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

  • Danwei Huang1, 2Email author,

    Affiliated with

    • Wilfredo Y Licuanan3,

      Affiliated with

      • Andrew H Baird4 and

        Affiliated with

        • Hironobu Fukami5

          Affiliated with

          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).
          http://static-content.springer.com/image/art%3A10.1186%2F1471-2148-11-37/MediaObjects/12862_2010_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).

          http://static-content.springer.com/image/art%3A10.1186%2F1471-2148-11-37/MediaObjects/12862_2010_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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