- Research article
- Open Access
Incongruence between morphotypes and genetically delimited species in the coral genus Stylophora: phenotypic plasticity, morphological convergence, morphological stasis or interspecific hybridization?
© Flot et al; licensee BioMed Central Ltd. 2011
Received: 25 March 2011
Accepted: 4 October 2011
Published: 4 October 2011
Morphological data suggest that, unlike most other groups of marine organisms, scleractinian corals of the genus Stylophora are more diverse in the western Indian Ocean and in the Red Sea than in the central Indo-Pacific. However, the morphology of corals is often a poor predictor of their actual biodiversity: hence, we conducted a genetic survey of Stylophora corals collected in Madagascar, Okinawa, the Philippines and New Caledonia in an attempt to find out the true number of species in these various locations.
A molecular phylogenetic analysis of the mitochondrial ORF and putative control region concurs with a haploweb analysis of nuclear ITS2 sequences in delimiting three species among our dataset: species A and B are found in Madagascar whereas species C occurs in Okinawa, the Philippines and New Caledonia. Comparison of ITS1 sequences from these three species with data available online suggests that species C is also found on the Great Barrier Reef, in Malaysia, in the South China Sea and in Taiwan, and that a distinct species D occurs in the Red Sea. Shallow-water morphs of species A correspond to the morphological description of Stylophora madagascarensis, species B presents the morphology of Stylophora mordax, whereas species C comprises various morphotypes including Stylophora pistillata and Stylophora mordax.
Genetic analysis of the coral genus Stylophora reveals species boundaries that are not congruent with morphological traits. Of the four hypotheses that may explain such discrepancy (phenotypic plasticity, morphological stasis, morphological convergence, and interspecific hybridization), the first two appear likely to play a role but the fourth one is rejected since mitochondrial and nuclear markers yield congruent species delimitations. The position of the root in our molecular phylogenies suggests that the center of origin of Stylophora is located in the western Indian Ocean, which probably explains why this genus presents a higher biodiversity in the westernmost part of its area of distribution than in the "Coral Triangle".
The reason why most marine life forms, including corals, display their peak of biodiversity in the so called 'Coral Triangle' in Southeast Asia remains mysterious and much debated [1, 2]. The rare examples of sea creatures that do not conform to this general pattern may offer information crucial for our understanding of its root causes, provided that a solid taxonomic framework is available to interpret their present and past distribution (which is unfortunately rarely the case). Several such exceptions to the 'Coral Triangle' rule can be found in the scleractinian coral family Pocilloporidae that comprises the three genera Pocillopora, Seriatopora and Stylophora: although morphospecies of Seriatopora are most diverse in the Coral Triangle and therefore seem to follow the rule, Pocillopora "has what appears to be many regional endemics, especially in the central and far eastern Pacific" and Stylophora "has a higher diversity in the western Indian Ocean and Red Sea than in the central Indo-Pacific" . However, ongoing genetic studies of species boundaries in Pocillopora and Seriatopora suggest that, even though morphological descriptions of pocilloporid corals appear well founded in some locations [4–6], in others places current taxonomy is a poor predictor of the actual number of species [7–11].
Another widespread species according to Veron  is Stylophora subseriata (Ehrenberg, 1834), also found across the Indo-Pacific region, whereas the five other morphospecies of this genus are restricted to the Red Sea and the Gulf of Aden (Stylophora kuehlmanni Scheer and Pillai, 1983; Stylophora danae Milne Edwards and Haime, 1850; Stylophora mamillata Scheer and Pillai, 1983), to Madagascar (Stylophora madagascarensis Veron, 2000) or to both of these regions (Stylophora wellsi Scheer, 1964). Hence, the pattern of occurrence of the various species of Stylophora seems to contradict strongly the common "Coral Triangle" center of biodiversity model. However, recent reports of S. danae and S. kuehlmanni from the Philippines  have started to question this pattern, raising further concern that morphological species may not correspond to actual genetic entities (and indeed, Sheppard and Sheppard  considered S. danae, S. kuehlmanni and S. subseriata as ecomorphs of S. pistillata).
Phylogenetic analysis of mitochondrial sequences reveals the presence of two Stylophora clades in Madagascar vs. a single one in the Pacific Ocean
Haploweb analysis of nuclear ITS2 sequences shows that these three clades represent distinct species
We obtained nuclear internal transcribed spacer 2 (ITS2) sequences from all individuals sampled, and analyzed them together with the single published Stylophora ITS2 sequence available from GenBank (also from a Stylophora pistillata individual from Taiwan ). Despite its multiple-copy nature and its concerted mode of evolution , the ITS2 behaved in the present study just like a "regular" single-copy nuclear marker, with each individual harboring either one or two sequence types. Moreover, most ITS2 sequences types found co-occurring in some individuals were also observed occurring alone in other coral colonies, suggesting that these sequence types were allelic and segregated in a Mendelian fashion: for this reason we decided to call "heterozygotes" all individuals found to possess two different ITS2 types, even though we could not be totally sure that all ITS2 sequences obtained were really allelic (in the closely related genus Pocillopora, for instance, three ITS2 sequences types were observed in one individual ).
Phylogenetic analysis of nuclear ITS1 sequences reveals the existence of a fourth species of Stylophora in the Red Sea
The three species delimited from the mitochondrial and ITS2 datasets were recovered as distinct clades of ITS1 sequences: the monophyly of species B was very strongly supported (>98% bootstrap support using all three methods), whereas the monophyly of species C received weaker bootstrap support and the monophyly of species A was very weakly supported. All previously published ITS1 sequences from Australia, Malaysia, the South China Sea, Taiwan and Japan turned out to belong to species C, whereas all published Stylophora sequences from the Red Sea fell in a well supported fourth clade D (>90% bootstrap support using maximum likelihood and neighbor-joining) that can be considered a distinct species following the criterion of reciprocal monophyly.
Haplowebs are useful tools to delineate species
The present study confirms the usefulness of our recently proposed haploweb approach to deal with sequences of nuclear markers . Whereas the corresponding phylogenetic tree supported the delineation of clades A and B but revealed a large number of clades among our sequences from the Pacific Ocean, haploweb analysis (Figure 4) showed that these various Pacific Ocean clades are actually conspecific (since many heterozygous individuals harbor sequences from two different clades). The monophyly of species C was only very weakly supported in the maximum-likelihood phylogeny (with a bootstrap value of only 43%) and not at all supported using neighbor-joining and parsimony: therefore, this species would probably not have been detected in our ITS2 data if we had not taken into account the information provided by the co-occurrence of phylogenetically distant alleles in some individuals. In contrast, haploweb analysis delineated three groups of alleles among our ITS2 sequences, a result perfectly congruent with the mitochondrial phylogeny obtained from the same set of individuals.
Unlike in our previous article , the haploweb presented here was built on a tree rather than a network. Indeed, tree-based haplowebs are more straightforward to draw than their network-based counterparts, and are also more informative since they display the genotype of each sequenced individual. However, precisely due to their larger information content, tree-based haplowebs tend to become messy when dealing with large datasets and/or non-monophyletic species: in such cases, network-based haplowebs often turn out to be faster to draw and easier to interpret than tree-based ones.
Are molecularly delimited species of Stylophora congruent with morphology?
Finally, all published ITS1 sequences from the Red Sea fell in a distinct well-supported species D. The coral colonies sequenced were collected at depths of 2-4 meters in the Gulf of Aqaba and reported under the name S. pistillata , but according to another study the main morphospecies of Stylophora found in shallow waters in Aqaba is actually S. mordax : therefore, species D probably comprises a mixture of S. pistillata and S. mordax morphotypes. Since the type localities of S. pistillata and S. mordax are both in the Pacific Ocean, another name will be required for species D (possibly S. subseriata, since this species was described from the Red Sea and was considered by some authors as a synonym of S. pistillata ).
What causes the discrepancy between morphological and molecular species delimitations in Stylophora?
Our study revealed extensive morphological variation within species A and C: a more detailed genetic investigation using a larger number of variable markers such as microsatellites will be required to find out whether these variations are due to phenotypic plasticity or to underlying intraspecific genetic differences. However, phenotypic plasticity is well documented in Stylophora [30, 31, 28, 29] and is therefore likely to be responsible for at least part of the observed morphological variations.
The occurrence of the S. mordax morphotype in both species B and C can hardly be explained by intra-specific variation alone, but may rather result from phenotypic convergence (whereby two non-sister species independently evolve similar morphologies) and/or morphological stasis (whereby the appearance of the common ancestor of two sister species is passed on to both of them). Since the sister-species relationship between B and C was very strongly supported by all molecular markers analyzed, morphological stasis appears more likely than phenotypic convergence to explain the similar appearance of species B and of some morphs of species C.
Even though the data available are not yet sufficient to pin down completely the causes of the interspecific morphological similarities and intraspecific phenotypic variations observed in Stylophora, the observed congruence between nuclear and mitochondrial phylogenies allows us to reject the hypothesis that hybridization could be responsible for the discrepancy between morphological and genetic species boundaries in this genus. This contrasts with previous reports that hybridization may be rampant in corals (e.g. [39–50]); instead, our results concur with two recent articles on the closely related genus Pocillopora [9, 11] in suggesting that many such reports actually result from improper delineation of species boundaries and not from actual introgression between distinct genetic entities.
A new light on the biogeography and biodiversity of Stylophora in the Indo-Pacific Ocean
Surprisingly, the incongruence between morphological species delimitations and genetic species boundaries revealed in our study does not seem to affect the general picture of the biogeographic distribution of Stylophora species: with a least three species in the westernmost part of its area of occurrence versus a single one so far in the "Coral Triangle", Stylophora stands confirmed as a blatant exception to the usual biodiversity pattern observed in tropical marine invertebrates. The mitochondrial and ITS2 phylogenies of Stylophora comprise only species A, B and C and do not contradict the topology of the more complete (but less resolved) ITS1 phylogeny: the sister-group relationship of species B and C is strongly supported by all markers, whereas the root of the mitochondrial and ITS1 phylogenies fall between species A (from Madagascar) and species B and C (respectively from Madagascar and from the Pacific Ocean). Even though the sister-group of species D could not be determined unambiguously due to the current lack of mitochondrial and ITS2 sequences for this species, the position of the root in our molecular phylogenies suggests that the center of origin of Stylophora is located in the western Indian Ocean. This hypothesis will need to be confirmed by analyzing more samples from key locations in the Red Sea, the Gulf of Aden and the Indian Ocean, but would explain well the unusual concentration of the biodiversity of this genus in the westernmost part of his area of distribution.
While waiting for a global taxonomic revision of the genus Stylophora, for the sake of taxonomic stability we recommend that the preliminary results presented here not be translated yet into nomenclature, but that each genetically delimited species be provisionally designated by a letter (i.e., "Stylophora sp. A", "Stylophora sp. B", "Stylophora sp. C" and "Stylophora sp. D"). It is only when a complete picture of the species boundaries of Stylophora over its whole area of distribution becomes available that names will be reliably assigned to each species: for instance, even though the name S. madagascarensis appears suitable for species A given its morphological traits and the location where it was collected, this species may very well have been described first under another name in a different location, in which case S. madagascarensis would become a junior synonym of the actual name of this species.
Genetic analysis of the coral genus Stylophora reveals species boundaries that are not congruent with morphology. Of the four hypotheses capable of explaining such discrepancy (phenotypic plasticity, morphological stasis, morphological convergence, and interspecific hybridization), the first two seem likely to play a role but the fourth one is rejected since mitochondrial and nuclear markers yield congruent species delimitations. The center of origin of Stylophora appears to be located in the Indian Ocean, which probably explains why this genus presents a higher biodiversity in the westernmost part of its area of distribution than in the "Coral Triangle".
Sample collection and processing
Localization and depth of each Stylophora sample analyzed
( 23°23'07"S, 43°38'18"E)
( 23°23'07"S, 43°38'18"E)
PCR amplification and sequencing
Primers used for DNA amplification and sequencing
Determination of nuclear haplotypes
The ITS2 chromatogram pairs obtained from 43 individuals contained double peaks, indicating that each of these individuals harbored two sequence types. Finding out the sequence types was trivial for 5 individuals whose chromatograms contained only one double peak. Furthermore, 21 other chromatogram pairs had numerous double peaks, a situation typical of length-variant heterozygotes [53, 54] that allowed direct deconvolution of their superposed sequences using the program CHAMPURU  (available online at http://www.mnhn.fr/jfflot/champuru). The remaining 17 chromatograms pairs had several double peaks (at most 9), as expected from heterozygotes with no intra-individual length variation: we first attempted to resolve their haplotypes statistically by reference to the rest of the dataset using SeqPHASE  (available online at http://www.mnhn.fr/jfflot/seqphase) and PHASE , but only 7 individuals were phased unambiguously, i.e., with posterior probabilities equal or nearly equal to 1 (04NC064, 04NC182, 04NC251, 04NC282, 04NC324, 04NC436, 07Mad087). Among the 10 remaining heterozygotes, the haplotypes of 2 individuals (07Mad151, 07Mad189) were deduced directly from their chromatograms thanks to clear-cut differences in peak sizes (reflecting either differences in copy number in ribosomal DNA arrays or differential amplification during PCR), and the sequences of the 8 others (04NC024, 04NC132, 04NC365, 04NC379, 07Mad073, 07Mad074, 07Mad088, 07Mad157) were inferred using Clark's method . Length-variant heterozygosity was also observed in the ITS1 chromatograms of five individuals, all of which were resolved using CHAMPURU.
Phylogenetic analyses and haploweb construction
All haplotype sequences were deposited in public databases [GenBank:JN558840-JN559111]. ORF sequences were aligned in MEGA5  by taking advantage of the high degree of conservation of their aminoacid translations: all sequences from Stylophora were first aligned by hand as there were only few indels, before aligning them with outgroup sequences from Pocillopora and Seriatopora using the MEGA5 implementation of MUSCLE . CR, ITS1 and ITS2 sequences were aligned using MAFFT's Q-INS-I option [61, 62]. Since the two mitochondrial markers ORF and CR yielded congruent phylogenies, they were concatenated and only the result of the combined analysis is presented here. The best suited nucleotide model among 88 possible ones was determined for each dataset following the Bayesian Information Criterion  as implemented in jModelTest , and used to perform maximum-likelihood phylogenetic analyses in PhyML  with 1000 bootstrap replicates . Additional bootstrap analyses (1000 replicates) using neighbor-joining (K2P model, pairwise deletion) and parsimony (dataset collapsed using FaBox , complete deletion) were conducted in MEGA5. The Newick format haplotype trees ("haplotrees") produced by PhyML were converted into enhanced metafiles (emf) using the program FigTree 1.3.1 (available online at http://tree.bio.ed.ac.uk/software/figtree/), then imported in Microsoft PowerPoint. The ITS2 haploweb was obtained from the corresponding haplotree by drawing connections between haplotypes found co-occurring in heterozygous individuals .
Thanks to Annie Tillier, Josie Lambourdière and Céline Bonillo (Service de Systématique Moléculaire, CNRS UMS 2700, MNHN) for assistance with lab work, and to Eric Folcher, Catherine Geoffray, Jean-Louis Menou and Mark Vergara for helping with sample collection. Fieldwork in New Caledonia and Madagascar was financed by grants from the MNHN programs "Structure et évolution des écosystèmes" et "État et structure phylogénétique de la biodiversité actuelle et fossile"; thanks to Man Wai Rabenevanana, director of the Institut Halieutique et des Sciences Marines, for his logistic support in Tuléar (Toliara). Thanks also to two anonymous reviewers for their useful comments. This project was part of agreement n°2005/67 between Genoscope and MNHN on the project 'Macrophylogeny of life' directed by Guillaume Lecointre; support from the Consortium National de Recherche en Génomique is gratefully acknowledged. This is contribution n°78 from the Courant Research Center "Geobiology" funded by the German Initiative of Excellence.
- Veron JEN: Corals in Space and Time: Biogeography & Evolution of the Scleractinia. 1995, Sydney, Australia: University of New South Wales PressGoogle Scholar
- Hoeksema B: Delineation of the Indo-Malayan centre of maximum marine biodiversity: the Coral Triangle. Biogeography, Time, and Place: Distributions, Barriers, and Islands. Edited by: Renema W. 2007, Dordrecht: Springer Netherlands, 117-178.View ArticleGoogle Scholar
- Veron JEN, Stafford-Smith M: Corals of the World. 2000, Australian Institute of Marine ScienceGoogle Scholar
- Flot JF, Tillier S: Molecular phylogeny and systematics of the scleractinian coral genus Pocillopora in Hawaii. Proceedings of the 10th International Coral Reef Symposium. 2006, 1: 24-29.Google Scholar
- Chen C, Dai CF, Plathong S, Chiou CY, Chen CA: The complete mitochondrial genomes of needle corals, Seriatopora spp. (Scleractinia: Pocilloporidae): an idiosyncratic atp8, duplicated trnW gene, and hypervariable regions used to determine species phylogenies and recently diverged populations. Molecular Phylogenetics and Evolution. 2008, 46: 19-33. 10.1016/j.ympev.2007.09.013.View ArticlePubMedGoogle Scholar
- Flot JF, Magalon H, Cruaud C, Couloux A, Tillier S: Patterns of genetic structure among Hawaiian corals of the genus Pocillopora yield clusters of individuals that are compatible with morphology. Comptes Rendus Biologies. 2008, 331: 239-247. 10.1016/j.crvi.2007.12.003.View ArticlePubMedGoogle Scholar
- Flot JF, Licuanan W, Nakano Y, Payri C, Cruaud C, Tillier S: Mitochondrial sequences of Seriatopora corals show little agreement with morphology and reveal the duplication of a tRNA gene near the control region. Coral Reefs. 2008, 27: 789-794. 10.1007/s00338-008-0407-2.View ArticleGoogle Scholar
- Bongaerts P, Riginos C, Ridgway T, Sampayo EM, van Oppen MJH, Englebert N, Vermeulen F, Hoegh-Guldberg O: Genetic divergence across habitats in the widespread coral Seriatopora hystrix and its associated Symbiodinium. PLoS ONE. 2010, 5: e10871-10.1371/journal.pone.0010871.PubMed CentralView ArticlePubMedGoogle Scholar
- Flot JF, Couloux A, Tillier S: 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 Evolutionary Biology. 2010, 10: 372-10.1186/1471-2148-10-372.PubMed CentralView ArticlePubMedGoogle Scholar
- Souter P: Hidden genetic diversity in a key model species of coral. Marine Biology. 2010, 157: 875-885. 10.1007/s00227-009-1370-3.View ArticleGoogle Scholar
- Pinzón JH, LaJeunesse TC: Species delimitation of common reef corals in the genus Pocillopora using nucleotide sequence phylogenies, population genetics and symbiosis ecology. Molecular Ecology. 2011, 20: 311-325. 10.1111/j.1365-294X.2010.04939.x.View ArticlePubMedGoogle Scholar
- Takabayashi M, Carter DA, Lopez JV, Hoegh-Guldberg O: Genetic variation of the scleractinian coral Stylophora pistillata, from western Pacific reefs. Coral Reefs. 2003, 22: 17-22. 10.1007/s00338-002-0272-3.Google Scholar
- Zvuloni A, Mokady O, Al-Zibdah M, Bernardi G, Gaines SD, Abelson A: Local scale genetic structure in coral populations: a signature of selection. Marine Pollution Bulletin. 2008, 56: 430-438. 10.1016/j.marpolbul.2007.11.002.View ArticlePubMedGoogle Scholar
- Esper EJC: Fortsetzungen der Pflanzenthiere in Abbildungen nach der Natur mit Farben erleuchtet nebst Beschreibungen. Erster Theil. 1797, Nürnberg: Raspische BuchhandlungGoogle Scholar
- Veron JEN, Pichon M: Scleractinia of eastern Australia. I. Families Thamnasteriidae, Astrocoeniidae, Pocilloporidae. Australian Institute of Marine Science Monograph Series. 1976, 1: 1-86.Google Scholar
- Scheer G, Pillai CSG: Report on the stony corals from the Red Sea. Zoologica. 1983, 45: 1-198.Google Scholar
- Scheer G, Pillai CSG: Report on the Scleractinia from the Nicobar Islands. Results of the Xarifa Expedition 1957/58 of the International Institute for Submarine Research, Vaduz, Liechtenstein (Director Dr. Hans Hass). Zoologica. 1974, 42: 1-75.Google Scholar
- Pillai CSG, Scheer G: Report on the stony corals from the Maldive Archipelago. Results of the Xarifa Expedition 1957/58 of the International Institute for Submarine Research, Vaduz, Liechtenstein (Director Dr. Hans Hass). Zoologica. 1976, 43: 1-83.Google Scholar
- Faure G: Recherche sur les peuplements de Scléractiniaires des récifs coralliens de l'archipel des Mascareignes (Océan Indien occidental). Volume 2 - Systématique. PhD thesis. 1982, Université d'Aix-Marseille II, Faculté des Sciences de LuminyGoogle Scholar
- Hamilton HGH, Brakel WH: Structure and coral fauna of East African reefs. Bulletin of Marine Science. 1984, 34: 248-266.Google Scholar
- Gattuso JP, Pichon M, Jaubert J: Physiology and taxonomy of scleractinian corals: a case study in the genus Stylophora. Coral Reefs. 1991, 9: 173-182. 10.1007/BF00290419.View ArticleGoogle Scholar
- Hidaka M: Use of nematocyst morphology for taxonomy of some related species of scleractinian corals. Galaxea. 1992, 11: 21-28.Google Scholar
- Cairns SD, Hoeksema BW, van der Land J: Appendix: list of extant stony corals. Atoll Research Bulletin. 1999, 459: 13-46.View ArticleGoogle Scholar
- Pichon M: Scleractinia of New Caledonia: check list of reef dwelling species. Compendium of marine species of New Caledonia, Documents Scientifiques et Techniques II7. Edited by: Payri CE. 2007, Richer de Forges B. Nouméa: IRD, 149-157. 2Google Scholar
- Dana JD: United States Exploring Expedition. Vol. VII. Zoophytes. 1846, Philadelphia: C. ShermanGoogle Scholar
- Licuanan WY, Capili EB: New records of stony corals from the Philippines previously known from peripheral areas of the Indo-Pacific. The Raffles Bulletin of Zoology. 2004, 52: 285-288.Google Scholar
- Sheppard CRC, Sheppard ALS: Corals and coral communities of Arabia. Fauna of Saudi Arabia. 1991, 12: 3-170.Google Scholar
- Shaish L, Abelson A, Rinkevich B: Branch to colony trajectory in a modular organism: pattern formation in the Indo-Pacific coral Stylophora pistillata. Developmental Dynamics. 2006, 235: 2111-2121. 10.1002/dvdy.20861.View ArticlePubMedGoogle Scholar
- Shaish L, Abelson A, Rinkevich B: How plastic can phenotypic plasticity be? The branching coral Stylophora pistillata as a model system. PLoS ONE. 2007, 2: e644-10.1371/journal.pone.0000644.PubMed CentralView ArticlePubMedGoogle Scholar
- Meroz E, Brickner I, Loya Y, Peretzman-Shemer A, Ilan M: The effect of gravity on coral morphology. Proceedings of the Royal Society of London Series B, Biological Sciences. 2002, 269: 717-720. 10.1098/rspb.2001.1924.View ArticleGoogle Scholar
- Nakamura T, Yamasaki H: Morphological changes of pocilloporid corals exposed to water flow. Proceedings of the 10th International Coral Reef Symposium. 2006, 1: 872-875.Google Scholar
- Miller KJ, Ayre DJ: The role of sexual and asexual reproduction in structuring high latitude populations of the reef coral Pocillopora damicornis. Heredity. 2004, 92: 557-568. 10.1038/sj.hdy.6800459.View ArticlePubMedGoogle Scholar
- Flot JF, Tillier S: The mitochondrial genome of Pocillopora (Cnidaria: Scleractinia) contains two variable regions: The putative D-loop and a novel ORF of unknown function. Gene. 2007, 401: 80-87. 10.1016/j.gene.2007.07.006.View ArticlePubMedGoogle Scholar
- Chen C, Chiou CY, Dai CF, Chen CA: Unique mitogenomic features in the scleractinian family Pocilloporidae (Scleractinia: Astrocoeniina). Marine Biotechnology. 2008, 10: 538-553. 10.1007/s10126-008-9093-x.View ArticlePubMedGoogle Scholar
- Chen CA, Chang CC, Wei NV, Chen CH, Lein YT, Lin HE, Dai CF, Wallace CC: Secondary structure and phylogenetic utility of the ribosomal internal transcribed spacer 2 (ITS2) in scleractinian corals. Zoological Studies. 2004, 43: 759-771.Google Scholar
- Hillis DM, Dixon MT: Ribosomal DNA: molecular evolution and phylogenetic inference. Quarterly Review of Biology. 1991, 66: 411-453. 10.1086/417338.View ArticlePubMedGoogle Scholar
- Doyle JJ: The irrelevance of allele tree topologies for species delimitation, and a non-topological alternative. Systematic Botany. 1995, 20: 574-588. 10.2307/2419811.View ArticleGoogle Scholar
- Veron JEN: New species described in Corals of the World. Australian Institute of Marine Science Monograph Series. 2002, 11: 1-206.Google Scholar
- Kenyon JC: Models of reticulate evolution in the coral genus Acropora based on chromosome numbers: parallels with plants. Evolution. 1997, 51: 756-767. 10.2307/2411152.View ArticleGoogle Scholar
- Szmant AM, Weil E, Miller MW, Colón DE: Hybridization within the species complex of the scleractinan coral Montastraea annularis. Marine Biology. 1997, 129: 561-572. 10.1007/s002270050197.View ArticleGoogle Scholar
- Hatta M, Fukami H, Wang WQ, Omori M, Shimoike K, Hayashibara T, Ina Y, Sugiyama T: Reproductive and genetic evidence for a reticulate evolutionary history of mass-spawning corals. Molecular Biology and Evolution. 1999, 16: 1607-1613.View ArticlePubMedGoogle Scholar
- Diekmann OE, Bak RPM, Stam WT, Olsen JL: Molecular genetic evidence for probable reticulate speciation in the coral genus Madracis from a Caribbean fringing reef slope. Marine Biology. 2001, 139: 221-233. 10.1007/s002270100584.View ArticleGoogle Scholar
- van Oppen MJH, McDonald BJ, Willis B, Miller DJ: 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?. Molecular Biology and Evolution. 2001, 18: 1315-1329. 10.1093/oxfordjournals.molbev.a003916.View ArticlePubMedGoogle Scholar
- Márquez LM, Van Oppen MJH, Willis BL, Reyes A, Miller DJ: The highly cross-fertile coral species, Acropora hyacinthus and Acropora cytherea, constitute statistically distinguishable lineages. Molecular Ecology. 2002, 11: 1339-1349. 10.1046/j.1365-294X.2002.01526.x.View ArticlePubMedGoogle Scholar
- van Oppen MJH, Willis BL, Van Rheede T, Miller DJ: Spawning times, reproductive compatibilities and genetic structuring in the Acropora aspera group: evidence for natural hybridization and semi-permeable species boundaries in corals. Molecular Ecology. 2002, 11: 1363-1376. 10.1046/j.1365-294X.2002.01527.x.View ArticlePubMedGoogle Scholar
- Vollmer SV, Palumbi SR: Hybridization and the evolution of reef coral diversity. Science. 2002, 296: 2023-2025. 10.1126/science.1069524.View ArticlePubMedGoogle Scholar
- Miller DJ, van Oppen MJH: A 'fair go' for coral hybridization. Molecular Ecology. 2003, 12: 805-807. 10.1046/j.1365-294X.2003.01808.x.View ArticlePubMedGoogle Scholar
- Willis BL, van Oppen MJH, Miller DJ, Vollmer SV, Ayre DJ: The role of hybridization in the evolution of reef corals. Annual Review of Ecology, Evolution, and Systematics. 2006, 37: 489-517. 10.1146/annurev.ecolsys.37.091305.110136.View ArticleGoogle Scholar
- Combosch DJ, Guzman HM, Schuhmacher H, Vollmer SV: Interspecific hybridization and restricted trans-Pacific gene flow in the Tropical Eastern Pacific Pocillopora. Molecular Ecology. 2008, 17: 1304-1312. 10.1111/j.1365-294X.2007.03672.x.View ArticlePubMedGoogle Scholar
- Frade PR, Reyes-Nivia MC, Faria J, Kaandorp JA, Luttikhuizen PC, Bak RPM: Semi-permeable species boundaries in the coral genus Madracis: Introgression in a brooding coral system. Molecular Phylogenetics and Evolution. 2010, 57: 1072-1090. 10.1016/j.ympev.2010.09.010.View ArticlePubMedGoogle Scholar
- Sargent TD, Jamrich M, Dawid IB: Cell interactions and the control of gene activity during early development of Xenopus laevis. Developmental Biology. 1986, 114: 238-246. 10.1016/0012-1606(86)90399-4.View ArticlePubMedGoogle Scholar
- Fukami H, Budd AF, Levitan DR, Jara J, Kersanach R, Knowlton N: Geographic differences in species boundaries among members of the Montastraea annularis complex based on molecular and morphological markers. Evolution. 2004, 38: 324-337.View ArticleGoogle Scholar
- Creer S, Malhotra A, Thorpe RS, Pook CE: Targeting optimal introns for phylogenetic analyses in non-model taxa: experimental results in Asian pitvipers. Cladistics. 2005, 21: 390-395. 10.1111/j.1096-0031.2005.00072.x.View ArticleGoogle Scholar
- Flot JF, Tillier A, Samadi S, Tillier S: Phase determination from direct sequencing of length-variable DNA regions. Molecular Ecology Notes. 2006, 6: 627-630. 10.1111/j.1471-8286.2006.01355.x.View ArticleGoogle Scholar
- Flot JF: Champuru 1.0: a computer software for unraveling mixtures of two DNA sequences of unequal lengths. Molecular Ecology Notes. 2007, 7: 974-977. 10.1111/j.1471-8286.2007.01857.x.View ArticleGoogle Scholar
- Flot JF: SeqPHASE: a web tool for interconverting PHASE input/output files and FASTA sequence alignments. Molecular Ecology Resources. 2010, 10: 162-166. 10.1111/j.1755-0998.2009.02732.x.View ArticlePubMedGoogle Scholar
- Stephens M, Smith NJ, Donnelly P: A new statistical method for haplotype reconstruction from population data. The American Journal of Human Genetics. 2001, 68: 978-989. 10.1086/319501.View ArticlePubMedGoogle Scholar
- Clark A: Inference of haplotypes from PCR-amplified samples of diploid populations. Molecular Biology and Evolution. 1990, 7: 111-122.PubMedGoogle Scholar
- Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S: MEGA5: Molecular Evolutionary Genetics Analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution.Google Scholar
- Edgar RC: MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research. 2004, 32: 1792-1797. 10.1093/nar/gkh340.PubMed CentralView ArticlePubMedGoogle Scholar
- Katoh K, Misawa K, Kuma Ki, Miyata T: MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Research. 2002, 30: 3059-3066. 10.1093/nar/gkf436.PubMed CentralView ArticlePubMedGoogle Scholar
- Katoh K, Toh H: Improved accuracy of multiple ncRNA alignment by incorporating structural information into a MAFFT-based framework. BMC Bioinformatics. 2008, 9: 212-10.1186/1471-2105-9-212.PubMed CentralView ArticlePubMedGoogle Scholar
- Schwarz G: Estimating the dimension of a model. The Annals of Statistics. 1978, 6: 461-464. 10.1214/aos/1176344136.View ArticleGoogle Scholar
- Posada D: jModelTest: Phylogenetic model averaging. Molecular Biology and Evolution. 2008, 25: 1253-1256. 10.1093/molbev/msn083.View ArticlePubMedGoogle Scholar
- Guindon S, Gascuel O: A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology. 2003, 52: 696-704. 10.1080/10635150390235520.View ArticlePubMedGoogle Scholar
- Felsenstein J: Confidence limits on phylogenies: an approach using the bootstrap. Evolution. 1985, 39: 783-791. 10.2307/2412923.View ArticleGoogle Scholar
- Villesen P: FaBox: an online toolbox for fasta sequences. Molecular Ecology Notes. 2007, 7: 965-968. 10.1111/j.1471-8286.2007.01821.x.View ArticleGoogle Scholar
- Veron JEN, Stafford-Smith M: Coral ID Release 1. 2002, Australian Institute of Marine Science and CRR Qld Pty LtdGoogle Scholar
- Takabayashi M, Carter DA, Loh WKW, Hoegh-Guldberg O: A coral-specific primer for PCR amplification of the internal transcribed spacer region in ribosomal DNA. Molecular Ecology. 1998, 7: 925-931.View ArticleGoogle Scholar
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