Skip to main content
SpringerLink
Log in

Genetic relationships of the hydrocoral Millepora alcicornis and its symbionts within and between locations across the Atlantic

  • Report
  • Published:
Coral Reefs Aims and scope Submit manuscript

Abstract

Although the hydrocoral Millepora alcicornis is a prominent and ecologically relevant amphi-Atlantic reef builder, little attention has been given to its endosymbionts which are also involved in the survival and adaptation success of the species in different environments. In this study, we resolve the genetic relationships between M. alcicornis and its symbionts (Symbiodiniaceae) within both sides and across the Atlantic. The COI and 16S-rDNA regions were selected for the host tissues, and the 23S-rDNA and ITS regions were chosen for the symbionts. Phylogenetic networks consistently showed that host populations from the eastern Atlantic archipelagos (Canary and Cape Verde Islands) were more related to western Atlantic populations than they were between them. However, results for Symbiodiniaceae species varied according to the molecular marker used. Samples from Mexico were grouped as Symbiodinium sp. (formerly Symbiodinium clade A) by both markers. Specimens from Puerto Rico were grouped as either Symbiodinium sp. or Breviolum sp. (formerly Symbiodinium clade B), according to the molecular marker used. Most samples from the eastern Atlantic were identified as Breviolum sp. by both markers, except for one sample from the Canary Islands and two samples from the Cape Verde Islands, which were identified as Cladocopium sp. (formerly Symbiodinium clade C) using ITS-rDNA. These results suggest that these two genera of Symbiodiniaceae may cohabit the same M. alcicornis colony. Because hydrocorals from the Canary Islands were phylogenetically related to the western Atlantic, but symbionts were more related to those of the Cape Verde Islands, the origin of the coral and its symbionts is probably different. This may be explained either by “horizontal” transmission, i.e. acquisition from the environment, or by a change in the dominant symbiont composition within the host. The flexibility of this hydrocoral to select symbionts, depending on environmental conditions, can provide new insight to understand how this coral may face ongoing climate change.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

References

  • Amaral FMD, Steiner AQ, Broadhurst MK, Cairns SD (2008) An overview of the shallow-water calcified hydroids from Brazil (Hydrozoa: Cnidaria), including the description of a new species. Zootaxa 56–68

  • Apprill AM, Gates RD (2007) Recognizing diversity in coral symbiotic dinoflagellate communities: Fast-track article. Mol Ecol 16:1127–1134

    Article  CAS  PubMed  Google Scholar 

  • Arif C, Daniels C, Bayer T, Banguera-Hinestroza E, Barbrook A, Howe CJ, LaJeunesse TC, Voolstra CR (2014) Assessing Symbiodinium diversity in scleractinian corals via next-generation sequencing-based genotyping of the ITS2 rDNA region. Mol Ecol 23:4418–4433

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Baker AC (2003) Flexibility and specificity in coral-algal symbiosis: Diversity, ecology, and biogeography of Symbiodinium. Annu Rev Ecol Evol Syst 34:661–689

    Article  Google Scholar 

  • Baker AC, Starger CJ, McClanahan T, Glynn P (2004) Corals’ adaptive response to climate change. Nature 7001

  • Banaszak AT, LaJeunesse TC, Trench RK (2000) The synthesis of mycosporine-like amino acids (MAAS) by cultured, symbiotic dinoflagellates. J Exp Mar Bio Ecol 249:219–233

    Article  CAS  Google Scholar 

  • Berkelmans R, van Oppen MJH (2006) The role of zooxanthellae in the thermal tolerance of corals: a “nugget of hope” for coral reefs in an era of climate change. Proc Biol Sci 273:2305–2312

    Article  PubMed  PubMed Central  Google Scholar 

  • Bertelsen E, Ussing H (1936) Marine tropical animals carried to the Copenhagen Sydhavn on a ship from the Bermudas. Dansk Naturhistorisk Foren i Kjobenharn Vidensk Meddelelser 100:237–245

    Google Scholar 

  • Boschma H (1948) Specific characters in Millepora. Proc K Ned Akad Wet 51:818–823

    Google Scholar 

  • Brito A, Falcón JM, Herrera R (2005) Sobre la tropicalización reciente de la ictiofauna litoral de las islas Canarias y su relación con cambios ambientales y actividades antrópicas. Vieraea 33:515–526

    Google Scholar 

  • Buddemeier RW, Kleypas JA, Aronson RB (2004) Coral reef ecosystems and global climate change: potential contributions of climate change to stresses on coral reef ecosystems. Pew Cent Glob Clim Chang 10

  • Byler KA, Carmi-Veal M, Fine M, Goulet TL (2013) Multiple symbiont acquisition strategies as an adaptive mechanism in the coral Stylophora pistillata. PLoS One 8:e59596

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Casado-Amezúa P, Machordom A, Bernardo J, González-Wangüemert M (2014) New insights into the genetic diversity of zooxanthellae in Mediterranean anthozoans. Symbiosis 63:41–46

    Article  Google Scholar 

  • Casado-Amezúa P, Terrón-Sigler A, Pinzón JH, Furla P, Forcioli D, Allemand D, Ribes M, Coma R (2016) General ecological aspects of Anthozoan-Symbiodinium interactions in the Mediterranean Sea. In: Goffredo S, Dubinsky Z (eds) The Cnidaria, past, present and future: the world of medusa and her sisters. Springer International Publishing, Cham, pp 375–386

    Chapter  Google Scholar 

  • Castresana J (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 17:540–552

    Article  CAS  PubMed  Google Scholar 

  • Clemente S, Rodríguez A, Brito A, Ramos A, Monterroso Ó, Hernández JC (2010) On the occurrence of the hydrocoral Millepora (Hydrozoa: Milleporidae) in the subtropical eastern Atlantic (Canary Islands): is the colonization related to climatic events? Coral Reefs 30:237–240

    Article  Google Scholar 

  • Coffroth MA, Poland DM, Petrou EL, Brazeau DA, Holmberg JC (2010) Environmental symbiont acquisition may not be the solution to warming seas for reef-building corals. PLoS One 5:e13258

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Coffroth MA, Santos SR (2005) Genetic diversity of symbiotic dinoflagellates in the genus Symbiodinium. Protist 156:19–34

    Article  CAS  PubMed  Google Scholar 

  • Coffroth MA, Santos SR, Goulet TL (2001) Early ontogenetic expression of specificity in a cnidarian-algal symbiosis. Mar Ecol Prog Ser 222:85–96

    Article  Google Scholar 

  • Costa CF, Sassi R, Gorlach-Lira K, LaJeunesse TC, Fitt WK (2013) Seasonal changes in zooxanthellae harbored by zoanthids (Cnidaria, Zoanthidea) from coastal reefs in northeastern Brazil. Panam J Aquat Sci 8:253–264

    Google Scholar 

  • Cunningham CW, Buss LW (1993) Molecular evidence for multiple episodes of paedomorphosis in the family Hydractiniidae. Biochem Syst Ecol 21:57–69

    Article  CAS  Google Scholar 

  • Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and high- performance computing. Nat Methods 9:772

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Davy SK, Allemand D, Weis VM (2012) Cell biology of Cnidarian-Dinoflagellate symbiosis. Microbiol Mol Biol Rev 76:229–261

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • de Palmas S, Denis V, Ribas-Deulofeu L, Loubeyres M, Woo S, Hwang SJ, Song JI, Chen CA (2015) Symbiodinium spp. associated with high-latitude scleractinian corals from Jeju Island. South Korea. Coral Reefs 34:919–925

    Article  Google Scholar 

  • de Souza JN, Nunes FLD, Zilberberg C, Sanchez Ja, Migotto AE, Hoeksema BW, Serrano XM, Baker AC, Lindner A (2017) Contrasting patterns of connectivity among endemic and widespread fire coral species (Millepora spp.) in the tropical Southwestern Atlantic. Coral Reefs 36:701

    Google Scholar 

  • de Vienne DM, Giraud T, Martin OC (2007) A congruence index for testing topological similarity between trees. Bioinformatics 23:3119–3124

    Article  CAS  PubMed  Google Scholar 

  • de Weerdt WH (1984) Taxonomic characters in Caribbean Millepora species (Hydrozoa, Coelenterata). Bijdr Dierk 54:243–255

    Article  Google Scholar 

  • de Weerdt WH, Glynn PW (1991) A new and presumably now extinct species of Millepora (Hydrozoa) in the eastern Pacific. Zool Med Leiden 65:267–276

    Google Scholar 

  • Díaz-Almeyda EM, Prada C, Ohdera AH, Moran H, Civitello DJ, Iglesias-Prieto R, Carlo TA, LaJeunesse TC, Medina M (2017) Intraspecific and interspecific variation in thermotolerance and photoacclimation in Symbiodinium dinoflagellates. Proc R Soc B Biol Sci 284:20171767

    Article  CAS  Google Scholar 

  • Fay SA, Weber MX (2012) The occurrence of mixed infections of Symbiodinium (Dinoflagellata) within individual hosts. J Phycol 48:1306–1316

    Article  PubMed  Google Scholar 

  • Faye S, Lazar A, Sow BA, Gaye AT (2015) A model study of the seasonality of sea surface temperature and circulation in the Atlantic North-eastern Tropical Upwelling System. Front Phys 3:1–20

    Article  Google Scholar 

  • Finney JC, Pettay DT, Sampayo EM, Warner ME, Oxenford HA, LaJeunesse TC (2010) The relative significance of host-habitat, depth, and geography on the ecology, endemism, and speciation of coral endosymbionts in the genus Symbiodinium. Microb Ecol 60:250–263

    Article  PubMed  Google Scholar 

  • Gates RD (1990) Seawater temperature and sublethal coral bleaching in Jamaica. Coral Reefs 8:193–197

    Article  Google Scholar 

  • González-Delgado S, López C, Brito A, Clemente S (2018) Marine community effects of two colonial zoanthids in intertidal habitats of the Canary Islands. Reg Stud Mar Sci

  • Goulet TL (2006) Most corals may not change their symbionts. Mar Ecol Prog Ser 321:1–7

    Article  Google Scholar 

  • Goulet TL (2007) Most scleractinian corals and octocorals host a single symbiotic zooxanthella clade Mar. Ecol Prog Ser 335:243–248

    Article  Google Scholar 

  • Goulet TL, Coffroth MA (2003) Genetic composition of zooxanthellae between and within colonies of the octocoral Plexaura kuna, based on small subunit rDNA and multilocus DNA fingerprinting. Mar Biol 142:233–239

    Article  CAS  Google Scholar 

  • Govindarajan AF, Halanych KM, Cunningham CW (2005) Mitochondrial evolution and phylogeography in the hydrozoan Obelia geniculata (Cnidaria). Mar Biol 146:213–222

    Article  CAS  Google Scholar 

  • Graham NAJ, Nash KL (2013) The importance of structural complexity in coral reef ecosystems. Coral Reefs 32:315–326

    Article  Google Scholar 

  • Grajales A, Sanchez JA (2016) Holobiont assemblages of dominant coral species (Symbiodinium types and coral species) shape Caribbean reef community structure. Rev Acad Colomb Cienc Exact Fís Nat 40:300–311

    Article  Google Scholar 

  • Greenstein BJ, Pandolfi JM (2008) Escaping the heat: range shifts of reef coral taxa in coastal Western Australia. Glob Chang Biol 14:513–528

    Article  Google Scholar 

  • Grégoire V, Schmacka F, Coffroth MA, Karsten U (2017) Photophysiological and thermal tolerance of various genotypes of the coral endosymbiont Symbiodinium sp. (Dinophyceae). J Appl Phycol 29:1893–1905

    Article  Google Scholar 

  • Hansen G, Daugbjerg N (2009) Symbiodinium natans SP. Nov.: A “free-living” dinoflagellate from Tenerife (northeast-atlantic ocean). J Phycol 45:251–263

    Article  PubMed  Google Scholar 

  • Hickson SJ (1899) The meduse of Millepora. Proc R Soc London 66:3–10

    Google Scholar 

  • Hirose M, Kinzie R, Hidaka M (2001) Timing and process of entry of zooxanthellae into oocytes of hermatypic corals. Coral Reefs 20:273–280

    Article  Google Scholar 

  • Hoegh-Guldberg O, Mumby PJ, Hooten AJ, Steneck S, Greenfield P, Gomez E, Harvell CD, Sale PF, Edwards AJ, Caldeira K, Knowlton N, Eakin CM, Iglesias-Prieto R, Muthiga N, Bradbury RH, Dubi AM, Hatziolos E (2007) Coral reefs under rapid climate change and ocean acidification. Science 318:1737–1742

    Article  CAS  PubMed  Google Scholar 

  • Hoeksema BW, Nunes FLD, Lindner A, De Souza JN (2017) Millepora alcicornis (Hydrozoa: Capitata) at Ascension Island: confirmed identity base on morphological and molecular analyses. J Mar Biol Assoc UK 97:709–712

    Article  Google Scholar 

  • Hunter C, Morden C, Smith C (1997) among Zooxanthellae and corals. Proc 8th Int Coral Reef Symp 2:1599–1602

  • Iglesias-Prieto R, Beltrán VH, LaJeunesse TC, Reyes-Bonilla H, Thomé PE (2004) Different algal symbionts explain the vertical distribution of dominant reef corals in the eastern Pacific. ProcBiol Sci 271:1757–1763

    CAS  Google Scholar 

  • Kemp DW, Thornhill DJ, Rotjan RD, Iglesias-Prieto R, Fitt WK, Schmidt GW (2015) Spatially distinct and regionally endemic Symbiodinium assemblages in the threatened Caribbean reef-building coral Orbicella faveolata. Coral Reefs 34:535–547

    Article  Google Scholar 

  • Kumar S, Stecher G, Tamura K (2016) MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets. Mol Biol Evol 33:1870–1874

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kunihiro S, Reimer JD (2018) Phylogenetic analyses of Symbiodinium isolated from Waminoa and their anthozoan hosts in the Ryukyu Archipelago, southern Japan. Symbiosis 1–12

  • Laborel J (1974) West African reef corals: an hypothesis on their origin. Proc 2nd Int Coral Reef Symp 1:425–443

  • LaJeunesse TC (2001) Investigating the biodiversity, ecology, and phylogeny of endosymbiotic dinoflagellates in the genus Symbiodinium using the ITS region: In search of a “species” level marker. J Phycol 37:866–880

    Article  CAS  Google Scholar 

  • LaJeunesse TC (2002) Diversity and community structure of symbiotic dinoflagellates from Caribbean coral reefs. Mar Biol 141:387–400

    Article  Google Scholar 

  • LaJeunesse TC (2005) “Species” radiations of symbiotic dinoflagellates in the Atlantic and Indo-Pacific since the Miocene-Pliocene transition. Mol Biol Evol 22:570–581

    Article  CAS  PubMed  Google Scholar 

  • LaJeunesse TC, Trench RK (2000) Biogeography of two species of Symbiodinium (Freudenthal) inhabiting the intertidal sea anemone Anthopleura elegantissima (Brandt). Biol Bull 199:126–134

    Article  CAS  PubMed  Google Scholar 

  • LaJeunesse TC, Loh WKW, van Woesik R, Hoegh-Guldberg O, Schmidt GW, Fitt WK (2003) Low symbiont diversity in southern Great Barrier Reef corals relative to those of the Caribbean. Limnol Oceanogr 48:2046–2054

    Article  Google Scholar 

  • LaJeunesse TC, Bhagooli R, Hidaka M, DeVantier L, Done T, Schmidt GW, Fitt WK, Hoegh-Guldberg O (2004) Closely related Symbiodinium spp. differ in relative dominance in coral reef host communities across environmental, latitudinal and biogeographic gradients. Mar Ecol Prog Ser 284:147–161

    Article  Google Scholar 

  • LaJeunesse TC, Pettay DT, Sampayo EM, Phongsuwan N, Brown B, Obura DO, Hoegh-Guldberg O, Fitt WK (2010) Long-standing environmental conditions, geographic isolation and host-symbiont specificity influence the relative ecological dominance and genetic diversification of coral endosymbionts in the genus Symbiodinium. J Biogeogr 37:785–800

    Article  Google Scholar 

  • LaJeunesse TC, Parkinson JE, Reimer JD (2012) A genetics-based description of Symbiodinium minutum sp. nov. and S. psygmophilum sp. nov. (dinophyceae), two dinoflagellates symbiotic with cnidaria. J Phycol 48:1380–1391

    Article  PubMed  Google Scholar 

  • LaJeunesse TC, Parkinson JE, Gabrielson PW, Jeong HJ, Reimer JD, Voolstra CR, Santos SR (2018) Systematic revision of symbiodiniaceae highlights the antiquity and diversity of coral endosymbionts. Curr Biol 28:2570–2580

    Article  CAS  PubMed  Google Scholar 

  • Lewis JB (1989) The ecology of Millepora. Coral Reefs 8:99–107

    Article  Google Scholar 

  • Lewis JB (2006) Biology and ecology of the hydrocoral Millepora on coral reefs. Adv Mar Biol 50:1–55

    Article  PubMed  Google Scholar 

  • Lien Y-T, Fukami H, Yamashita Y (2012) Symbiodinium clade C dominates zooxanthellate corals (Scleractinia) in the temperate region of Japan. Zool Stud 29:173–180

    Google Scholar 

  • Linnaeus C (1758) Systema naturae per regna tria naturae, secundum classes, ordines, genera, species, cum characteribus, differentiis, synonymis, locis, vol 1, 10th edn. Laurentii Salvii, Holmiae, p 824

    Google Scholar 

  • López C, Clemente S, Almeida C, Brito A, Hernández M (2015) A genetic approach to the origin of Millepora sp. in the eastern Atlantic. Coral Reefs 34:631–638

    Article  Google Scholar 

  • Mayer AG (1910) Medusae of the world: the hydromedusae. Carnegie institution of Washington

  • Mangan J (1909) The entry of zooxanthellae into the ovum of Millepora, and some particulars concerning the medusae. J Cell Sci 2:697–710

    Google Scholar 

  • Mieog JC, Olsen JL, Berkelmans R, Bleuler-Martinez SA, Willis BL, van Oppen MJH (2009) The roles and interactions of symbiont, host and environment in defining coral fitness. PLoS One 4:e6364

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Monteiro JG, Costa CF, Gorlach-Lira K, Fitt WK, Stefanni SS, Sassi R, Santos RS, LaJeunesse TC (2013) Ecological and biogeographic implications of Siderastrea symbiotic relationship with Symbiodinium sp. C46 in Sal Island (Cape Verde, East Atlantic Ocean). Mar Biodivers 43:261–272

    Article  Google Scholar 

  • Nitschke MR, Davy SK, Ward S (2016) Horizontal transmission of Symbiodinium cells between adult and juvenile corals is aided by benthic sediment. Coral Reefs 35:335–344

    Article  Google Scholar 

  • Ortiz-González IC, Rivera-Vicéns RE, Schizas NV (2017) De novo transcriptome assembly of the hydrocoral Millepora alcicornis (branching fire coral) from the Caribbean. Mar Genomics 32:27–30

    Article  Google Scholar 

  • Parkinson JE, Banaszak AT, Altman NS, LaJeunesse TC, Baums IB (2015) Intraspecific diversity among partners drives functional variation in coral symbioses. Sci Rep 5:1–12

    Article  CAS  Google Scholar 

  • Parkinson JE, Baums IB (2014) The extended phenotypes of marine symbioses: Ecological and evolutionary consequences of intraspecific genetic diversity in coral-algal associations. Front Microbiol 5:1–19

    Article  Google Scholar 

  • Pettay DT, Wham DC, Pinzón JH, LaJeunesse TC (2011) Genotypic diversity and spatial-temporal distribution of Symbiodinium clones in an abundant reef coral. Mol Ecol 20:5197–5212

    Article  PubMed  PubMed Central  Google Scholar 

  • Picciani N, de Lossio e Seiblitz IG, de Paiva PC, e Castro CB, Zilberberg C (2016) Geographic patterns of Symbiodinium diversity associated with the coral Mussismilia hispida (Cnidaria, Scleractinia) correlate with major reef regions in the Southwestern Atlantic Ocean. Mar Biol 163:1–11

    Article  Google Scholar 

  • Pinzón JH, Devlin-Durante MK, Weber MX, Baums IB, LaJeunesse TC (2011) Microsatellite loci for Symbiodinium A3 (S. fitti) a common algal symbiont among Caribbean Acropora (stony corals) and Indo-Pacific giant clams (Tridacna). Conserv Genet Resour 3:45–47

    Article  Google Scholar 

  • Rambaut A (2009) FigTree tree figure drawing tool. version 1.4.2. Available at http://tree.bio.ed.ac. uk/software/figtree/

  • Razak TB, Hoeksema BW (2003) The hydrocoral genus Millepora (Hydrozoa: Capitata: Milleporidae) in Indonesia. Zool Verh 345:313–336

    Google Scholar 

  • Reimer JD, Hirose M, Wirtz P (2010a) Zoanthids of the Cape Verde Islands and their symbionts: previously unexamined diversity in the Northeastern Atlantic. 79:147–163

  • Reimer JD, Lorion J, Irei Y, Hoeksema BW, Wirtz P (2017) Ascension Island shallow-water Zoantharia (Hexacorallia: Cnidaria) and their zooxanthellae (Symbiodinium). J Mar Biol Assoc United Kingdom 97(4):695–703

    Article  CAS  Google Scholar 

  • Reimer JD, Shah MMR, Sinniger F, Yanagi K, Suda S (2010b) Preliminary analyses of cultured Symbiodinium isolated from sand in the oceanic Ogasawara Islands, Japan. Mar Biodivers 40:237–247

    Article  Google Scholar 

  • Reynolds JM, Bruns BU, Fitt WK, Schmidt GW (2008) Enhanced photoprotection pathways in symbiotic dinoflagellates of shallow-water corals and other cnidarians. Proc Natl Acad Sci USA105:13674–13678

  • Rodriguez-Lanetty M (2003) Evolving lineages of Symbiodinium-like dinoflagellates based on ITS1 rDNA. Mol Phylogenet Evol 28:152–168

    Article  CAS  PubMed  Google Scholar 

  • Rodriguez-Lanetty M, Hoegh-Guldberg O (2003) Symbiont diversity within the widespread scleractinian coral Plesiastrea versipora, across the northwestern Pacific. Mar Biol 143:501–509

    Article  Google Scholar 

  • Ronquist F, Teslenko M, Van Der Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP (2012) Mrbayes 3.2: Efficient bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61:539–542

    Article  PubMed  PubMed Central  Google Scholar 

  • Rowan R, Knowlton N (1995) Intraspecific diversity and ecological zonation in coral-algal symbiosis. Proc Natl Acad Sci 92:2850–2853

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ruiz-Ramos DV (2009) Morphological and genetic variation in the Caribbean species of the hydrocoral genus Millepora. Diss. MS thesis in Marine Sciences, University of Puerto Rico, Mayagüez

  • Ruiz-Ramos DV, Weil E, Schizas NV (2014) Morphological and genetic evaluation of the hydrocoral Millepora species complex in the Caribbean. Zool Stud 53:4

    Article  CAS  Google Scholar 

  • Sampayo EM, Dove S, Lajeunesse TC (2009) Cohesive molecular genetic data delineate species diversity in the dinoflagellate genus Symbiodinium. Mol Ecol 18:500–519

    Article  CAS  PubMed  Google Scholar 

  • Sampayo EM, Ridgway T, Franceschinis L, Roff G, Hoegh-Guldberg O, Dove S (2016) Coral symbioses under prolonged environmental change: living near tolerance range limits. Sci Rep 6:36271

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Santos SR, Taylor DJ, Coffroth MA (2001) Genetic comparisons of freshly isolated versus cultured symbiotic dinoflagellates: implications for extrapolating to the intact symbiosis. J Phycol 37:900–912

    Article  CAS  Google Scholar 

  • Santos SR, Taylor DJ, Kinzie RA, Hidaka M, Sakai K, Coffroth MA (2002) Molecular phylogeny of symbiotic dinoflagellates inferred from partial chloroplast large subunit (23S)-rDNA sequences. Mol Phylogenet Evol 23:97–111

    Article  CAS  PubMed  Google Scholar 

  • Schwarz G (1978) Estimating the dimension of a model. Ann Stat 6:461–464

    Article  Google Scholar 

  • Shinzato C, Inoue M, Kusakabe M (2014) A snapshot of a coral “holobiont”: A transcriptome assembly of the scleractinian coral, Porites, captures a wide variety of genes from both the host and symbiotic zooxanthellae. PLoS One 9:e85182

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Silverstein RN, Correa AMS, LaJeunesse TC, Baker AC (2011) Novel algal symbiont (Symbiodinium spp.) diversity in reef corals of Western Australia. Mar Ecol Prog Ser 422:63–75

    Article  Google Scholar 

  • Srividhya S, Chellaram C (2012) Role of marine life in nanomedicine. Indian J Innov Dev 1:31–33

    Google Scholar 

  • Stat M, Bird CE, Pochon X, Chasqui L, Chauka LJ, Concepcion GT, Logan D, Takabayashi M, Toonen RJ, Gates RD (2011) Variation in Symbiodinium ITS2 sequence assemblages among coral colonies. PLoS One 6:e15854

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stat M, Carter D, Hoegh-Guldberg O (2006) The evolutionary history of Symbiodinium and scleractinian hosts-Symbiosis, diversity, and the effect of climate change. Perspect Plant Ecol Evol Syst 8:23–43

    Article  Google Scholar 

  • Stat M, Loh WKW, Hoegh-Guldberg O, Carter DA (2008) Symbiont acquisition strategy drives host-symbiont associations in the southern Great Barrier Reef. Coral Reefs 27:763–772

    Article  Google Scholar 

  • Takama O, Fernandez-Silva I, López C, Reimer JD (2018) Molecular phylogeny demonstrates the need for taxonomic reconsideration of species diversity of the hydrocoral genus Millepora (Cnidaria: Hydrozoa) in the Pacific. Zoolog Sci 35:123–133

    Article  CAS  PubMed  Google Scholar 

  • Takishita K, Ishikura M, Koike K, Maruyama T (2003) Comparison of phylogenies based on nuclear-encoded SSU rDNA and plastid-encoded psbA in the symbiotic dinoflagellate genus Symbiodinium. Phycologia 42:285–291

    Article  Google Scholar 

  • Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thornhill DJ, Kemp DW, Bruns BU, Fitt WK, Schmidt GW (2008) Correspondence between cold tolerance and temperate biogeography in a western Atlantic Symbiodinium (Dinophyta) lineage. J Phycol 44:1126–1135

    Article  CAS  PubMed  Google Scholar 

  • Thornhill DJ, LaJeunesse TC, Kemp DW, Fitt WK, Schmidt GW (2006) Multi-year, seasonal genotypic surveys of coral-algal symbioses reveal prevalent stability or post-bleaching reversion. Mar Biol 148:711–722

    Article  Google Scholar 

  • Thornhill DJ, Xiang Y, Pettay DT, Zhong M, Santos SR (2013) Population genetic data of a model symbiotic cnidarian system reveal remarkable symbiotic specificity and vectored introductions across ocean basins. Mol Ecol 22:4499–4515

    Article  CAS  PubMed  Google Scholar 

  • Toller WW, Rowan R, Knowlton N (2001) Repopulation of zooxanthellae in the Caribbean corals Montastraea annularis and M. faveolata following experimental and disease-associated bleaching. Biol Bull 201:360–373

    Article  CAS  PubMed  Google Scholar 

  • Van Oppen MJH, McDonald BJ, Willis B, Miller DJ (2001) The evolutionary history of the coral genus Acropora (Scleractinia, Cnidaria) based on a mitochondrial and a nuclear marker: reticulation, incomplete lineage sorting, or morphological convergence? Mol Biol Evol 18:1315–1329

    Article  PubMed  Google Scholar 

  • van Oppen MJ, Baker AC, Coffroth MA, Willis BL (2009) Bleaching resistance and the role of algal endosymbionts. Coral bleaching. Ecological Studies. Berlin, Heidelberg, pp 83–102

  • Vargas-Ángel B, Thomas JD, Hoke SM (2003) High-latitude Acropora cervicornis thickets off Fort Lauderdale, Florida, USA. Coral Reefs 22:465–473

    Article  Google Scholar 

  • Visram S, Wiedenmann J, Douglas AE (2006) Molecular diversity of symbiotic algae of the genus Symbiodinium (Zooxanthellae) in cnidarians of the Mediterranean Sea. J Mar Biol Assoc UK 86:1281–1283

    Article  CAS  Google Scholar 

  • Vollmer SV, Palumbi SR (2004) Testing the utility of internally transcribed spacer sequences in coral phylogenetics. Mol Ecol 13:2763–2772

    Article  CAS  PubMed  Google Scholar 

  • Wahle CM (1980) Detection, pursuit, and overgrowth of tropical gorgonians by milleporid hydrocorals: Perseus and Medusa revisited. Science (80-) 209:689–691

  • Warner ME, Chilcoat GC, McFarland FK, Fitt WK (2002) Seasonal fluctuations in the photosynthetic capacity of photosystem II in symbiotic dinoflagellates in the Caribbean reef-building coral Montastraea. Mar Biol 141:31–38

    Article  CAS  Google Scholar 

  • Weis V, Reynolds W, deBoer M, Krupp D (2001) Host-symbiont specificity during onset of symbiosis between the dinoflagellates Symbiodinium spp. and planula larvae of the scleractinian coral Fungia scutaria. Coral Reefs 20:301–308

    Article  Google Scholar 

  • Wilcox TP (1998) Large-subunit ribosomal RNA systematics of symbiotic dinoflagellates: morphology does not recapitulate phylogeny. Mol Phylogenet Evol 10:436–448

    Article  CAS  PubMed  Google Scholar 

  • Yamano H, Sugihara K, Nomura K (2011) Rapid poleward range expansion of tropical reef corals in response to rising sea surface temperatures. Geophys Res Lett 38

  • Yang YA, Soong K, Chen CA (2000) Seasonal variation in symbiont community composition within single colonies of Acropora palifera. Proc 9th Int Coral Reef Symp Bali 1:37

  • Yellowlees D, Rees TAV, Leggat W (2008) Metabolic interactions between algal symbionts and invertebrate hosts. Plant, Cell Environ 31:679–694

    Article  CAS  Google Scholar 

  • Zheng L, He J, Lin Y, Cao W, Zhang W (2014) 16S rRNA is a better choice than COI for DNA barcoding hydrozoans in the coastal waters of China. Acta Oceanol Sin 33:55–76

    Article  CAS  Google Scholar 

Download references

Acknowledgments

L. Rodríguez was supported by a FPU fellowship (Formación del Profesorado Universitario) from the Spanish Ministry of Education, Culture and Sports (Ref AP2012-3702). The Agencia Canaria de Investigación, Innovación y Sociedad de la Información de la Consejería de Economía, Industria, Comercio y Conocimiento (ACIISI) and Fondo Social Europeo (FSE) Programa Operativo Integrado de Canarias 2014–2020, Eje 3 Tema Prioritario 74 (85%) supported C. López. The research was also supported by the Systematics Research Fund (SRF) award from the Linnean Society and the Systematics Association. In México, the research was supported by UNAM-ICML Project Number 608. We want to thank the laboratory assistance from Anais Redruello, Sandra Sacristan and Lidia Plaza (URJC), and we thank Dr. Luis Parmenio Suescún and Dr. Patricia Thomé for sharing laboratory equipment and scientific advice during the work developed in Mexico (UNAM). We thank Ingrid C. Ortiz González, Dr. Nikolaos V. Schizas and the Department of Marine Sciences at the University of Puerto Rico, and Mayagüez for their support and laboratory assistance in Puerto Rico.

Author information

Authors and Affiliations

  1. Departamento de Biología y Geología, Física y Química Inorgánica, Universidad Rey Juan Carlos, c/Tulipán sn, Móstoles, 28933, Madrid, Spain

    Laura Rodríguez, Brezo Martínez & Alfredo García-Fernández

  2. Departamento de Biología Animal, Edafología y Geología, Universidad de La Laguna (ULL), Tenerife, Spain

    Cataixa López

  3. EU-US Marine Biodiversity Research Group. Life Sciences Department, University of Alcalá, Alcalá de Henares, Spain

    Pilar Casado-Amezua

  4. School of Natural Sciences, University of California, Merced, CA, 95343, USA

    Dannise V. Ruiz-Ramos

  5. Unidad Académica de Sistemas Arrecifales, Puerto Morelos, Instituto de Ciencias del Mar y Limnología, Universidad Nacional Autónoma de México, Mexico, Mexico

    Anastazia Banaszak

  6. IU-ECOAQUA, Grupo en Biodiversidad y Conservación, Universidad de Las Palmas de Gran Canaria, Canary Islands, 35017, Las Palmas de G.C, Spain

    Fernando Tuya

  7. Departamento de Bioquímica, Microbiología, Biología Celular y Genética, Instituto Universitario de Enfermedades Tropicales y Salud Pública de Canarias, Universidad de La Laguna, San Cristóbal de La Laguna, Tenerife, Spain

    Mariano Hernández

Authors
  1. Laura Rodríguez
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Cataixa López
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Pilar Casado-Amezua
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Dannise V. Ruiz-Ramos
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Brezo Martínez
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Anastazia Banaszak
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Fernando Tuya
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Alfredo García-Fernández
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Mariano Hernández
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Cataixa López.

Ethics declarations

Conflict of interest

On behalf of all authors, the corresponding author states that there is no conflict of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Topic Editor Morgan S. Pratchett

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 436 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Rodríguez, L., López, C., Casado-Amezua, P. et al. Genetic relationships of the hydrocoral Millepora alcicornis and its symbionts within and between locations across the Atlantic. Coral Reefs 38, 255–268 (2019). https://doi.org/10.1007/s00338-019-01772-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00338-019-01772-1

Keywords

Search

Navigation