Abstract
Species boundaries remain unresolved in many scleractinian corals. In this study, we examine evolutionary boundaries of species in the Acropora humilis species group. Five morphologically discrete units are recognized using principal components and hierarchical cluster analyses of quantitative and qualitative characters, respectively. Maximum parsimony and likelihood analyses of partial 28S rDNA sequences suggest that these morphological units diverged to form two evolutionarily distinct lineages, with A. humilis and A. gemmifera in one lineage and A. digitifera and two morphological types of A. monticulosa in the other. Low levels of sequence divergence but distinct morphologies of A. humilis and A. gemmifera within the former lineage suggest recent divergence or ongoing hybridization between these species. Substantially higher levels of divergence within and between A. digitifera and A. monticulosa suggest a more ancient divergence between these species, with sequence types being shared through occasional introgression without disrupting morphological boundaries. These results suggest that morphology has evolved more rapidly than the 28S rDNA marker, and demonstrate the utility of using morphological and molecular characters as complementary tools for interpreting species boundaries in corals.
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References
Arnold ML (1997) Natural hybridization and evolution. Oxford University Press, New York
Ayre DJ, Veron JEN, Dufty SL (1991) The corals Acropora palifera and Acropora cuneata are genetically and ecologically distinct. Coral Reefs 10:13–18
Babcock R, Miller K (1997) Genus Goniastrea: insights from morphological, genetic and reproductive variation. Proc ACRS 75th Anniversary Conf, Abstr 248
Brakel WH (1977) Corallite variation in Porites and the species problem in corals. Proc 3rd Int Coral Reef Symp 1:457–462
Brook G (1892) Preliminary descriptions of new species of Madrepora in the collections of the British Museum. Part II. Ann Mag Nat Hist 10:451–465
Brüggemann F (1879) Corals in zoology of Rodriguez. Phil Trans R Soc Lond B 168:569–579
Budd AF, Johnson KG, Potts DC (1994) Recognizing morphospecies in colonial reef corals: I. Landmark-based methods. Paleobiology 20:484–505
Chen CA, Yu J-K (2000) Universal primers for amplification of mitochondrial small subunit ribosomal RNA-encoding gene in scleractinian corals. Mar Biotechnol 2:146–153
Chen CA, Odorico D, Louis Mt, Veron J, Miller D (1995) Systematic relationships within the Anthozoa (Cnidaria: Anthozoa) using 5′-end of 28 s rDNA. Mol Phyl Evol 4:175–183
Chen CA, Wallace CC, Yu J-K, Wei NV (2000) Strategies for amplification by polymerase chain reaction of the complete sequence of the gene encoding nuclear large subunit ribosomal RNA in corals. Mar Biotechnol 2:558–570
Dana JD (1846) Zoophytes. US Explor Exped 7:1–740
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
Foster AB (1985) Variation within coral colonies and its importance for interpreting fossil species. J Paleontol 59:1359–1381
Garthwaite RL, Potts DC, Veron JEN, Done TJ (1994) Electrophoretic identification of poritid species (Anthozoa: Scleractinia). Coral Reefs 13:49–56
Hatta M, Fukami H, Wang W, 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
Hillis DM, Dixon MT (1991) Ribosomal DNA: molecular evolution and phylogenetic inference. Q Rev Biol 66:411–453
Hunter CL, Morden CW, Smith CM (1997) The utility of ITS sequences in assessing relationships among zooxanthellae and corals. Proc 8th Int Coral Reef Symp 2:1599–1602
Jameson SC (1997) Morphometric analysis of the Poritidae (Anthozoa: Scleractinia) off Belize. Proc 8th Int Coral Reef Symp 2:1591–1596
Kenyon JC (1997) Models of reticulate evolution in the coral genus Acropora based on chromosome numbers: parallels with plants. Evolution 51:756–767
Knowlton N (2001) Who are the players on coral reefs and does it matter? The importance of coral taxonomy for coral reef management. Bull Mar Sci 69:305–308
Knowlton N, Jackson JBC (1994) New taxonomy and niche partitioning on coral reefs: jack of all trades or master of some? Trends Ecol Evol 9:7–9
Lang JC (1984) Whatever works: the variable importance of skeletal and of non-skeletal characters in scleractinian taxonomy. Palaeontogr Am 54:18–44
Lopez JV, Kersanach R, Rehner SA, Knowlton N (1999) Molecular determination of species boundaries in corals: genetic analysis of the Montastraea annularis complex using amplified fragment length polymorphisms and a microsatellite marker. Biol Bull 196:80–93
Mayr E (1963) Animal species and evolution. Belknap Press, Cambridge, Massachusetts
Medina M, Weil E, Szmant AM (1999) Examination of the Montastraea annularis species complex (Cnidaria: Scleractinia) using ITS and COI sequences. Mar Biotechnol 1:89–97
Miller KJ, Benzie JAH (1997) No clear genetic distinction between morphological species within the coral genus Platygyra. Bull Mar Sci 61:907–917
Muko S, Kawasaki K, Sakai K, Takasu F, Shigesada N (2000) Morphological plasticity in the coral Porites sillimaniani and its adaptive significance. Bull Mar Sci 66:225–239
Odorico D, Miller D (1997a) Internal and external relationships of the Cnidaria: implications of primary and predicted secondary structure of the 5′-end of the 23S-like rDNA. Proc R Soc Lond B 264:77–82
Odorico DM, Miller DJ (1997b) 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
Palumbi SR (1994) Genetic divergence, reproductive isolation, and marine speciation. Annu Rev Ecol Syst 25:547–572
Posada D, Crandall KA (1998) MODELTEST: testing the model of DNA substitution. Bioinformatics 14:817–818
Rohlf F (1986–2000) NTSYS-pc. Numerical taxonomy and multivariate analysis system. Exeter Software, New York
Romano SL, Cairns SD (2000) Molecular phylogenetic hypotheses for the evolution of scleractinian corals. Bull Mar Sci 67:1043–1068
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
Swofford DL (2002) PAUP*. Phylogenetic analysis using parsimony (* and other methods). Sinauer Associates, Massachusetts
Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucl Acids Res 24:4876–4882
van Oppen MJH, Willis BL, van Vugt HWJA, 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 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
Veron JEN (1995) Corals in space and time: the biogeography and evolution of the Scleractinia. UNSW Press, Sydney
Veron JEN, Pichon M (1976) Scleractinia of eastern Australia. Part I. Families Thamnasteriidae, Astrocoeniidae, Pocilloporidae. Australian Government Publishing Service, Canberra
Veron JEN, Wallace CC (1984) Scleractinia of eastern Australia. Part V. Family Acroporidae. Australian National University Press, Canberra
Veron JEN, Odorico DM, Chen CA, Miller DJ (1996) Reassessing evolutionary relationships of scleractinian corals. Coral Reefs 15:1–9
Vogler AP (2001) The genic view: a useful model of the process of speciation? J Evol Biol 14:876–877
Wallace CC (1999) Staghorn corals of the world: a revision of the coral genus Acropora (Scleractinia; Astrocoeniina; Acroporidae) worldwide, with emphasis on morphology, phylogeny and biogeography. CSIRO Publishing, 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
Wallace CC, Pandolfi JM, Young A, Wolstenholme J (1991) Indo-Pacific coral biogeography: a case study from the Acropora selago group. Aust Syst Bot 4:199–210
Weil E (1992) Genetic and morphological variation in Caribbean and eastern Pacific Porites (Anthozoa, Scleractinia). Preliminary results. Proc 7th Int Coral Reef Symp 2:643–656
Weil E, Knowlton N (1994) A multi-character analysis of the Caribbean coral Montastraea annularis (Ellis and Solander, 1786) and its two 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: Coelenterata. Geological Survey of America and University of Kansas Press, Kansas, pp 328–443
Wilcox D, Dove B, McDavid D, Greer D (1995–96) UTHSCSA Image Tool for Windows. University of Texas Health Science Center, San Antonio
Willis BL (1985) Phenotypic plasticity versus phenotypic stability in the reef corals Turbinaria mesenterina and Pavona cactus. Proc 5th Int Coral Reef Symp 4:107–112
Willis BL (1990) Species concepts in extant scleractinian corals: considerations based on reproductive biology and genotypic population structures. Syst Bot 15:136–149
Willis BL, Babcock RC, Harrison PL, Wallace CC (1997) Experimental hybridization and breeding incompatibilities within the mating systems of mass spawning reef corals. Coral Reefs 16(Suppl):S53–S65
Wu C-I (2001) The genic view of the process of speciation. J Evol Biol 14:851–865
Acknowledgments
We thank T. Hughes, N. Daschbach, A. Green, and P. Craig for organizing field logistics and E. Dinsdale, M.-J. Boyle, and P. Craig for field assistance; J. Wright for photographing branch samples; and B. Radford, S. Klanten, and students at the Institute of Zoology, Academia Sinica, for laboratory support. T. Hughes, L. van Herwerden, A. Baird, P. Muir, and two anonymous reviewers provided useful comments on the manuscript. This study was funded by grants to J. Wolstenholme from the Australian Coral Reef Society and James Cook University, an ARC grant to T. Hughes, and an NSC grant and internal funding from Academia Sinica to C.A. Chen.
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Wolstenholme, J.K., Wallace, C.C. & Chen, C.A. Species boundaries within the Acropora humilis species group (Cnidaria; Scleractinia): a morphological and molecular interpretation of evolution. Coral Reefs 22, 155–166 (2003). https://doi.org/10.1007/s00338-003-0299-0
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DOI: https://doi.org/10.1007/s00338-003-0299-0