Abstract
While Faviidae is a widely and uniformly distributed coral family throughout the Indo-Pacific, the extensive phenotypic plasticity of colony surface and corallite features often confounds the use of macromorphological characters in species identification, and contributes to conflict between traditional classification and molecular analyses of the group. Recent advances in morphological and molecular techniques now provide a suite of methods to re-address coral taxonomy in complex groups, such as that represented by the Faviidae. This study combines morphologic measurements including “3D coordinates landmarks” data with phylogenetic assessments of nuclear (ITS) and mitochondrial (COI-trnM) DNA to assess species boundaries in nine species of Faviidae with para-septothecal walls from Thailand. Strong concordance was found between morphological features and a priori groupings based on both morphospecies and genetically defined groups (ITS and COI-trnM). Favia truncatus was the most well-defined species based on morphological analyses, and it was also shown to be monophyletic using phylogenetic analyses. Besides F. truncatus, the only other species that was found to be monophyletic in analyses of both genes was F. cf. helianthoides, but its skeletal morphology overlapped with the F. favus species complex (comprised of F. favus, F. speciosa, F. matthaii and F. rotumana). Although not genetically monophyletic, the F. favus species complex and F. pallida were fairly well delineated morphologically. Morphospecies within the F. favus species complex are therefore possibly a result of genetic drift and/or stable polymorphisms driven by divergent selection. These results represent a first step toward a taxonomic revision of the Indo-Pacific Favia, which will integrate morphological methods with the study of type material, genetic information, reproductive data, and tests of phenotypic plasticity—given that multiple lines of evidence are needed to resolve ambiguous species and assign species names.
References
Anderson MJ, Willis TJ (2003) Canonical analysis of principal coordinates: A useful method of constrained ordination for ecology. Ecology 84:511–525
Anderson MJ, Gorley RN, Clarke KR (2008) PERMANOVA+ for PRIMER: Guide to Software and Statistical Methods. PRIMER-E, Plymouth, UK
Benzoni F, Stefani F, Pichon M, Galli P (2010) The name game: morpho-molecular species boundaries in the genus Psammocora (Cnidaria, Scleractinia). Zool J Linn Soc 160:421–456
Borel Best M, Boekschoten GJ, Oosterbaan A (1984) Species concept and ecomorph variation in living and fossil scleractinia. Palaeontogr Am 54:70–79
Budd AF (1984) The species concept in fossil hermatypic corals: A statistical approach. Palaeontogr Am 54:58–69
Budd AF, Klaus JS (2001) The origin and early evolution of the Montastraea “annularis” species complex (Anthozoa : Scleractinia). J Paleontol 75:527–545
Budd AF, Pandolfi JM (2010) Evolutionary novelty is concentrated at the edge of coral species distributions. Science 328:1558–1561
Budd AF, Stolarski J (2009) Searching for new morphological characters in the systematics of scleractinian reef corals: comparison of septal teeth and granules between Atlantic and Pacific Mussidae. Acta Zool 90:142–165
Budd AF, Stolarski J (2011) Corallite wall and septal microstructure in scleractinian reef corals: Comparison of molecular clades within the family Faviidae. J Morphol 272:66–88
Budd AF, Johnson KG, Potts DC (1994) Recognizing morphospecies in colonial reef corals: I. Landmark-based methods. Paleobiology 20:484–505
Cairns SD (1999) Species richness of recent Scleractinia. Atoll Res Bull 459:1–46
Carlon DB, Budd AF (2002) Incipient speciation across a depth gradient in a scleractinian coral? Evolution 56:2227–2242
De Queiroz K (2007) Species concepts and species delimitation. Syst Biol 56:879–886
Diekmann OE, Bak RPM, Stam WT, Olsen JL (2001) Molecular genetic evidence for probable reticulate speciation in the coral genus Madracis from a Caribbean fringing reef slope. Mar Biol 139:221–233
Ditlev H (1976) Stony corals (Coelenterata: Scleractinia) from the west coast of Thailand. Phuket Mar Biological Center Research Bulletin 13:1–14
Flot JF, Tillier S (2006) Molecular phylogeny and systematics of the scleractinian coral genus Pocillopora in Hawaii. Proc 10th Int Coral Reef Symp 1:24–29
Flot JF, 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
Forsman ZH, Barshis DJ, Hunter CL, Toonen RJ (2009) Shape-shifting corals: Molecular markers show morphology is evolutionarily plastic in Porites. BMC Evol Biol 9:45
Frade PR, Reyes-Nivia MC, Faria J, Kaandorp JA, Luttikhuizen PC, Bak RPM (2010) Semi-permeable species boundaries in the coral genus Madracis: Introgression in a brooding coral system. Mol Phylogenet Evol 57:1072–1090
Fukami H, Budd AF, Levitan DR, Jara J, Kersanach R, Knowlton N (2004a) Geographic differences in species boundaries among members of the Montastraea annularis complex based on molecular and morphological markers. Evolution 58:324–337
Fukami H, Budd AF, Paulay G, Sole-Cava A, Chen CLA, Iwao K, Knowlton N (2004b) Conventional taxonomy obscures deep divergence between Pacific and Atlantic corals. Nature 427:832–835
Fukami H, Chen CA, Budd AF, Collins A, Wallace C, Chuang YY, Chen C, Dai CF, Iwao K, Sheppard C, Knowlton N (2008) Mitochondrial and nuclear genes suggest that stony corals are monophyletic but most families of stony corals are not (Order Scleractinia, Class Anthozoa, Phylum Cnidaria). PLoS ONE 3(9):e3222. doi:10.1371/journal.pone.0003222
Hatta M, Fukami H, Wang WQ, Omori M, Shimoike K, Hayashibara T, Ina Y, Sugiyama T (1999) Reproductive and genetic evidence for a reticulate evolutionary history of mass-spawning corals. Mol Biol Evol 16:1607–1613
Hey J, Nielsen R (2004) Multilocus methods for estimating population sizes, migration rates and divergence time, with applications to the divergence of Drosophila pseudoobscura and D. persimilis. Genetics 167:747–760
Huang DW, Meier R, Todd PA, Chou LM (2009) More evidence for pervasive paraphyly in scleractinian corals: Systematic study of Southeast Asian Faviidae (Cnidaria; Scleractinia) based on molecular and morphological data. Mol Phylogenet Evol 50:102–116
Huang DW, Licuanan WY, Baird AH, Fukami H (2011) Cleaning up the ‘Bigmessidae’: Molecular phylogeny of scleractinian corals from Faviidae, Merulinidae, Pectiniidae and Trachyphylliidae. BMC Evol Biol 11:11–37. doi:10.1186/1471-2148-1111-1137
Hubbard JAEB, Pocock YP (1972) Sediment rejection by recent scleractinian corals: a key to paleoenvironmental reconstruction. Geol Rundsch 61:598–626
Kongjandtre N (2004) Species distribution and population structure of faviid corals (Scleractinia: Faviidae) on coral reefs in the Gulf of Thailand. M.Sc. Thesis, Burapha University, p 203
Kongjandtre N, Ridgway T, Ward S, Hoegh-Guldberg O (2010) Broadcast spawning patterns of Favia species on the inshore reefs of Thailand. Coral Reefs 29:227–234
Lam K, Morton B (2003) Morphological and ITS1, 5.8S, and partial ITS2 ribosomal DNA sequence distinctions between two species Playtygyra (Cnidaria: scleractinia) from Hong Kong. Mar Biotechnol 5:555–567
Lang JC (1984) Whatever works: The variable importance of skeletal and of non-skeletal characters in scleractinian taxonomy. Palaeontogr Am 54:18–44
Levitan DR, Fukami H, Jara J, Kline D, McGovern TM, McGhee KE, Swanson CA, Knowlton N (2004) Mechanisms of reproductive isolation among sympatric broadcast-spawning corals of the Montastraea annularis species complex. Evolution 58:308–323
Mallet J (1995) A species definition for the modern synthesis. Trends Ecol Evol 10:294–299
Mangubhai S, Souter P, Grahn M (2007) Phenotypic variation in the coral Platygyra daedalea in Kenya: morphometry and genetics. Mar Ecol-Prog Ser 345:105–115
Mayden RL (2002) On biological species, species concepts and individuation in the natural world. Fish Fish (Oxford) 3:171–196
Michener CD (1970) Diverse approaches to systematics. Evol Biol 4:1–38
Miller K, Babcock R (1997) Conflicting morphological and reproductive species boundaries in the coral genus Platygyra. Biol Bull 192:98–110
Ow YX, Todd PA (2010) Light-induced morphological plasticity in the scleractinian coral Goniastrea pectinata and its functional significance. Coral Reefs 29:797–808
Pandolfi JM (1996) Limited membership in Pleistocene reef coral assemblages from the Huon Peninsula, Papua New Guinea: Constancy during global change. Paleobiology 22:152–176
Pandolfi JM, Budd AF (2008) Morphology and ecological zonation of Caribbean reef corals: the Montastraea ‘annularis’ species complex. Mar Ecol-Prog Ser 369:89–102
Phongsuwan N (1986) Taxonomic study of scleractinian corals (Coelenterata-Anthozoa), with notes on structure and condition of reefs in the Adang-Rawi Island group, Tarutao National Park, southern Thailand. MSc thesis, Prince of Songkla University, p 262
Rambaut A (1996) Se-Al: Sequence Alignment Editor. http://evolve.zoo.ox.ac.uk/
Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574
Rosen DE (1979) Fishes from the uplands and intermontane basins of Guatemala: Revisionary studies and comparative geography. Bull Am Mus Nat Hist 162:267–376
Sakai K, Yeemin T, Snidvongs A, Yamazato K, Nishihara M (1986) Distribution and community structure of hermatypic corals in the Sichang Islands, inner part of the Gulf of Thailand. Galaxea 5:27–74
Seutin G, White BN, Boag PT (1991) Preservation of Avian blood and tissue samples for DNA analyses. Can J Zool-Rev Can Zool 69:82–90
Sites JW, Marshall JC (2004) Operational criteria for delimiting species. Annual Review of Ecology Evolution and Systematics 35:199–227
Sokal RR, Crovello TJ (1970) The biological species concept: A critical evaluation. Am Nat 104:127–153
Stefani F, Benzoni F, Pichon M, Mitta G, Galli P (2008a) Genetic and morphometric evidence for unresolved species boundaries in the coral genus Psammocora (Cnidaria; Scleractinia). Hydrobiologia 596:153–172
Stefani F, Benzoni F, Pichon M, Cancelliere C, Galli P (2008b) A multidisciplinary approach to the definition of species boundaries in branching species of the coral genus Psammocora (Cnidaria, Scleractinia). Zool Scr 37:71–91
Stobart B (2000) A taxonomic reappraisal of Montipora digitata based on genetic and morphometric evidence. Zool Stud 39:179–190
Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599
Tel-Zur N, Abbo S, Myslabodski D, Mizrahi Y (1999) Modified CTAB procedure for DNA isolation from epiphytic cacti of the genera Hylocereus and Selenicereus (Cactaceae). Plant Molecular Biology Reporter 17:249–254
Todd PA (2008) Morphological plasticity in scleractinian corals. Biol Rev 83:315–337
Todd PA, Sidle RC, Lewin-Koh NJI (2004a) An aquarium experiment for identifying the physical factors inducing morphological change in two massive scleractinian corals. J Exp Mar Biol Ecol 299:97–113
Todd PA, Ladle RJ, Lewin-Koh NJI, Chou LM (2004b) Genotype x environment interactions in transplanted clones of the massive corals Favia speciosa and Diploastrea heliopora. Mar Ecol-Prog Ser 271:167–182
van Oppen MJH, Willis BL, Van Vugt H, Miller DJ (2000) Examination of species boundaries in the Acropora cervicornis group (Scleractinia, Cnidaria) using nuclear DNA sequence analyses. Mol Ecol 9:1363–1373
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
van Oppen MJH, Willis BL, Van Rheede T, Miller DJ (2002) Spawning times, reproductive compatibilities and genetic structuring in the Acropora aspera group: evidence for natural hybridization and semi-permeable species boundaries in corals. Mol Ecol 11:1363–1376
Veron JEN (2000) Corals of the world. Aust Inst Mar Sci, Townsville
Veron JEN (2002) New species described in Corals of the World. Australian Institute of Marine Science, Townsville, Australia
Veron JEN, Pichon M, Wijsman-Best M (1977) Scleractinia of Eastern Australia. Part II. Families Faviidae, Trachyphylliidae. Aust Inst Mar Sci Monogr Ser 3:1–233
Vollmer SV, Palumbi SR (2002) Hybridization and the evolution of reef coral diversity. Science 296:2023–2025
Vollmer SV, Palumbi SR (2004) Testing the utility of internally transcribed spacer sequences in coral phylogenetics. Mol Ecol 13:2763–2772
Wallace C (1999) Staghorn corals of the world: A revision of the genus Acropora. CSIRO Publishing, Collingwood, VIC, Australia
Wallace CC, Willis BL (1994) Systematics of the coral genus Acropora: implications of new biological findings for species concepts. Annu Rev Ecol Syst 25:237–262
Weil E, Knowlton N (1994) A multi-character analysis of the Caribbean coral Montastraea annularis (Ellis and Solander, 1786) and its 2 sibling species, M. faveolata (Ellis and Solander, 1786) and M. franksi (Gregory, 1895). Bull Mar Sci 55:151–175
Wells JW (1956) Scleractinia. In: Moore RC (ed) Treatise on Invertebrate Paleontology. Geological Society of America and University of Kansas Press, Lawrence, pp F328–F444
Wijsman-Best M (1972) Systematics and ecology of New Caledonian Faviinae (Coelenterata - Scleractinia). Bijdragen Dierkunde 42
Wijsman-Best M (1974a) Habitat-induced modification of reef corals (Faviidae) and its consequences for taxanomy. Proc 2nd Int Coral Reef Symp 2:217–228
Wijsman-Best M (1974b) Biological results of the Snellius the expedition : XXV. Faviidae collected by Snellius expedition. I. The genus Favia. Zoologische Mededelingen 48:249–261
Wiley EO (1978) The evolutionary species concept reconsidered. Syst Zool 27:17–26
Willis BL, van Oppen MJH, Miller DJ, Vollmer SV, Ayre DJ (2006) The role of hybridization in the evolution of reef corals. Annual Review of Ecology Evolution and Systematics 37:489–517
Wolstenholme JK, Wallace CC, Chen CA (2003) Species boundaries within the Acropora humilis species group (Cnidaria; Scleractinia): a morphological and molecular interpretation of evolution. Coral Reefs 22:155–166
Yabe H, Sugiyama T, Eguchi M (1936) Recent reef-building corals from Japan and the South Sea islands under the Japanese mandate. Science reports of the Tohoku Imperial University 2nd series, Geology, special volume 1:1–66
Acknowledgments
The authors thank three anonymous reviewers for their comprehensive and constructive comments that have improved the quality of the manuscript. PhD scholarship to NK was supported by the Royal Thai Government. Research funding provided by the Coral Reef Targeted Research Project (www.gefcoral.org) and the ARC Centre of Excellence for Coral Reef Studies to OHG (www.coralreefecosystems.org). Field observations and logistical support provided by the Marine and Coastal Resources Research Centre, the Phuket Marine Biological Centre, Faculty of Science Burapha University, Aquatic Resources Research Institute Chulalongkorn University and King Mongkut’s Institute of Technology Chumphon campus. We thank Prof. John Pandolfi for permission to use the Reflex microscope at The University of Queensland.
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Kongjandtre, N., Ridgway, T., Cook, L.G. et al. Taxonomy and species boundaries in the coral genus Favia Milne Edwards and Haime, 1857 (Cnidaria: Scleractinia) from Thailand revealed by morphological and genetic data. Coral Reefs 31, 581–601 (2012). https://doi.org/10.1007/s00338-011-0869-5
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DOI: https://doi.org/10.1007/s00338-011-0869-5