Abstract
One of the key issues in coral evolutionary biology is the significance of interspecific hybridisation in shaping modern reef corals. Despite this, few detailed studies of speciation and evolution exist for scleractinians. We examined molecular relationships among 25 species of the species-rich scleractinian genus Montipora sampled from Irian Jaya (Indonesia) and Magnetic Island (central Great Barrier Reef) using a nuclear and mitochondrial marker. Mitochondrial DNA (mtDNA) haplotypes are shared among several species and at least four species are not monophyletic based on the nuclear intron sequences. Moreover, although the mtDNA and nuclear trees have similar topologies, there are several important inconsistencies. These results, in combination with the observation of simultaneous spawning of and in vitro cross-fertility between some Montipora species, suggest that occasional gene exchange through interspecific hybridisation occurs between a small number of species in this coral genus. Little correlation was observed between morphological and molecular relationships.
Similar content being viewed by others
References
Adachi J, Hasegawa M (1996) MolPhy version 2.3: programs for molecular phylogenetics based on maximum likelihood. (Comp Sci Monogr 28) Institute of Statistical Mathematics, Tokyo
Ayre DJ, Veron JEN, Dufty SL (1991) The corals Acropora palifera and Acropora cuneata are genetically and ecologically distinct. Mar Biol 10:13–18
Babcock RC, Bull GD, Harrison PL, Heyward AJ, Oliver JK, Wallace CC, Willis BL (1986) Synchronous spawning of 105 coral species on the Great Barrier Reef. Mar Biol 90:379–394
Babcock RC, Willis BL, Simpson CJ (1994) Mass spawning of corals on a high latitude coral reef. Mar Biol 13:161–169
Budd AF, Johnson KG (1999) Origination preceding extinction during late Cenozoic turnover of Caribbean reefs. Paleobiology 25:188–200
Budd AF, Stemann TA, Johnson KG (1994) Stratigraphic distributions of genera and species of Neogene to recent Caribbean reef corals. J Paleontol 68:951–977
Callaerts P, Halder G, Gehring WJ (1997) Pax-6 in development and evolution. Annu Rev Neurosci 20:483–532
Catmull J, Hayward DC, McIntyre NE, Reece-Hoyes JS, Mastro R, Callaerts P, Ball EE, Miller DJ (1998) Pax-6 origins—implications from the structure of two coral Pax genes. Dev Genes Evol 208:352–356
Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1660
Coll JC, Bowden BF, Meehan GV, Konig GM, Carroll AR, Tapiolas DM, Alino PM, Heaton A, Nys RD (1994) Chemical aspects of mass spawning in corals 1. Sperm-attractant molecules in the eggs of the scleractinian coral Montipora digitata. Mar Biol 118:177–182
de Graaf M, Geertjes GJ, Videler JJ (1999) Observations on spawning of scleractinian corals and other invertebrates on the reefs of Bonaire (Netherlands Antilles, Caribbean). Bull Mar Sci 64:189–194
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
Frost SH (1977) Oligocene reef coral biogeography, Caribbean and western Tethys. Bull Res Geol Miniers Mem 89:342–352
Fukami H, Omori M, Hatta M (2000) Phylogenetic relationships in the coral family Acroporidae, reassessed by inference from mitochondrial genes. Zool Sci 17:689–696
Gardner JPA (1997) Hybridization in the sea. Adv Mar Biol 31:1–78
Garthwaite RL, Potts DC, Veron JEN, Done TJ (1994) Electrophoretic identification of poritid species (Anthozoa: Scleractinia). Coral Reefs 13:49–56
Gregory JW, Trench JB (1916) Eocene corals from the Fly River, New Guinea. Geol Mag 6:481–488, 529–536
Guest JR, Baird AH, Goh BPL (2002) Multispecific, synchronous coral spawning in Singapore. Coral Reefs 21:422–423
Harrison PL, Babcock RC, Bull GD, Oliver JK, Wallace CC, Willis BL (1984) Mass spawning in tropical reef corals. Science 223:1186–1189
Hatta M, Fukami H, Wang W, Mori 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
Hayashibara T, Shimoike K, Kimura T, Hosaka S, Heyward A, Harrison P, Kudo K, Omori M (1993) Patterns of coral spawning at Akajima Island, Okinawa, Japan. Mar Ecol Prog Ser 101:253–262
Heyward AJ (1986) Sexual reproduction in five species of the coral Montipora. In: Jokiel PL, Richmond RH, Rogers RA (eds) Coral reef population biology. (Sea Grant Coop Rep) Hawaii University, pp 170–178
Heyward AJ, Yamazato K, Yemin T, Minei M (1987) Sexual reproduction of corals in Okinawa. Galaxea 6:331–343
Márquez LM, Oppen MJH van, Willis BL, Miller DJ (2002a) Sympatric populations of the highly cross-fertile coral species Acropora hyacinthus and A. cytherea are genetically distinct. Proc R Soc Lond B Biol Sci 269:1289–1294
Márquez LM, Oppen MJH van, Willis BL, Reyes A, Miller DJ (2002b) The highly cross-fertile coral species, Acropora hyacinthus and A. cytherea, constitute statistically distinguishable lineages. Mol Ecol 11:1339–1349
Miller K, Babcock RC (1997) Conflicting morphological and reproductive species boundaries in the coral genus Platygyra. Biol Bull 192:98–110
Miller KJ (1994) The Platygyra species complex: implications for coral taxonomy and evolution. PhD thesis, James Cook University, Townsville, Australia
Miller KJ, Benzie JAH (1997) No clear genetic distinction between morphological species within the coral genus Platygyra. Bull Mar Sci 61:907–917
Odorico DM, Miller DJ (1997) Variation in the ribosomal internal transcribed spacers and 5.8S rDNA among five species of Acropora (Cnidaria; Scleractinia): patterns of variation consistent with reticulate evolution. Mol Biol Evol 14:465–473
Oppen MJH van, Willis BL, Miller DJ (1999) Atypically low rate of Cytochrome b evolution in the scleractinian coral genus Acropora. Proc R Soc Lond B Biol Sci 266:179–183
Oppen MJH van, Willis BL, Vugt HWJA van, Miller DJ (2000) Examination of species boundaries in the Acropora cervicornis group (Scleractinia, Cnidaria) using nuclear DNA sequence analyses. Mol Ecol 9:1363–1373
Oppen MJH van, McDonald BJ, Willis BL, 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
Oppen MJH van, Catmull J, McDondald BJ, Hislop NR, Hagerman PJ, Miller DJ (2002a) The mitochondrial genome of Acropora tenuis (Cnidaria; Scleractinia) contains a large group I intron and a candidate control region. J Mol Evol 55:1–13
Oppen MJH van, Willis BL, Rheede T van, Miller DJ (2002b) 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
Posada D, Crandall KA (1998) MODELTEST: testing the model of DNA substitution. Bioinformatics 14:817–818
Sánchez JA, Alvarado EM, Gil MF, Charry H, Arenas OL, Chasqui LH, Garcia RP (1999) Synchronous mass spawning of Montastraea annularis (Ellis & Solander) and Montastraea faveolata (Ellis & Solander) (Faviidae: Scleractinia) at Rosario Islands, Caribbean Coast of Colombia. Bull Mar Sci 65:873–879
ShearerTL, Oppen MJH van, RomanoSL, Wörheide G (2002) Slow mitochondrial DNA sequence evolution in the Anthozoa (Cnidaria). Mol Ecol 11:2475–2487
Shimodaira H, Hasegawa M (1999) Multiple comparisons of log-likelihoods with applications to phylogenetic inference. Mol Biol Evol 16:1114–1116
Simpson CJ, Pearce AF, Walker DI (1991) Mass spawning of corals on Western Australian reefs and comparisons with the Great Barrier Reef. In: The Leeuwin Current: an influence on the coastal climate and marine life of Western Australia. Proc R Soc W Aust 74:85–91
Stobart B (2000) A taxonomic reappraisal of Montipora digitata based on genetic and morphometric evidence. Zool Stud 39:179–190
Stobart B, Benzie JAH (1994) Allozyme electrophoresis demonstrates that the scleractinian coral Montipora digitata is two species. Mar Biol 118:183–190
Swedburg JL (1994) Systematics and distribution of the scleractinian coral Madracis in the Miocene to Pleistocene of tropical America. Thesis, University of Iowa, Iowa City
Swofford DL (1999) PAUP*: phylogenetic analysis using parsimony (*and other methods). Sinauer, Sunderland, Mass.
Szmant AM, Weil E, Miller MW, Colon DE (1997) Hybridization within the species complex of Montastrea annularis. Mar Biol 129:561–572
Veghel MLJ van (1993) Multiple species spawning on Curacao reefs. Bull Mar Sci 52:1017–1021
Vermeij (2002) Evolutionary ecology of the coral genus Madracis. PhD thesis, University of Amsterdam
Veron JEN (1995) Corals in space and time. The biogeography and evolution of the Scleractinia. UNSW Press, Sydney
Veron JEN (2000) Corals of the world. Australian Institute of Marine Science, Townsville
Veron JEN, Kelley R (1988) Species stability in reef corals of Papua New Guinea and the Indo Pacific. Assoc Aust Palaeontol 6:1–69
Veron JEN, Wallace CC (1984) Scleractinia of eastern Australia, Part 5. Acroporidae. Aust Inst Mar Sci Monogr Ser 6:1–485
Vollmer SV, Palumbi SR (2002) Hybridization and the evolution of reef coral diversity. Science 296:2023–2025
Wallace CC (1999) Staghorn corals of the world: a revision of the genus Acropora. CSIRO, Collingwood
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
Willis BL, Babcock RC, Harrison PL, Oliver JK, Wallace CC (1985) Patterns in the mass spawning of corals on the Great Barrier Reef from 1981 to 1984. Proc 5th Int Coral Reef Symp 4:343–348
Willis BL, Babcock RC, Harrison PL, Wallace CC (1997) Experimental hybridization and breeding incompatibilities within the mating system of mass spawning reef corals. Coral Reefs 16:S53–S65
Acknowledgements
We thank David Miller for allowing us to undertake a large part of this study in his laboratory at James Cook University (Townsville, Australia), Lesa Peplow for her contribution to gathering the data, and Carlos Sánchez for his help with primer design. This study was funded by the Australian Research Council and the Australian Institute of Marine Science.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by M.S. Johnson, Crawley
Rights and permissions
About this article
Cite this article
van Oppen, M.J.H., Koolmees, E.M. & Veron, J.E.N. Patterns of evolution in the scleractinian coral genus Montipora (Acroporidae). Marine Biology 144, 9–18 (2004). https://doi.org/10.1007/s00227-003-1188-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00227-003-1188-3