Coral Reefs

, Volume 32, Issue 1, pp 161–172 | Cite as

Assessing hidden species diversity in the coral Pocillopora damicornis from Eastern Australia

  • S. Schmidt-Roach
  • P. Lundgren
  • K. J. Miller
  • G. Gerlach
  • A. M. E. Noreen
  • N. Andreakis
Report

Abstract

The incredible range of morphological plasticity present in scleractinian corals has confused the taxonomy of the group, prompting the introduction of “ecomorphs” to explain the observed correlation between local environmental conditions and phenotypic variation. Pocillopora damicornis (Linnaeus, 1758) represents one of the best known examples of eco-phenotypic variation in scleractinian corals with a variety of forms and reproductive strategies reported across its global distribution range. Here, we reconstruct genealogical relationships of P. damicornis colonies collected from thirteen locations along the East Australian coast to examine the relationship between genetic and phenotypic diversity in this species. Haplotype networks computed from two mitochondrial DNA regions (CR, ORF) indicate that the range of morphotypes observed within this taxon fall into at least five genetically distinct mitochondrial lineages. Nuclear (HSP70, ITS2) haplowebs on the other hand recover sharp genetic discontinuities among three of the morphological groups. We conclude that P. damicornis from Eastern Australia constitutes a cryptic species complex. The misinterpretation of taxonomical units within P. damicornis may well explain its perceived variation in the ecology, biology and life history across its range.

Keywords

Speciation Cryptic Ecomorphs Phylogeny GBR Reproduction 

Notes

Acknowledgments

The authors would like to thank C. C. Wallace, P. Muir and J. E. N. Veron for constructive criticism and advice and M. J. H. van Oppen for comments on the manuscript and for contributing some of the mitochondrial sequences used in the final analyses. We also thank L. Peplow, D. Abrego and J. Doyle for technical advice and support, and G. Torda and A. Baird for field assistance and N. Vogel for laboratory assistance. This work has been funded through the Commonwealth Environment Research Facilities (CERF) programme, an Australian Government initiative supporting world class, public good research. The CERF Marine Biodiversity Hub is a collaborative partnership between the University of Tasmania, CSIRO Wealth from Oceans Flagship, Geoscience Australia, Australian Institute of Marine Science and Museum Victoria. Additionally, this study was kindly supported by a research award from the Winifred Violet Scott Estate Trust. S.S-R is also supported by an Endeavour International Postgraduate Research Scholarship (EIPRS), CERF Marine Biodiversity Hub scholarship and a scholarship from the German Academic Exchange Service (DAAD). This paper represents the first part of the Ph.D. thesis of S.S-R.

Supplementary material

338_2012_959_MOESM1_ESM.eps (23.1 mb)
Supplementary material 1 Photos of colonies representing examples of each morphological group. Colony numbers of tropical individuals correspond to individuals sequenced (EPS 23698 kb)
338_2012_959_MOESM2_ESM.eps (780 kb)
Supplementary material 2 Haplotype network based on ORF DNA sequence data (n = 145, total alignment length = 593 bp) (EPS 779 kb)
338_2012_959_MOESM3_ESM.eps (820 kb)
Supplementary material 3 Haplotype network based on CR DNA sequence data (n = 37, total alignment length = 1266 bp) (EPS 820 kb)
338_2012_959_MOESM4_ESM.eps (176 kb)
Supplementary material 4 Left: DGGE of Symbiodinium ITS2; letters indicate diagnostic bands of each Symbiodinium type. Right: Table showing scoring results (EPS 176 kb)
338_2012_959_MOESM5_ESM.docx (20 kb)
Supplementary material 5 (DOCX 20 kb)
338_2012_959_MOESM6_ESM.docx (19 kb)
Supplementary material 6 (DOCX 18 kb)

References

  1. 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 277:95–105CrossRefGoogle Scholar
  2. Ayre DJ, Hughes TP, Standish RS (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
  3. Bandelt HJ, Forster P, Röhl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16:37–48PubMedCrossRefGoogle Scholar
  4. 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 121:731–739CrossRefGoogle Scholar
  5. 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 22:148–155PubMedCrossRefGoogle Scholar
  6. 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 5:10871CrossRefGoogle Scholar
  7. Bouwmeester J, Berumen M, Baird AH (2011) Daytime broadcast spawning of Pocillopora verrucosa on coral reefs of the central Red Sea. Galaxea 13:23–24CrossRefGoogle Scholar
  8. Brown D, Brenneman R, Koepfli K-P, Pollinger J, Mila B, Georgiadis N, Louis E, Grether G, Jacobs D, Wayne R (2007) Extensive population genetic structure in the giraffe. BMC Biol 5:57PubMedCrossRefGoogle Scholar
  9. Bruno JF, Edmunds PJ (1997) Clonal variation for phenotypic plasticity in the coral Madracis mirabilis. Ecology 78:2177–2190Google Scholar
  10. Combosch DJ, Vollmer SV (2011) Population genetics of an ecosystem-defining reef coral Pocillopora damicornis in the tropical Eastern Pacific. PLoS ONE 6:e21200PubMedCrossRefGoogle Scholar
  11. Combosch DJ, Guzman HM, Schuhmacher H, Vollmer SV (2008) Interspecific hybridization and restricted trans-Pacific gene flow in the Tropical Eastern Pacific Pocillopora. Mol Ecol 17:1304–1312PubMedCrossRefGoogle Scholar
  12. De Queiroz K (2007) Species concepts and species delimitation. Syst Biol 56:879–886PubMedCrossRefGoogle Scholar
  13. Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131:479–491PubMedGoogle Scholar
  14. Fiene-Severns P (1998) A note on synchronous spawning in the reef coral Pocillopora meandrina at Molokini Islet, Hawaii. Reproduction in Reef Corals. E. F. Cox, University of Hawaii. Technical Report No. 42Google Scholar
  15. Flot J-F (2007) Champuru 1.0: a computer software for unraveling mixtures of two DNA sequences of unequal lengths. Mol Ecol Notes 7:974–977CrossRefGoogle Scholar
  16. Flot J-F (2010) SeqPHASE: a web tool for interconverting PHASE input/output files and FASTA sequence alignments. Mol Ecol Resour 10:162–166PubMedCrossRefGoogle Scholar
  17. Flot J-F, Tillier S (2006) Molecular phylogeny and systematics of the scleractinian coral genus Pocillopora in Hawaii. Proc 10th Int Coral Reef Symp 1:24–29Google Scholar
  18. Flot J-F, Tillier S (2007) The mitochondrial genome of Pocillopora (Cnidaria: Scleractinia) contains two variable regions: The putative D-loop and a novel ORF of unknown function. Gene 401:80–87PubMedCrossRefGoogle Scholar
  19. Flot J-F, Tillier A, Samadi S, Tillier S (2006) Phase determination from direct sequencing of length-variable DNA regions. Mol Ecol Notes 6:627–630CrossRefGoogle Scholar
  20. 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. CR Biol 331:239–247CrossRefGoogle Scholar
  21. 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 10:372PubMedCrossRefGoogle Scholar
  22. Flot J-F, Blanchot J, Charpy L, Cruaud C, Licuanan W, Nakano Y, Payri C, Tillier S (2011) Incongruence between morphotypes and genetically delimited species in the coral genus Stylophora: phenotypic plasticity, morphological convergence, morphological stasis or interspecific hybridization? BMC Ecol 11:22PubMedCrossRefGoogle Scholar
  23. Forsman Z, Barshis D, Hunter C, Toonen R (2009) Shape-shifting corals: Molecular markers show morphology is evolutionarily plastic in Porites. BMC Evol Biol 9:45PubMedCrossRefGoogle Scholar
  24. Gloor GB, Preston CR, Johnson-Schlitz DM, Nassif NA, Phillis RW, Benz WK, Robertson HM, Engels WR (1993) Type I Repressors of P Element Mobility. Genetics 135:81–95PubMedGoogle Scholar
  25. 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). Mar Biol 109:355–368CrossRefGoogle Scholar
  26. Hall TA (1999) BioEdit: a user-friendly biological sequence alignment program for Windows 95/98/NT. Nucleic Acids Symp 41:95–98Google Scholar
  27. Harriott VJ (1983) Reproductive seasonality, settlement, and post-settlement mortality of Pocillopora damicornis (Linnaeus), at Lizard Island, Great Barrier Reef. Coral Reefs 2:151–157CrossRefGoogle Scholar
  28. Hellberg M (2006) No variation and low synonymous substitution rates in coral mtDNA despite high nuclear variation. BMC Evol Biol 6:24PubMedCrossRefGoogle Scholar
  29. Kruger A, Schleyer MH (1998) Sexual reproduction in the coral Pocillopora verrucosa (Cnidaria : Scleractinia) in KwaZulu-Natal, South Africa. Mar Biol 132:703–710CrossRefGoogle Scholar
  30. LaJeunesse TC (2002) Diversity and community structure of symbiotic dinoflagellates from Caribbean coral reefs. Mar Biol 141:387–400CrossRefGoogle Scholar
  31. LaJeunesse TC, Trench RK (2000) The biogeography of two species of Symbiodinium (Freudenthal) inhabiting the intertidal sea anemone, Anthopleura elegantissima (Brandt). Biol Bull 199:126–134PubMedCrossRefGoogle Scholar
  32. 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 284:147–161CrossRefGoogle Scholar
  33. Magalon H, Flot JF, Baudry E (2007) Molecular identification of symbiotic dinoflagellates in Pacific corals in the genus Pocillopora. Coral Reefs 26:551–558CrossRefGoogle Scholar
  34. Medina M, Weil E, Szmant AM (1999) Examination of the Montastrea annularis species complex (Cnidaria:Scleractinia) using ITS and COI sequences. Mar Biotechnol 1:89–97PubMedCrossRefGoogle Scholar
  35. Miller KJ (1994) Morphological variation in the coral genus Platygyra: environmental influences and taxonomic implication. Mar Ecol Prog Ser 110:19–28CrossRefGoogle Scholar
  36. Miller KJ, Ayre DJ (2004) The role of sexual and asexual reproduction in structuring high latitude populations of the reef coral Pocillopora damicornis. Heredity 92:557–568PubMedCrossRefGoogle Scholar
  37. Muir P (1984) Periodicity and asexual planulae production in Pocillopora damicornis (Linnaeus) at Magnetic Island. Honours Thesis, James Cook University, p60Google Scholar
  38. Nunes F, Fukami H, Vollmer S, Norris R, Knowlton N (2008) Re-evaluation of the systematics of the endemic corals of Brazil by molecular data. Coral Reefs 27:423–432CrossRefGoogle Scholar
  39. Peakall ROD, Smouse PE (2006) genalex 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295CrossRefGoogle Scholar
  40. Pinzón JH, LaJeunesse TC (2010) Species delimitation of common reef corals in the genus Pocillopora using nucleotide sequence phylogenies, population genetics and symbiosis ecology. Mol Ecol 20:311–325PubMedCrossRefGoogle Scholar
  41. Richmond RH, Jokiel PL (1984) Lunar periodicity in larva release in the reef coral Pocillopora damicornis at Enewetak and Hawaii. Bull Mar Sci 34:280–287Google Scholar
  42. Ridgway T, Hoegh-Guldberg O, Ayre DJ (2001) Panmixia in Pocillopora verrucosa from South Africa. Mar Biol 139:175–181CrossRefGoogle Scholar
  43. Ridgway T, Riginos C, Davis J, Hoegh-Guldberg O (2008) Genetic connectivity patterns of Pocillopora verrucosa in southern African Marine Protected Areas. Mar Ecol Prog Ser 354:161–168CrossRefGoogle Scholar
  44. Rieger TT, Oliveira-Silva SV, Pachêco IA, Chagas BS, Santos JF (2007) Localization of HSP single-copy genes by inexpensive, permanent non-fluorescent in situ hybridization on meiotic chromosomes of the grasshopper Schistocerca pallens (Acrididae). Genet Mol Res 6:643–649PubMedGoogle Scholar
  45. Roca AL, Georgiadis N, Pecon-Slattery J, O’Brien SJ (2001) Genetic evidence for two species of elephant in Africa. Science 293:1473–1477PubMedCrossRefGoogle Scholar
  46. Rosen S, Skaletsky H (2000) Primer3 on the WWW for general users and biologist programmers. In: Misener S, Krawetz SA (eds) Bioinformatics methods and protocols. Humana Press, Totowa, NJ, pp 365–386Google Scholar
  47. Rozas J, Sanchez-DelBarrio JC, Messeguer X, Rozas R (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19:2496–2497PubMedCrossRefGoogle Scholar
  48. Sampayo EM, Franceschinis L, Hoegh-Guldberg O, Dove S (2007) Niche partitioning of closely related symbiotic dinoflagellates. Mol Ecol 16:3721–3733PubMedCrossRefGoogle Scholar
  49. Schlichting CD (2002) Phenotypic plasticity in plants. Plant Species Biol 17:85–88CrossRefGoogle Scholar
  50. Shaish L, Abelson A, Rinkevich B (2007) How plastic can phenotypic plasticity be? The branching coral Stylophora pistillata as a model system. PLoS ONE 2:e644PubMedCrossRefGoogle Scholar
  51. Shearer TL, Van Oppen MJH, Romano SL, Worheide G (2002) Slow mitochondrial DNA sequence evolution in the Anthozoa (Cnidaria). Mol Ecol 11:2475–2487PubMedCrossRefGoogle Scholar
  52. 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
  53. Sier CJS, Olive PJW (1994) Reproduction and reproductive variability in the coral Pocillopora verrucosa from the Republic-of-Maldives. Mar Biol 118:713–722CrossRefGoogle Scholar
  54. Souter P (2010) Hidden genetic diversity in a key model species of coral. Mar Biol 157:875–885CrossRefGoogle Scholar
  55. Starger CJ, Yeoh SSR, Dai C, Baker AC, Desalle R (2008) Ten polymorphic STR loci in the cosmopolitan reef coral, Pocillopora damicornis. Mol Ecol Resour 8:619–621PubMedCrossRefGoogle Scholar
  56. Stefani F, Benzoni F, Yang SY, Pichon M, Galli P, Chen C (2011) Comparison of morphological and genetic analyses reveals cryptic divergence and morphological plasticity in Stylophora (Cnidaria, Scleractinia). Coral Reefs 30:1033–1049CrossRefGoogle Scholar
  57. Stimson JS (1978) Mode and timing of reproduction in some common hermatypic corals of Hawaii and Enewetak. Mar Biol 48:173–184CrossRefGoogle Scholar
  58. Stobart B, Benzie JAH (1994) Allozyme electrophoresis demonstrates that the scleractinian coral Montipora digitata is two species. Mar Biol 118:183–190CrossRefGoogle Scholar
  59. Stoddart JA, Black R (1985) Cycles of gametogenesis and planulation in the coral Pocillopora damicornis. Mar Ecol Prog Ser 23:153–164CrossRefGoogle Scholar
  60. Tanner JE (1996) Seasonality and lunar periodicity in the reproduction of pocilloporid corals. Coral Reefs 15:59–66Google Scholar
  61. Todd PA (2008) Morphological plasticity in scleractinian corals. Biol Rev Camb Philos Soc 83:315–337PubMedCrossRefGoogle Scholar
  62. 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 18:1315–1329PubMedCrossRefGoogle Scholar
  63. Veron JEN (1986) Corals of Australia and the Indo-Pacific. Angus and Robertson, SydneyGoogle Scholar
  64. Veron JEN (2000) Corals of the world. Australian Institute of Marine Science, Townsville, AustraliaGoogle Scholar
  65. Veron JEN, Pichon M (1976) Scleractinia of Eastern Australia, Monogr Ser Aust Inst Mar Sci IGoogle Scholar
  66. Villanueva RD, Yap HT, Montano MNE (2008) Timing of planulation by pocilloporid corals in the northwestern Philippines. Mar Ecol Prog Ser 370:111–119CrossRefGoogle Scholar
  67. Waits LP, Luikart G, Taberlet P (2001) Estimating the probability of identity among genotypes in natural populations: cautions and guidelines. Mol Ecol 10:249–256PubMedCrossRefGoogle Scholar
  68. Ward S (1992) Evidence for broadcast spawning as well as brooding in the Scleractinian coral Pocillopora damicornis. Mar Biol 112:641–646CrossRefGoogle Scholar
  69. Wicks LC, Sampayo E, Gardner JPA, Davy SK (2010) Local endemicity and high diversity characterise high-latitude coral–Symbiodinium partnerships. Coral Reefs 4:989–1003CrossRefGoogle Scholar
  70. Willis BL (1985) Phenotypic plasticity versus phenotypic stability in the reef corals Turbinaria mesenterina and Pavona cactus. Proc 5th Int Coral Reef Congr 4:107–112Google Scholar
  71. Willis BL, van Oppen MJH, Miller DJ, Vollmer SV, Ayre DJ (2006) The role of hybridization in the evolution of reef corals. Annu Rev Ecol Evol Syst 37:489–517CrossRefGoogle Scholar
  72. Yeoh SR, Dai CF (2010) The production of sexual and asexual larvae within single broods of the scleractinian coral, Pocillopora damicornis. Mar Biol 157:351–359CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2012

Authors and Affiliations

  • S. Schmidt-Roach
    • 1
    • 2
  • P. Lundgren
    • 2
    • 4
  • K. J. Miller
    • 1
  • G. Gerlach
    • 3
  • A. M. E. Noreen
    • 2
  • N. Andreakis
    • 2
  1. 1.Institute for Marine and Antarctic StudiesUniversity of TasmaniaHobarAustralia
  2. 2.Australian Institute of Marine ScienceTownsville MCAustralia
  3. 3.Fakultät V, Institut für BiologieCarl von Ossietzky Universität OldenburgOldenburgGermany
  4. 4.Great Barrier Reef Marine Park AuthorityTownsvilleAustralia

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