reviewed and edited the manuscript.
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Oury, N., Gélin, P. & Magalon, H. Cryptic species and genetic connectivity among populations of the coral Pocillopora damicornis (Scleractinia) in the tropical southwestern Pacific. Mar Biol 167, 142 (2020). https://doi.org/10.1007/s00227-020-03757-z
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DOI: https://doi.org/10.1007/s00227-020-03757-z