The amphibian tree of life

FROST, D. R., T. GRANT, J. FAIVOVICH, A. HAAS, C. F. B. HADDAD, R. BAIN, R. O. DE SÁ, S. C. DONNELLAN, C. J. RAXWORTHY, M. WILKINSON, A. CHANNING, J. A. CAMPBELL, B. L. BLOTTO, P. MOLER, R. C. DREWES, R. A. NUSSBAUM, J. D. LYNCH, D. GREEN, W. C. WHEELER

Bulletin of the American Museum of Natural History

American Museum of Natural History

Año: 2006 p. 1 - 370

The evidentiary basis of the currently accepted classification of living amphibians is discussedand shown not to warrant the degree of authority conferred on it by use and tradition.A new taxonomy of living amphibians is proposed to correct the deficiencies of the old one.This new taxonomy is based on the largest phylogenetic analysis of living Amphibia so faraccomplished. We combined the comparative anatomical character evidence of Haas (2003)with DNA sequences from the mitochondrial transcription unit H1 (12S and 16S ribosomalRNA and tRNAValine genes, ø 2,400 bp of mitochondrial sequences) and the nuclear geneshistone H3, rhodopsin, tyrosinase, and seven in absentia, and the large ribosomal subunit 28S(ø 2,300 bp of nuclear sequences; ca. 1.8 million base pairs; x¯ 5 3.7 kb/terminal). The datasetincludes 532 terminals sampled from 522 species representative of the global diversity ofamphibians as well as seven of the closest living relatives of amphibians for outgroup comparisons.The primary purpose of our taxon sampling strategy was to provide strong tests of themonophyly of all ‘‘family-group’’ taxa. All currently recognized nominal families and subfamilieswere sampled, with the exception of Protohynobiinae (Hynobiidae). Many of the currentlyrecognized genera were also sampled. Although we discuss the monophyly of genera, andprovide remedies for nonmonophyly where possible, we also make recommendations for futureresearch.A parsimony analysis was performed under Direct Optimization, which simultaneously optimizesnucleotide homology (alignment) and tree costs, using the same set of assumptionsthroughout the analysis. Multiple search algorithms were run in the program POY over aperiod of seven months of computing time on the AMNH Parallel Computing Cluster.Results demonstrate that the following major taxonomic groups, as currently recognized,are nonmonophyletic: Ichthyophiidae (paraphyletic with respect to Uraeotyphlidae), Caeciliidae(paraphyletic with respect to Typhlonectidae and Scolecomorphidae), Salamandroidea(paraphyletic with respect to Sirenidae), Leiopelmatanura (paraphyletic with respect to Ascaphidae),Discoglossanura (paraphyletic with respect to Bombinatoridae), Mesobatrachia (paraphyleticwith respect to Neobatrachia), Pipanura (paraphyletic with respect to Bombinatoridaeand Discoglossidae/Alytidae), Hyloidea (in the sense of containing Heleophrynidae; paraphyleticwith respect to Ranoidea), Leptodactylidae (polyphyletic, with Batrachophrynidae formingthe sister taxon of Myobatrachidae 1 Limnodynastidae, and broadly paraphyletic withrespect to Hemiphractinae, Rhinodermatidae, Hylidae, Allophrynidae, Centrolenidae, Brachycephalidae,Dendrobatidae, and Bufonidae), Microhylidae (polyphyletic, with Brevicipitinaebeing the sister taxon of Hemisotidae), Microhylinae (poly/paraphyletic with respect to theremaining non-brevicipitine microhylids), Hyperoliidae (para/polyphyletic, with Leptopelinaeforming the sister taxon of Arthroleptidae 1 Astylosternidae), Astylosternidae (paraphyleticwith respect to Arthroleptinae), Ranidae (paraphyletic with respect to Rhacophoridae and Mantellidae).In addition, many subsidiary taxa are demonstrated to be nonmonophyletic, such as(1) Eleutherodactylus with respect to Brachycephalus; (2) Rana (sensu Dubois, 1992), whichis polyphyletic, with various elements falling far from each other on the tree; and (3) Bufo,with respect to several nominal bufonid genera.A new taxonomy of living amphibians is proposed, and the evidence for this is presentedto promote further investigation and data acquisition bearing on the evolutionary history ofamphibians. The taxonomy provided is consistent with the International Code of ZoologicalNomenclature (ICZN, 1999).Salient features of the new taxonomy are (1) the three major groups of living amphibians,caecilians/Gymnophiona, salamanders/Caudata, and frogs/Anura, form a monophyletic group,to which we restrict the name Amphibia; (2) Gymnophiona forms the sister taxon of Batrachia(salamanders 1 frogs) and is composed of two groups, Rhinatrematidae and Stegokrotaphia;(3) Stegokrotaphia is composed of two families, Ichthyophiidae (including Uraeotyphlidae)and Caeciliidae (including Scolecomorphidae and Typhlonectidae, which are regarded as subfamilies);(4) Batrachia is a highly corroborated monophyletic group, composed of two taxa,Caudata (salamanders) and Anura (frogs); (5) Caudata is composed of two taxa, Cryptobranchoidei(Cryptobranchidae and Hynobiidae) and Diadectosalamandroidei new taxon (all othersalamanders); (6) Diadectosalamandroidei is composed of two taxa, Hydatinosalamandroideinew taxon (composed of Perennibranchia and Treptobranchia new taxon) and Plethosalamandroideinew taxon; (7) Perennibranchia is composed of Proteidae and Sirenidae; (8) Treptobranchianew taxon is composed of two taxa, Ambystomatidae (including Dicamptodontidae)and Salamandridae; (9) Plethosalamandroidei new taxon is composed of Rhyacotritonidaeand Xenosalamandroidei new taxon; (10) Xenosalamandroidei is composed of Plethodontidaeand Amphiumidae; (11) Anura is monophyletic and composed of two clades, Leiopelmatidae(including Ascaphidae) and Lalagobatrachia new taxon (all other frogs); (12) Lalagobatrachiais composed of two clades, Xenoanura (Pipidae and Rhinophrynidae) and Sokolanura newtaxon (all other lalagobatrachians); (13) Bombinatoridae and Alytidae (former Discoglossidae)are each others’ closest relatives and in a clade called Costata, which, excluding Leiopelmatidaeand Xenoanura, forms the sister taxon of all other frogs, Acosmanura; (14) Acosmanurais composed of two clades, Anomocoela (5 Pelobatoidea of other authors) and Neobatrachia;(15) Anomocoela contains Pelobatoidea (Pelobatidae and Megophryidae) and Pelodytoidea(Pelodytidae and Scaphiopodidae), and forms the sister taxon of Neobatrachia, together formingAcosmanura; (16) Neobatrachia is composed of two clades, Heleophrynidae, and all otherneobatrachians, Phthanobatrachia new taxon; (17) Phthanobatrachia is composed of two majorunits, Hyloides and Ranoides; (18) Hyloides comprises Sooglossidae (including Nasikabatrachidae)and Notogaeanura new taxon (the remaining hyloids); (19) Notogaeanura contains twotaxa, Australobatrachia new taxon and Nobleobatrachia new taxon; (20) Australobatrachia isa clade composed of Batrachophrynidae and its sister taxon, Myobatrachoidea (Myobatrachidaeand Limnodynastidae), which forms the sister taxon of all other hyloids, excluding sooglossids;(21) Nobleobatrachia new taxon, is dominated at its base by frogs of a treefrogmorphotype, several with intercalary phalangeal cartilages—Hemiphractus (Hemiphractidae)forms the sister taxon of the remaining members of this group, here termed Meridianura newtaxon; (22) Meridianura comprises Brachycephalidae (former Eleutherodactylinae 1 Brachycephalus)and Cladophrynia new taxon; (23) Cladophrynia is composed of two groups, Cryptobatrachidae(composed of Cryptobatrachus and Stefania, previously a fragment of the polyphyleticHemiphractinae) and Tinctanura new taxon; (24) Tinctanura is composed of Amphignathodontidae(Gastrotheca and Flectonotus, another fragment of the polyphyletic Hemiphractinae)and Athesphatanura new taxon; (25) Athesphatanura is composed of Hylidae(Hylinae, Pelodryadinae, and Phyllomedusinae, and excluding former Hemiphractinae, whoseinclusion would have rendered this taxon polyphyletic) and Leptodactyliformes new taxon;(26) Leptodactyliformes is composed of Diphyabatrachia new taxon (composed of Centrolenidae[including Allophryne] and Leptodactylidae, sensu stricto, including Leptodactylus andrelatives) and Chthonobatrachia new taxon; (27) Chthonobatrachia is composed of a reformulatedCeratophryidae (which excludes such genera as Odontophrynus and Proceratophrysand includes other taxa, such as Telmatobius) and Hesticobatrachia new taxon; (28) Hesticobatrachiais composed of a reformulated Cycloramphidae (which includes Rhinoderma) andAgastorophrynia new taxon; (29) Agastorophrynia is composed of Bufonidae (which is partiallyrevised) and Dendrobatoidea (Dendrobatidae and Thoropidae); (30) Ranoides new taxonforms the sister taxon of Hyloides and is composed of two major monophyletic components,Allodapanura new taxon (microhylids, hyperoliids, and allies) and Natatanura new taxon(ranids and allies); (31) Allodapanura is composed of Microhylidae (which is partially revised)and Afrobatrachia new taxon; (32) Afrobatrachia is composed of Xenosyneunitanura newtaxon (the ‘‘strange-bedfellows’’ Brevicipitidae [formerly in Microhylidae] and Hemisotidae)and a more normal-looking group of frogs, Laurentobatrachia new taxon (Hyperoliidae andArthroleptidae, which includes Leptopelinae and former Astylosternidae); (33) Natatanura newtaxon is composed of two taxa, the African Ptychadenidae and the worldwide Victoranuranew taxon; (34) Victoranura is composed of Ceratobatrachidae and Telmatobatrachia newtaxon; (35) Telmatobatrachia is composed of Micrixalidae and a worldwide group of ranoids,Ametrobatrachia new taxon; (36) Ametrobatrachia is composed of Africanura new taxon andSaukrobatrachia new taxon; (37) Africanura is composed of two taxa: Phrynobatrachidae(Phrynobatrachus, including Dimorphognathus and Phrynodon as synonyms) and Pyxicephaloidea;(38) Pyxicephaloidea is composed of Petropedetidae (Conraua, Indirana, Arthroleptides,and Petropedetes), and Pyxicephalidae (including a number of African genera, e.g.Amietia [including Afrana], Arthroleptella, Pyxicephalus, Strongylopus, and Tomopterna); and(39) Saukrobatrachia new taxon is the sister taxon of Africanura and is composed of Dicroglossidae and Aglaioanura new taxon, which is, in turn, composed of Rhacophoroidea (Mantellidaeand Rhacophoridae) and Ranoidea (Nyctibatrachidae and Ranidae, sensu stricto).Many generic revisions are made either to render a monophyletic taxonomy or to render ataxonomy that illuminates the problems in our understanding of phylogeny, so that future workwill be made easier. These revisions are: (1) placement of Ixalotriton and Lineatriton (Caudata:Plethodontidae: Bolitoglossinae) into the synonymy of Pseudoeurycea, to render a monophyleticPseudoeurycea; (2) placement of Haideotriton (Caudata: Plethodontidae: Spelerpinae)into the synonymy of Eurycea, to render a monophyletic Eurycea; (3) placement of Nesomantis(Anura: Sooglossidae) into the synonymy of Sooglossus, to assure a monophyletic Sooglossus;(4) placement of Cyclorana and Nyctimystes (Anura: Hylidae: Pelodryadinae) into Litoria, butretaining Cyclorana as a subgenus, to provide a monophyletic Litoria; (5) partition of ‘‘Limnodynastes’’(Anura: Limnodynastidae) into Limnodynastes and Opisthodon to render monophyleticgenera; (6) placement of Adenomera, Lithodytes, and Vanzolinius (Anura: Leptodactylidae)into Leptodactylus, to render a monophyletic Leptodactylus; (7) partition of ‘‘Eleutherodactylus’’(Anura: Brachycephalidae) into Craugastor, ‘‘Eleutherodactylus’’, ‘‘Euhyas’’,‘‘Pelorius’’, and Syrrhophus to outline the taxonomic issues relevant to the paraphyly of thisnominal taxon to other nominal genera; (8) partition of ‘‘Bufo’’ (Anura: Bufonidae) into anumber of new or revived genera (i.e., Amietophrynus new genus, Anaxyrus, Chaunus, Cranopsis,Duttaphrynus new genus, Epidalea, Ingerophrynus new genus, Nannophryne, Peltophryne,Phrynoidis, Poyntonophrynus new genus; Pseudepidalea new genus, Rhaebo, Rhinella,Vandijkophrynus new genus); (9) placement of the monotypic Spinophrynoides (Anura:Bufonidae) into the synonymy of (formerly monotypic) Altiphrynoides to make for a moreinformative taxonomy; (10) placement of the Bufo taitanus group and Stephopaedes (as asubgenus) into the synonymy of Mertensophryne (Anura: Bufonidae); (11) placement of Xenobatrachus(Anura: Microhylidae: Asterophryinae) into the synonymy of Xenorhina to rendera monophyletic Xenorhina; (12) transfer of a number of species from Plethodontohyla toRhombophryne (Microhylidae: Cophylinae) to render a monophyletic Plethodontohyla; (13)placement of Schoutedenella (Anura: Arthroleptidae) into the synonymy of Arthroleptis; (14)transfer of Dimorphognathus and Phrynodon (Anura: Phrynobatrachidae) into the synonymyof Phrynobatrachus to render a monophyletic Phrynobatrachus; (15) placement of Afrana intothe synonymy of Amietia (Anura: Pyxicephalidae) to render a monophyletic taxon; (16) placementof Chaparana and Paa into the synonymy of Nanorana (Anura: Dicroglossidae) to rendera monophyletic genus; (17) recognition as genera of Ombrana and Annandia (Anura: Dicroglossidae:Dicroglossinae) pending placement of them phylogenetically; (18) return of Phrynoglossusinto the synonymy of Occidozyga to resolve the paraphyly of Phrynoglossus (Anura:Dicroglossidae: Occidozyginae); (19) recognition of Feihyla new genus for Philautus palpebralisto resolve the polyphyly of ‘‘Chirixalus’’; (20) synonymy of ‘‘Chirixalus’’ with Chiromantisto resolve the paraphyly of ‘‘Chirixalus’’; (21) recognition of the genus Babina,composed of the former subgenera of Rana, Babina and Nidirana (Anura: Ranidae); (22)recognition of the genera Clinotarsus, Humerana, Nasirana, Pelophylax, Pterorana, Pulchrana,and Sanguirana, formerly considered subgenera of Rana (Anura: Ranidae), with nospecial relationship to Rana (sensu stricto); (23) consideration of Glandirana (Anura: Ranidae),formerly a subgenus of Rana, as a genus, with Rugosa as a synonym; (24) recognition ofHydrophylax (Anura: Ranidae) as a genus, with Amnirana and most species of former Chalcoranaincluded in this taxon as synonyms; (25) recognition of Hylarana (Anura: Ranidae)as a genus and its content redefined; (26) redelimitation of Huia to include as synonymsEburana and Odorrana (both former subgenera of Rana); (27) recognition of Lithobates (Anura:Ranidae) for all species of North American ‘‘Rana’’ not placed in Rana sensu stricto(Aquarana, Pantherana, Sierrana, Trypheropsis, and Zweifelia considered synonyms of Lithobates);(28) redelimitation of the genus Rana as monophyletic by inclusion as synonymsAmerana, Aurorana, Pseudoamolops, and Pseudorana, and exclusion of all other former subgenera;(29) redelimitation of the genus Sylvirana (Anura: Ranidae), formerly a subgenus ofRana, with Papurana and Tylerana included as synonyms.