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. 2011 Feb 7;11:37. doi: 10.1186/1471-2148-11-37

Cleaning up the 'Bigmessidae': Molecular phylogeny of scleractinian corals from Faviidae, Merulinidae, Pectiniidae and Trachyphylliidae

Danwei Huang 1,2,✉, Wilfredo Y Licuanan 3, Andrew H Baird 4, Hironobu Fukami 5
PMCID: PMC3042006  PMID: 21299898

Abstract

Background

Molecular phylogenetic studies on scleractinian corals have shown that most taxa are not reflective of their evolutionary histories. Based principally on gross morphology, traditional taxonomy suffers from the lack of well-defined and homologous characters that can sufficiently describe scleractinian diversity. One of the most challenging clades recovered by recent analyses is 'Bigmessidae', an informal grouping that comprises four conventional coral families, Faviidae, Merulinidae, Pectiniidae and Trachyphylliidae, interspersed among one another with no apparent systematic pattern. There is an urgent need for taxonomic revisions in this clade, but it is vital to first establish phylogenetic relationships within the group. In this study, we reconstruct the evolutionary history of 'Bigmessidae' based on five DNA sequence markers gathered from 76 of the 132 currently recognized species collected from five reef regions in the central Indo-Pacific and the Atlantic.

Results

We present a robust molecular phylogeny of 'Bigmessidae' based on the combined five-gene data, achieving a higher degree of resolution compared to previous analyses. Two Pacific species presumed to be in 'Bigmessidae' are more closely related to outgroup clades, suggesting that other unsampled taxa have unforeseen affinities. As expected, nested within 'Bigmessidae' are four conventional families as listed above, and relationships among them generally corroborate previous molecular analyses. Our more resolved phylogeny supports a close association of Hydnophora (Merulinidae) with Favites + Montastraea (Faviidae), rather than with the rest of Merulinidae, i.e., Merulina and Scapophyllia. Montastraea annularis, the only Atlantic 'Bigmessidae' is sister to Cyphastrea, a grouping that can be reconciled by their septothecal walls, a microstructural feature of the skeleton determined by recent morphological work. Characters at the subcorallite scale appear to be appropriate synapomorphies for other subclades, which cannot be explained using macromorphology. Indeed, wide geographic sampling here has revealed more instances of possible cryptic taxa confused by evolutionary convergence of gross coral morphology.

Conclusions

Numerous examples of cryptic taxa determined in this study support the assertion that diversity estimates of scleractinian corals are erroneous. Fortunately, the recovery of most 'Bigmessidae' genera with only minor degrees of paraphyly offers some hope for impending taxonomic amendments. Subclades are well defined and supported by subcorallite morphological features, providing a robust framework for further systematic work.

Background

For the last two decades, coral systematists have been untangling the complex evolutionary relationships among scleractinian species using DNA sequence data. Seminal molecular phylogenetic work by Romano and Palumbi [1,2] divided the Scleractinia into two major clades, the robust and complex groups, and indicated many problems with traditional taxonomy based on morphology (see also [3]). For instance, Leptastrea was recovered within a Fungiina clade rather than the suborder Faviina, where morphological studies had placed it (e.g., [4,5]). Gradually, using more genetic loci, further evidence was uncovered to show that non-monophyly of coral taxa is widespread in Scleractinia (e.g., [6-11]). This culminated in a comprehensive survey of the entire taxon by Fukami et al. [12], which showed that while Scleractinia is monophyletic, most taxonomic groups within it are not. In fact, a staggering 11 of 16 conventional families are polyphyletic.

Undoubtedly, one of the most challenging clades that have been recovered by recent analyses is a group of robust corals in clade XVII [12]. The disarray within the clade is epitomized by its informal name 'Bigmessidae' [13,14]. This clade contains species from four traditional coral families, Faviidae, Merulinidae, Pectiniidae and Trachyphylliidae, interspersed among one another in the tree based on mitochondrial cytochrome oxidase I (COI) and cytochrome b gene sequences [12]. With the exception of the Montastraea annularis complex, all members of this clade are from the Indo-Pacific. Families with all species included within clade XVII are Trachyphylliidae (monospecific) and Merulinidae, the latter being polyphyletic, while Faviidae and Pectiniidae have representatives present within and outside clade XVII. Although the clade has not been examined in detail, Huang et al. [15] showed that representatives from other families (Merulinidae and Mussidae) are also nested within it, and several genera are not monophyletic (i.e., Echinopora, Favia, Favites, Goniastrea and Montastraea). In addition, Fukami et al. [12] found para- or polyphyly in Leptoria, Oulophyllia and Platygyra for at least one marker.

Clearly, there exists an urgent need for taxonomic revisions in this clade, amidst the ongoing disarray in the Scleractinia. But in order to begin any form of revision for clade XVII, it is first necessary to determine which subclades are problematic, using as complete a morphological and genetic coverage as possible. Up to this point, the largest number of markers used for analysis of this group has been derived from Fukami et al. [12], who used the aforementioned mitochondrial genes, as well as the nuclear β-tubulin and 28S rDNA separately. However, only 33 species represented by 38 terminals were analyzed for clade XVII, and several subclades were not resolved due to their short branches. Resolution was improved in Huang et al. [15], which included 85 terminals from 43 species, but that study used only COI and a noncoding intergenic mitochondrial region (IGR).

In this study, we present data for five molecular markers—two mitochondrial and three nuclear loci—from 76 of the 132 currently recognized species in clade XVII [12]. We also included seven species from other robust corals as outgroups. Corals were sequenced from five reef regions—the central and northern Great Barrier Reef in Australia, Wakayama in Japan, Batangas in the Philippines, Singapore and the Caribbean. We reconstruct the evolutionary history of clade XVII and identify subclade placement of species that have not been studied in a molecular phylogenetic context. As some species were sampled from multiple locations, we also test if these corals were as widespread as previously recorded.

Methods

Specimen collection and DNA extraction

Specimens were collected from coral reefs in five regions—Singapore, Wakayama (Japan), Queensland (Australia), Batangas (The Philippines), and the Caribbean. To ensure consistency in identifications among localities, each coral was sampled by at least two authors, based on morphological features that can be recognized in the field. The identity was later confirmed in the laboratory after examining skeletal traits [5,16-21]. In total, 124 specimens from 83 species in clades XIV-XXI have been included in the present analysis (Table 1; see Additional file 1). We photographed each colony in the field and collected between 10 and 100 cm2 of coral from each colony using a hammer and chisel, with ~2cm2 of tissue preserved in 100% ethanol.

Table 1.

Species and DNA sequences examined in this study.

No. Species Voucher 28S rDNA histone H3 ITS rDNA mt COI mt IGR
1 Acanthastrea echinata (XX; Mussidae) S031 HQ203399 HQ203520 HQ203308 EU371658
2 Barabattoia amicorum S047 HQ203400 HQ203521 HQ203309 FJ345412 FJ345480
3 Caulastraea echinulata S041 HQ203401 HQ203522 FJ345414 FJ345496
4 Caulastraea furcata P108 HQ203402 HQ203523 HQ203248 HQ203639
5 Caulastraea tumida G61875 HQ203403 HQ203524 HQ203310 HQ203249 HQ203640
6 Cyphastrea chalcidicum G61902 HQ203404 HQ203525 HQ203311 HQ203250
7 Cyphastrea chalcidicum S103 HQ203405 HQ203526 HQ203312 FJ345415
8 Cyphastrea microphthalma S069 HQ203406 HQ203527 FJ345416
9 Cyphastrea serailia G61889 HQ203407 HQ203528 HQ203313 HQ203251
10 Cyphastrea serailia S024 HQ203408 HQ203529 HQ203314 EU371659
11 Cyphastrea serailia P120 HQ203409 HQ203530 HQ203252
12 Diploastrea heliopora (XV) S048 HQ203410 HQ203531 HQ203315 EU371660
13 Echinopora gemmacea S120 HQ203411 HQ203532 HQ203316 FJ345418 FJ345457
14 Echinopora horrida G61907 HQ203412 HQ203533 HQ203317 HQ203253 HQ203641
15 Echinopora lamellosa S109 HQ203413 HQ203534 HQ203318 FJ345419 FJ345458
16 Echinopora mammiformis G61884 HQ203414 HQ203535 HQ203319 HQ203254 HQ203642
17 Echinopora pacificus S110 HQ203415 HQ203536 HQ203320 FJ345420 FJ345459
18 Favia danae G61885 HQ203416 HQ203537 HQ203321 HQ203643
19 Favia danae S092 HQ203417 HQ203538 EU371663 FJ345476
20 Favia favus G61880 HQ203418 HQ203539 HQ203322 HQ203255 HQ203644
21 Favia favus G61915 HQ203419 HQ203540 HQ203323 HQ203256 HQ203645
22 Favia favus S003 HQ203420 HQ203541 HQ203324 EU371710 FJ345511
23 Favia favus S025 HQ203421 HQ203542 EU371664 FJ345465
24 Favia favus S040 HQ203422 HQ203543 HQ203325 EU371665 FJ345466
25 Favia favus P105 HQ203423 HQ203544 HQ203257 HQ203646
26 Favia fragum (XXI) AF549222 AB117222
27 Favia cf. laxa S013 HQ203424 HQ203545 EU371707 FJ345508
28 Favia cf. laxa S014 HQ203425 HQ203546 HQ203326 EU371708 FJ345509
29 Favia lizardensis G61872 HQ203426 HQ203547 HQ203327 HQ203647
30 Favia lizardensis S072 HQ203427 HQ203548 HQ203328 EU371668 FJ345484
31 Favia lizardensis P136 HQ203428 HQ203549 HQ203648
32 Favia cf. maritima G61912 HQ203429 HQ203550 HQ203329 HQ203258 HQ203649
33 Favia matthaii G61881 HQ203430 HQ203551 HQ203330
34 Favia matthaii G61883 HQ203431 HQ203552 HQ203331 HQ203259 HQ203650
35 Favia matthaii S005 HQ203432 HQ203553 HQ203332 EU371669 FJ345471
36 Favia matthaii S029 HQ203433 HQ203554 HQ203333 EU371671 FJ345473
37 Favia maxima S052 HQ203434 HQ203555 HQ203334 EU371674
38 Favia maxima P142 HQ203435 HQ203556 HQ203260 HQ203651
39 Favia cf. maxima P134 HQ203436 HQ203557 HQ203335 HQ203261 HQ203652
40 Favia pallida G61898 HQ203437 HQ203558 HQ203336 HQ203653
41 Favia pallida S036 HQ203438 HQ203559 HQ203337 EU371675 FJ345482
42 Favia rosaria G61911 HQ203439 HQ203560 HQ203338 HQ203262 HQ203654
43 Favia rotumana S068 HQ203440 HQ203561 HQ203339 FJ345427 FJ345485
44 Favia rotundata G61874 HQ203441 HQ203562 HQ203340 HQ203263
45 Favia rotundata P132 HQ203442 HQ203563
46 Favia speciosa S001 HQ203443 HQ203564 HQ203341 EU371677 FJ345505
47 Favia speciosa S026 HQ203444 HQ203565 EU371680 FJ345506
48 Favia speciosa P103 HQ203445 HQ203566 HQ203342 HQ203264 HQ203655
49 Favia stelligera P141 HQ203446 HQ203567 HQ203343 HQ203265 HQ203656
50 Favia truncatus G61897 HQ203447 HQ203568 HQ203344 HQ203266 HQ203657
51 Favites abdita S002 HQ203448 HQ203569 HQ203345 HQ203267
52 Favites chinensis S084 HQ203449 HQ203570 HQ203346 HQ203268
53 Favites complanata S007 HQ203450 HQ203571 HQ203347 EU371689
54 Favites flexuosa P116 HQ203451 HQ203572 HQ203348 HQ203269
55 Favites halicora S115 HQ203452 HQ203573 HQ203349 HQ203270
56 Favites paraflexuosa S100 HQ203453 HQ203574 HQ203350 EU371694 FJ345521
57 Favites pentagona S086 HQ203454 HQ203575 HQ203351 EU371695
58 Favites pentagona P111 HQ203455 HQ203576 HQ203271
59 Favites russelli G61895 HQ203456 HQ203577 HQ203352 HQ203272 HQ203658
60 Favites stylifera P128 HQ203457 HQ203578 HQ203353 HQ203273 HQ203659
61 Goniastrea aspera S107 HQ203458 HQ203579 HQ203354 FJ345430 FJ345487
62 Goniastrea australensis G61876 HQ203459 HQ203580 HQ203355 HQ203274 HQ203660
63 Goniastrea australensis S088 HQ203460 HQ203581 HQ203356 FJ345431 FJ345490
64 Goniastrea australensis S098 HQ203461 HQ203582 EU371696 FJ345491
65 Goniastrea edwardsi S045 HQ203462 HQ203583 HQ203357 EU371697 FJ345492
66 Goniastrea edwardsi S117 HQ203463 HQ203584 FJ345432 FJ345493
67 Goniastrea favulus G61877 HQ203464 HQ203585 HQ203358 HQ203661
68 Goniastrea favulus S022 HQ203465 HQ203586 EU371698 FJ345494
69 Goniastrea palauensis S021 HQ203466 HQ203587 HQ203359 EU371699 FJ345488
70 Goniastrea pectinata G61879 HQ203467 HQ203588 HQ203360 HQ203662
71 Goniastrea pectinata S043 HQ203468 HQ203589 FJ345434 FJ345489
72 Goniastrea pectinata P110 HQ203469 HQ203590 HQ203663
73 Goniastrea retiformis S083 HQ203470 HQ203591 HQ203361 EU371700 FJ345527
74 Goniastrea retiformis P119 HQ203471 HQ203592 HQ203275 HQ203664
75 Hydnophora exesa (Merulinidae) P127 HQ203472 HQ203593 HQ203362 HQ203276 HQ203665
76 Hydnophora microconos (Merulinidae) P121 HQ203473 HQ203594 HQ203363 HQ203277 HQ203666
77 Hydnophora pilosa (Merulinidae) P138 HQ203474 HQ203595 HQ203364 HQ203278 HQ203667
78 Leptoria irregularis P133 HQ203475 HQ203596 HQ203279 HQ203668
79 Leptoria phrygia S081 HQ203476 HQ203597 HQ203365 EU371705 FJ345529
80 Lobophyllia corymbosa (XIX; Mussidae) AF549237 AB117241
81 Merulina ampliata (Merulinidae) P106 HQ203477 HQ203598 HQ203280 HQ203669
82 Merulina scabricula (Merulinidae) P114 HQ203478 HQ203599 HQ203366 HQ203281 HQ203670
83 Montastraea annularis A622 HQ203479 HQ203600 HQ203367 HQ203282
84 Montastraea cf. annuligera P117 HQ203481 HQ203602 HQ203369 HQ203671
85 Montastraea cavernosa (XVI) A005 HQ203480 HQ203601 HQ203368 HQ203283
86 Montastraea colemani P118 HQ203482 HQ203603 HQ203284
87 Montastraea curta G61882 HQ203483 HQ203604 HQ203370 HQ203285
88 Montastraea curta P122 HQ203484 HQ203605 HQ203286
89 Montastraea magnistellata G61896 HQ203485 HQ203606 HQ203371 HQ203287
90 Montastraea magnistellata P109 HQ203486 HQ203607 HQ203288
91 Montastraea multipunctata P131 HQ203487 HQ203608 HQ203372 HQ203289
92 Montastraea salebrosa P139 HQ203488 HQ203609 HQ203373 HQ203290 HQ203672
93 Montastraea valenciennesi G61904 HQ203489 HQ203610 HQ203291 HQ203673
94 Montastraea valenciennesi S006 HQ203490 HQ203611 HQ203374 EU371713 FJ345514
95 Montastraea valenciennesi S008 HQ203491 HQ203612 EU371714 FJ345515
96 Montastraea valenciennesi P102 HQ203492 HQ203613 HQ203375 HQ203292
97 Moseleya latistellata G61909 HQ203493 HQ203614 HQ203376 HQ203293 HQ203674
98 Mussa angulosa (XXI; Mussidae) AF549236 AB441402 NC_008163
99 Mycedium elephantotus (Pectiniidae) S121 HQ203494 HQ203615 HQ203377 HQ203294 HQ203675
100 Mycedium robokaki (Pectiniidae) S126 HQ203495 HQ203616 HQ203378 HQ203295 HQ203676
101 Oulophyllia bennettae G61873 HQ203496 HQ203617 HQ203296 HQ203677
102 Oulophyllia bennettae S033 HQ203497 HQ203618 HQ203379 FJ345436 FJ345497
103 Oulophyllia aff. bennettae P140 HQ203498 HQ203619 HQ203380 HQ203297
104 Oulophyllia crispa S055 HQ203499 HQ203620 HQ203381 EU371721 FJ345500
105 Pectinia alcicornis (Pectiniidae) P124 HQ203500 HQ203621 HQ203382 HQ203298 HQ203678
106 Pectinia ayleni (Pectiniidae) S122 HQ203501 HQ203622 HQ203383 HQ203299 HQ203679
107 Pectinia lactuca (Pectiniidae) P115 HQ203502 HQ203623 HQ203384 HQ203300 HQ203680
108 Pectinia paeonia (Pectiniidae) P126 HQ203503 HQ203624 HQ203385 HQ203301 HQ203681
109 Platygyra acuta P123 HQ203504 HQ203625 HQ203386 HQ203682
110 Platygyra contorta P112 HQ203505 HQ203626 HQ203387 HQ203683
111 Platygyra daedalea G61878 HQ203506 HQ203627 HQ203684
112 Platygyra daedalea S116 HQ203507 HQ203628 HQ203388 FJ345440 FJ345530
113 Platygyra lamellina G61887 HQ203508 HQ203629 HQ203389 HQ203302 HQ203685
114 Platygyra lamellina S114 HQ203509 HQ203630 FJ345441 FJ345531
115 Platygyra pini G61899 HQ203510 HQ203631 HQ203390 HQ203303 HQ203686
116 Platygyra pini S035 HQ203511 HQ203632 HQ203391 FJ345443 FJ345535
117 Platygyra ryukyuensis P101 HQ203512 HQ203633 HQ203392 HQ203304 HQ203687
118 Platygyra sinensis S118 HQ203513 HQ203634 HQ203393 FJ345442 FJ345534
119 Platygyra sinensis P130 HQ203514 HQ203635 HQ203305 HQ203688
120 Platygyra cf. verweyi S037 HQ203515 HQ203636 HQ203394 EU371722 FJ345532
121 Plesiastrea versipora (XIV) S127 HQ203397 HQ203518 HQ203307 HQ203246
122 Plesiastrea versipora (XIV) P137 HQ203398 HQ203519 HQ203247
123 Scapophyllia cylindrica (Merulinidae) S060 HQ203516 HQ203637 HQ203395 FJ345444 FJ345502
124 Trachyphyllia geoffroyi (Trachyphylliidae) J001 HQ203517 HQ203638 HQ203396 HQ203306 HQ203689
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Unless indicated by roman numerals and/or family names in parentheses, all species belong to clade XVII and Faviidae, respectively. Species placed in a molecular phylogenetic context for the first time are in bold. Specimens with voucher numbers starting with 'G' are from Great Barrier Reef (Australia), 'S' from Singapore, 'J' from Japan, 'P' from the Philippines, and 'A' from the Atlantic. GenBank accession numbers are displayed for each molecular marker.

For each colony from Singapore, Japan and the Caribbean, DNA was extracted from ~2 cm2 of tissue digested in twice their volume of CHAOS solution (not an acronym; 4 M guanidine thiocyanate, 0.1% N-lauroyl sarcosine sodium, 10 mM Tris pH 8, 0.1 M 2-mercaptoethanol) for at least three days at room temperature before DNA extraction using a phenol-chloroform based method with a phenol extraction buffer (100 mM TrisCl pH 8, 10 mM EDTA, 0.1% SDS) [15,22-24]. For specimens from Australia and the Philippines, genomic DNA was extracted from the tissues preserved in ethanol using the Qiagen DNeasy kit, following the manufacturer's instructions.

The rest of the colony was sprayed with a powerful water jet to remove as much tissue as possible before being bleached in 5-10% sodium hypochlorite solution. The skeletons were rinsed in fresh water, dried, and deposited in the Raffles Museum of Biodiversity Research (Singapore), Seto Marine Biological Laboratory (Wakayama, Japan), Museum of Tropical Queensland (Australia), and De La Salle University (Manila, The Philippines) (Table 1).

PCR amplification and sequencing

A total of five molecular markers were amplified for a majority of the samples (Tables 1 and 2). They consist of three nuclear and two mitochondrial loci: (1) 28S rDNA D1 and D2 fragments; (2) histone H3; (3) internal transcribed spacers 1 and 2, including 5.8S rDNA (ITS in short); (4) cytochrome oxidase subunit I (COI); and (5) noncoding intergenic region situated between COI and the formylmethionine transfer RNA gene (IGR in short) [8,23,25-27].

Table 2.

Molecular markers utilized for phylogenetic reconstruction.

Marker Primer pairs Total characters (informative) Model Source
28S rDNA C1': 5'-ACC CGC TGA ATT TAA GCA T-3'
D2MAD: 5'-GAC GAT CGA TTT GCA CGT CA-3'		 861 (135) HKY+Γ [25]
histone H3 H3F: 5'-ATG GCT CGT ACC AAG CAG ACV GC-3'
H3R: 5'-ATA TCC TTR GGC ATR ATR GTG AC-3'		 374 (73) HKY+Γ [26]
ITS rDNA A18S: 5'-GATCGAACGGTTTAGTGAGG-3'
ITS-4: 5'-TCCTCCGCTTATTGATATGC-3'		 1137 (425) SYM+Γ [27]
mt COI MCOIF: 5'-TCTACAAATCATAAAGACATAGG-3'
MCOIR: 5'-GAGAAATTATACCAAAACCAGG-3'		 719 (71) HKY+I [8]
mt IGR MNC1f: 5'-GAGCTGGGCTTCTTTAGAGTG-3'
MNC1r: 5'-GTGAGACTCGAACTCACTTTTC-3'		 1509 (763) SYM+I [23]
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The mitochondrial intergenic region (IGR) was too variable to be aligned across the entire clade, so only alignable sequences were included in the analysis. ITS comprises multiple copies in the nuclear genome, but the primers we used have shown high fidelity for a single copy, precluding the need to clone the amplicons [27-33]. Nevertheless, in the unlikely case that paralogs were sequenced, our analyses could be confused by incomplete lineage sorting [7]. We therefore sequenced the ITS locus from at most one representative of each species, unless analyses of the other four markers did not recover its sequences as a clade. In the latter case, sequences may actually belong to separate cryptic species that have been obscured by gross morphological similarities. For COI, not all specimens of each species were necessarily sequenced since intraspecific variation of this gene is limited [15,24].

PCR products were purified with ExoSAP-IT (GE Healthcare, Uppsala, Sweden) and sequencing was performed by Advanced Studies in Genomics, Proteomics and Bioinformatics (ASGPB) at the University of Hawaii at Manoa using the Applied Biosystems BigDye Terminator kit and an ABI 3730XL sequencer. New sequences were deposited in GenBank under accession numbers HQ203246-HQ203689 (Table 1).

Phylogenetic analyses

Sequences were organized into five separate data matrices using Mesquite 2.72 [34], and each aligned with the accurate alignment option (E-INS-i) in MAFFT 6.7 [35-37] under default parameters. Substitution saturation of protein-coding genes was assessed via DAMBE [38,39], where we found histone H3 and COI to be unsaturated at the third codon positions for tree inference. Consequently, we concatenated the five gene matrices into a single partitioned matrix consisting of 4600 characters, 1467 of which were parsimony informative. This was analyzed using maximum parsimony, Bayesian likelihood, and maximum likelihood methods. We also carried out these analyses on a four-gene dataset omitting the ITS partition to determine if the phylogenetic reconstruction was sensitive to the ITS sampling strategy.

Under a maximum parsimony framework, we utilized new search technologies [40,41] in the software TNT 1.1 [42,43]. Tree searches consisted of 50000 random addition sequence replicates under the default sectorial, ratchet, drift and tree fusing parameters. Gaps were treated as missing data and clade stability was inferred using 1000 bootstrap replicates each employing 100 random addition sequences.

For maximum likelihood, neighbor-joining and Bayesian analyses, we determined the most suitable model of molecular evolution for each gene partition and the concatenated matrix using jModelTest 0.1.1 [44,45] to test for a total of 24 models, following the Akaike Information Criterion (AIC). The maximum likelihood tree for each partition and the combined dataset was inferred using RAxML 7.2.3 [46,47] at the Cyberinfrastructure for Phylogenetic Research (CIPRES; http://www.phylo.org), employing the GTRGAMMA model. The proportion of invariable sites and gamma distribution shape parameter for variable sites were estimated during the maximum likelihood analysis. Multiparametric bootstrap analysis was carried out using 1000 bootstrap replicates. Maximum likelihood analysis was also carried out with PhyML 3.0 [45] on the combined data, utilizing the AIC-chosen model (GTR+I+Γ), and generating 1000 bootstrap replicates. The neighbor-joining tree of the combined data was calculated in PAUP*4.0b10 [48] with 1000 bootstrap replicates, employing the evolutionary model selected above.

Bayesian inference was carried out in MrBayes 3.1.2 [49,50], using the resources of the Computational Biology Service Unit from Cornell University, with each partition modeled (Table 2) but unlinked for separate parameter estimations. Four Markov chains of 10 million generations were implemented in twelve runs, saving a tree every 100th generation. MCMC convergence among the runs was monitored using Tracer 1.5 [51], where we ascertained that only four of the twelve runs converged on the shortest trees (only two runs converged for the four-gene analysis; see [52-54]), and the first 40001 trees were to be discarded as burn-in.

Additionally, compensatory base changes because of the secondary structure of the ITS rDNA loci may lead to non-independence and increased homoplasy of characters [55-57]. Hence, analysis of the secondary structure of this region may result in a more rigorous phylogeny [58-61]. Using the ITS2 segment of each ITS sequence, secondary structure was predicted by searching the ITS2 database [62] for the best match template and then modeling its structure based on free energy minimization. The ITS2 sequences and their associated structural information were aligned using 4SALE 1.5 [63,64], and then exported for analysis in ProfDistS 0.9.8 [65-68]. The profile neighbor-joining algorithm was executed with 10000 bootstrap replicates on the RNA structural alignment, using the GTR model and rate matrix 'Q_ITS2.txt' for distance correction. ITS2 could not be amplified from Hydnophora microconos, H. pilosa and Merulina scabricula. Consequently these species were excluded from the analysis.

Results and Discussion

In this study, the evolutionary history of the 'Bigmessidae' corals was robustly reconstructed using five genes. Relations among other clade representatives chosen as outgroups were also inferred. The maximum likelihood reconstructions carried out by RAxML 7.2.3 and PhyML 3.0 had log likelihood values of -36224.67 and -36995.48, respectively. As they were identical when considering nodes with bootstrap values ≥50, we present the RAxML tree that garnered a higher likelihood score (Figures 1 and 2). A total of 182 most parsimonious trees (tree length = 6178) were obtained. No conflicts between tree optimization procedures (including Bayesian inference and the neighbor-joining algorithm) were apparent when considering only the supported nodes (bootstrap ≥50 and posterior probability ≥0.9) (see Additional file 2). Analyses excluding the ITS partition also gave congruent results. Several clades were consistent and well supported among maximum likelihood, parsimony and Bayesian inferences. We named some of these groups within clade XVII from A to I, consistent with the classification in Budd and Stolarski [69]. On the other hand, the neighbor-joining method generated a relatively unresolved tree—subclades A, C, F and I did not achieve bootstrap values of ≥50 (see Additional file 2).

Figure 1.

Figure 1

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Maximum likelihood tree of the combined molecular data. Species have been summarized into genera where possible. One asterisk denotes paraphyletic genus, two asterisks polyphyly, and three represents a genus that is both para- and polyphyletic. All taxa from conventional family Faviidae unless otherwise indicated. Clade designations XIV to XXI shown; clade XVII divided into well-supported subclades. Numbers adjacent to branches/taxa are support values (maximum likelihood bootstrap ≥50, maximum parsimony bootstrap ≥50, followed by Bayesian posterior probability ≥0.9). Filled circles indicate well-supported clades (bootstrap values ≥98 and posterior probability of 1).

Figure 2.

Figure 2

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Maximum likelihood topologies of each subclade. Numbers above branches are maximum likelihood bootstrap ≥50 and Bayesian posterior probability ≥0.9, while number below denotes maximum parsimony bootstrap ≥50. Family classification follows definitions given for Figure 1. Type species of genera are in bold.

The combined five-gene data yielded the most resolved phylogeny hitherto of clade XVII, with most branches garnering high support values. However, most partitions gave fairly unresolved trees when analyzed individually (see Additional file 3). By examining the support of subclades among trees obtained via different partitions, we found that nuclear markers contributed a greater extent to the final tree topology (Table 3). Histone H3, for instance, supported all higher-level groupings and all subclades except D/E (Figure 1). The 28S and ITS rDNA gene trees had moderate resolution within clade XVII, with only two unresolved subclades each. Surprisingly, the tree based on ITS2 rDNA secondary structure had less resolution than the primary sequence alignment. Indeed, the former has demonstrated potential for resolving intrageneric phylogenies in other anthozoans [70,71], but it is less informative for relationships at higher taxonomic levels [72,73]. Evidently, the COI tree was poorly resolved, with ≥50 bootstrap support for few relationships among major clades and only one subclade. The slow evolution of the mitochondrial COI gene among anthozoans is certainly the reason behind this [24,74,75]. While the intergenic marker (IGR) adjacent to COI on the mitochondrial genome has shown promise for phylogenetic reconstruction among Faviidae and Mussidae [15,23,76], it cannot be unambiguously aligned between the major clades. We urge the development of more nuclear phylogenetic markers that can be reliably applied across diverse scleractinian clades.

Table 3.

Clades supported by maximum likelihood analysis for each partition.

Clade Nuclear DNA mt DNA 28S rDNA histone H3 ITS
sequence		 ITS
structure		 mt COI mt IGR
XV to XXI √√ √√ √√ √√ √√ √√ √√
XV+XVI √√ X √√ √√ √ √√ XX
XVII to XXI √√ √√ √ √√ √√ √ √√
XXI √√ √√ √ √√
XIX+XX1 √√ √ √ √√ X √√ √
XVII √√ X √ √√ √ X X √√
XVII-A √√ X √√ √√ √√ X X X
XVII-B √√ X X √√ √√ √√ X √
XVII-C √√ XX √√ √√ √√ X X
XVII-D/E √√ XX X X √√ √ XX √√
XVII-F √√ X √√ √√ X √√ XX
XVII-G √√ √√ √√ √√ X X √ √√
XVII-H √√ X √√ √√ √√ √√ √√
XVII-I2 √√ X √√ √√ √√ √ X X
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1Montastraea multipunctata and Moseleya latistellata are herein considered as part of clade XIX+XX.

2Subclade I is expanded to include Montastraea salebrosa.

'√√': clade present with ≥50 bootstrap support; '√': clade present but not supported (<50 bootstrap); 'XX': contradicted clade with ≥50 bootstrap support; and 'X': contradicted clade not supported. Empty cells indicate insufficient data.

Most relationships among clades XV to XXI obtained in this study corroborate results of Fukami et al. [12] (Figure 1). The only difference occurs in the sister grouping of Diploastrea heliopora (XV) and Montastraea cavernosa (XVI) (supported by all analyses except Bayesian likelihood) that form a grade in Fukami et al. [12]. The monophyly of the clade XVII+XIX+XX (Pacific faviids and mussids) is recovered but not well supported. Montastraea multipunctata and Moseleya latistellata are Pacific faviids, and therefore presumably in clade XVII. But as a result of superficial similarities, they have historically been associated with the Pacific mussids Blastomussa merleti (clade XIV) [77] and Acanthastrea hillae (clade XVIII) [5,18], respectively. Here, we find them to be more closely related to clades XIX and XX instead, revealing a taxonomic situation more challenging than anticipated. Pacific faviids other than Diploastrea heliopora can no longer be restricted to clade XVII, and the possibility exists that yet-to-be sampled taxa provisionally placed in clade XVII—particularly the monotypic genera, Australogyra, Erythrastrea, Boninastrea and Paraclavarina—have unexpected affinities.

Nested within clade XVII are four conventional families—Faviidae, Merulinidae, Pectiniidae and Trachyphylliidae (Figure 1). Two Pectiniidae genera, Pectinia and Mycedium (XVII-E) form the sister clade to Oulophyllia. This is a similar relationship to the results of Fukami et al. [12], although here we also show with reasonable support that Oulophyllia is monophyletic, and Caulastraea is an outgroup rather than nested within Oulophyllia (XVII-D). Merulinidae is represented by Hydnophora, Merulina and Scapophyllia. Hydnophora is more closely related to Favites and Pacific Montastraea spp. than Merulina and Scapophyllia, which form a grade within the clade dominated by Goniastrea. The monospecific Trachyphylliidae is nested within the clade consisting primarily of Favia spp., and is sister to Favia lizardensis and F. truncatus (Figure 2). Work is ongoing to redescribe clade XVII by incorporating the above families and applying a new taxon name since the type species of Faviidae, Favia fragum (Esper, 1797), belongs to clade XXI [12].

The genetic affiliation of Hydnophora and Trachyphyllia with Faviidae has previously been proposed by Fukami et al. [8,12]. However, this is not exclusively a molecular hypothesis. Based on a combination of colony, corallite and subcorallite characters (e.g., polyp budding; wall, septal and columellar structures), Vaughan and Wells, 1943 [78], placed the two taxa within Faviidae. But later, Chevalier, 1975 [79], attempted to distinguish Trachyphyllia from Faviidae based on minor differences in wall and septal structures by elevating it to the rank of family. Correspondingly, Veron, 1985 [17], moved Hydnophora into Merulinidae because of Hydnophora species' macromorphological similarities (i.e., colony growth form and polyp structure) with Merulina ampliata and Scapophyllia cylindrica, which are genetically in the same lineage (subclade A) as several Goniastrea spp. and Favia stelligera (Figures 1 and 2; see also [8,12]).

Montastraea annularis and likely other members of the species complex (M. faveolata and M. franksi) are the only Atlantic species in clade XVII (see also [8,12]). Most significantly here, M. annularis is sister to Cyphastrea, forming clade XVII-C (Figure 1). This placement may seem bizarre in the context of traditional macromorphological characters used to classify scleractinians (e.g., [4,78]). However, recent work at the microstructural scale (centers of rapid accretion and thickening deposits) has suggested that their septothecal walls (formed by fusion of outer margins of septa) may unite the two taxa [69] (see also [80]). These subcorallite features appear to be appropriate synapomorphies for other subclades. For instance, clade XVII-A consists of Merulina, Scapophyllia, Goniastrea A and Favia stelligera (Figure 2). At the corallite level, these corals cannot be reconciled within the same taxon, since Favia stelligera corallites have single centers with separate walls (plocoid), Goniastrea spp. have fused walls (cerioid) and may form valleys (meandroid), while Merulina and Scapophyllia are composed predominantly of elongated valleys (see Additional file 1). On the other hand, they share the apomorphy of having septothecal walls with abortive septa (thin bands between normal septa with their own centers of rapid accretion).

The use of macromorphology for identifying 'Bigmessidae' species is known for being problematic as most of these characters are homoplasious [15,80,81]. The ability to distinguish clades based on microstructural features is encouraging for scleractinian systematics. Micromorphology, at the scale of septal teeth and granules, has also exhibited promise as phylogenetic characters [25,80,82-85]. Interestingly, in light of recent molecular hypotheses, other biological traits, in particular, sexuality and to a lesser extent, breeding mode appear highly conserved and could be further developed as phylogenetic markers [86,87].

Prior to the use of molecular data to build evolutionary trees, it was a great challenge to determine which morphological characters could be useful for classification, given their intraspecific variability [32,88] and phenotypic plasticity [89-94]. Indeed, the general anthozoan body plan is relatively simple, and scleractinians in particular have few discrete morphological characters that are known to be phylogenetically informative at the polyp level [4,95-97]. As a result of the recent disarray in coral systematics, morphological taxonomies of scleractinians have been heavily criticized (e.g., [8,12,98,99]). Molecular characters, which are much more numerous and arguably neutrally evolving, can certainly aid our understanding of evolutionary relationships. However, morphological evidence supporting various molecular clades in the present analysis suggests that morphology at novel scales will play an essential role in the taxonomy of 'Bigmessidae' [80].

Widespread sampling in this study has shown that corals thought to belong to the same species across the central Indo-Pacific are actually from distinct lineages. Consider Goniastrea australensis (Milne Edwards and Haime, 1857), which occurs in two clades (Figures 1 and 2; see also Additional file 1). Since this species was first described from Australia, the Australian specimen that clustered with Favites russelli and Montastraea curta should be considered G. australensis, while the two specimens from Singapore (S088 and S098, subclade A) probably represent new species yet to be described. This is certainly not an isolated case. A similar situation is revealed for Montastraea valenciennesi. Specimens from Australia (G61904) and Singapore (S006 and S008) are in subclade B of mostly Favia spp., while the representative from the Philippines (P102) is in subclade F, a distant clade comprising mainly Favites species. Interestingly, two reproductively isolated morphotypes of M. valenciennesi were recently found to co-occur in Wakayama (Japan), distinguished by the degree of wall fusion among corallites [100]. Chevalier, 1971 [101], upon examination of the holotype, placed the species in Favia on the basis of corallites possessing separate walls and budding intratentacularly (see also [102-108]). This suggests that the name Favia valenciennesi (Milne Edwards and Haime, 1848) could be applied to the Australian and Singaporean specimens in subclade B, while P102 (subclade F) is a new species.

Less extensive issues occur among Goniastrea and Favia species. For instance, G. pectinata (subclade A), collected from three locations, is clearly paraphyletic, with G. australensis and G. favulus nested within them (Figure 2). For Favia (subclade B), of six F. favus specimens collected from three localities, only three of these form a supported clade while the rest are dispersed within clade XVII-B with no apparent biogeographical pattern. The nesting of Barabattoia amicorum among Favia spp. has been consistently recovered in recent molecular phylogenies [12,15], but this affinity was in fact the dominant hypothesis [5,107-109] until Veron, 1986 [18], included the species in its current genus. Conversely, Favia rotundata clusters with Favites spp. rather than its congeners, but it was indeed originally described as Favites rotundata Veron, Pichon and Wijsman-Best, 1977 [5] (see also [109,110]).

The polyphyly of most 'Bigmessidae' genera seems to confer a bleak outlook for revisionary work. However, as we have shown in Figure 1, several genera can be clearly grouped as clades with limited name changes. For instance, subclade F is composed of species from Favites Link, 1807, Montastraea de Blainville, 1830, and Favia Ehrenberg, 1834 (Figure 2). While the remaining Favites spp. (i.e., F. pentagona, F. russelli, and F. stylifera) are not included within this subclade, the type species of this genus is Favites abdita (Ellis and Solander, 1786, type locality 'Probablement les mers des Grandes-Indes', Lamarck, 1816 [111]). The representative of the latter we used falls well within subclade F. Since no other type species were recovered and with Favites Link, 1807, being the oldest valid genus in the subclade, Favites should be expanded to include the other species, while F. pentagona, F. russelli and F. stylifera will have to be subsumed within other genera. Several other multi-species genera in fact appear stable: Caulastraea, Cyphastrea, Echinopora, Hydnophora, Leptoria, Merulina and Oulophyllia. Name changes are certainly not necessary for Favites and Platygyra, since they host their respective type species in the subclades shown in Figure 2.

Conclusions

Numerous instances of cryptic taxa determined in this study support the assertion that coral diversity estimates have been fraught with errors [8]. Traits relating to the gross skeletal morphology of corals are unreliable for species description and identification because of their potential for intraspecific variability [32,88] and environment-induced plasticity [89-94]. Yet, these characters have served as the foundation for scleractinian taxonomy (e.g., [4,5]). Fortunately, using molecular data, the recovery of most genera within the 'Bigmessidae' with only minor degrees of paraphyly spells hope for impending taxonomic amendments. Our results show that most genera only require slight revisions, and most major changes are necessary only at the level of the major clades described in Fukami et al. [12]. Certainly, broad taxonomic sampling within Faviidae has revealed more species with unexpected affinities, such as Moseleya latistellata and Montastraea multipunctata. Clade XVII may consequently have to be redefined to exclude them.

Nevertheless, 'Bigmessidae' subclades are well defined and will no doubt provide a robust framework for taxonomic revisions. The fact that microstructural features support 'Bigmessidae' subclades also offers hope for the morphological approach. Evolutionary relationships among subclades are still provisional due to insufficient statistical support, but they can be clarified with further sampling of nuclear sequences. Eventually, a well-resolved tree of a redescribed clade XVII will be available to reconstruct the morphological evolution of 'Bigmessidae' at various scales.

Authors' contributions

DH obtained the DNA sequences in the laboratory, performed the phylogenetic analyses, and had a major role in writing the manuscript. All authors collected the specimens examined, contributed to and approved the final manuscript.

Supplementary Material

Additional file 1

'Bigmessidae' corals. Photographs of most coral specimens sequenced in this study. More photographs are available from the authors.

Click here for file (10.9MB, PDF)
Additional file 2

Maximum likelihood tree topology of the combined molecular data. Numbers above branches are maximum likelihood bootstrap ≥50 and Bayesian posterior probability ≥0.9, while numbers below denote maximum parsimony bootstrap ≥50 and neighbor-joining bootstrap ≥50. Family classification follows definitions given for Figure 1.

Click here for file (131.9KB, PDF)
Additional file 3

Maximum likelihood tree topology of each partition. Numbers adjacent to branches are bootstrap support values ≥50. Definitions for family classification follow Figure 1.

Click here for file (686.7KB, PDF)

Contributor Information

Danwei Huang, Email: huangdanwei@ucsd.edu.

Wilfredo Y Licuanan, Email: licuananw@dlsu.edu.ph.

Andrew H Baird, Email: andrew.baird@jcu.edu.au.

Hironobu Fukami, Email: hirofukami@cc.miyazaki-u.ac.jp.

Acknowledgements

We thank all who helped with the field collections, including Zeehan Jaafar, Ywee Chieh Tay, Katrina Luzon, Norievill Espana, Eznairah-Jeung Narida and Monica Orquieza. Flavia Nunes kindly provided the Atlantic specimens. We acknowledge Ann Budd for critical discussions on coral morphology; Carmen Ablan-Lagman and Glenn Oyong for lab support at De La Salle University; Rudolf Meier, Loke Ming Chou and Peter Todd for lab support at National University of Singapore; Carden Wallace, Paul Muir and Barbara Done for museum support at Museum of Tropical Queensland; and staff of Orpheus Island Research Station for field support at Orpheus Island. Special thanks go to Gregory Rouse and Nancy Knowlton for valuable advice and support. For comments on this manuscript, we thank Liz Borda, Tito Lotufo, Yun Lei Tan, three anonymous reviewers and the Associate Editor. Collections were made in Australia under Great Barrier Reef Marine Park Authority permit G09/29715.1, and in the Philippines under Department of Agriculture gratuitous permit FBP-0027-09. This study is partly funded by National Geographic Committee for Research and Exploration grant 8449-08.

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Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Supplementary Materials

Additional file 1

'Bigmessidae' corals. Photographs of most coral specimens sequenced in this study. More photographs are available from the authors.

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Additional file 2

Maximum likelihood tree topology of the combined molecular data. Numbers above branches are maximum likelihood bootstrap ≥50 and Bayesian posterior probability ≥0.9, while numbers below denote maximum parsimony bootstrap ≥50 and neighbor-joining bootstrap ≥50. Family classification follows definitions given for Figure 1.

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Additional file 3

Maximum likelihood tree topology of each partition. Numbers adjacent to branches are bootstrap support values ≥50. Definitions for family classification follow Figure 1.

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