Open Access

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

  • Danwei Huang1, 2Email author,
  • Wilfredo Y Licuanan3,
  • Andrew H Baird4 and
  • Hironobu Fukami5
BMC Evolutionary Biology201111:37

DOI: 10.1186/1471-2148-11-37

Received: 15 June 2010

Accepted: 7 February 2011

Published: 7 February 2011

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., [611]). 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, 1621]. 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

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, 2224]. 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, 2527].
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]

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 [2733]. 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 [3537] 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 [5254]), 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 [5557]. Hence, analysis of the secondary structure of this region may result in a more rigorous phylogeny [5861]. 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 [6568]. 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).
https://static-content.springer.com/image/art%3A10.1186%2F1471-2148-11-37/MediaObjects/12862_2010_Article_1998_Fig1_HTML.jpg
Figure 1

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).

https://static-content.springer.com/image/art%3A10.1186%2F1471-2148-11-37/MediaObjects/12862_2010_Article_1998_Fig2_HTML.jpg
Figure 2

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

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, 8285]. 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 [8994]. 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, 9597]. 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 [102108]). 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, 107109] 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 [8994]. 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.

Declarations

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.

Authors’ Affiliations

(1)
Scripps Institution of Oceanography, University of California
(2)
Department of Biological Sciences, National University of Singapore
(3)
Br. Alfred Shields Marine Station and Biology Department, De La Salle University
(4)
ARC Center of Excellence for Coral Reef Studies, James Cook University
(5)
Department of Marine Biology and Environmental Science, University of Miyazaki

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