THE AMPHIBIAN TREE OF LIFE

Abstract The evidentiary basis of the currently accepted classification of living amphibians is discussed and 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 far accomplished. We combined the comparative anatomical character evidence of Haas (2003) with DNA sequences from the mitochondrial transcription unit H1 (12S and 16S ribosomal RNA and tRNAValine genes, ≈ 2,400 bp of mitochondrial sequences) and the nuclear genes histone H3, rhodopsin, tyrosinase, and seven in absentia, and the large ribosomal subunit 28S (≈ 2,300 bp of nuclear sequences; ca. 1.8 million base pairs; x̄ = 3.7 kb/terminal). The dataset includes 532 terminals sampled from 522 species representative of the global diversity of amphibians 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 the monophyly of all “family-group” taxa. All currently recognized nominal families and subfamilies were sampled, with the exception of Protohynobiinae (Hynobiidae). Many of the currently recognized genera were also sampled. Although we discuss the monophyly of genera, and provide remedies for nonmonophyly where possible, we also make recommendations for future research. A parsimony analysis was performed under Direct Optimization, which simultaneously optimizes nucleotide homology (alignment) and tree costs, using the same set of assumptions throughout the analysis. Multiple search algorithms were run in the program POY over a period 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 (paraphyletic with respect to Neobatrachia), Pipanura (paraphyletic with respect to Bombinatoridae and Discoglossidae/Alytidae), Hyloidea (in the sense of containing Heleophrynidae; paraphyletic with respect to Ranoidea), Leptodactylidae (polyphyletic, with Batrachophrynidae forming the sister taxon of Myobatrachidae + Limnodynastidae, and broadly paraphyletic with respect to Hemiphractinae, Rhinodermatidae, Hylidae, Allophrynidae, Centrolenidae, Brachycephalidae, Dendrobatidae, and Bufonidae), Microhylidae (polyphyletic, with Brevicipitinae being the sister taxon of Hemisotidae), Microhylinae (poly/paraphyletic with respect to the remaining non-brevicipitine microhylids), Hyperoliidae (para/polyphyletic, with Leptopelinae forming the sister taxon of Arthroleptidae + Astylosternidae), Astylosternidae (paraphyletic with 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), which is 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 presented to promote further investigation and data acquisition bearing on the evolutionary history of amphibians. The taxonomy provided is consistent with the International Code of Zoological Nomenclature (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 + 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 other salamanders); (6) Diadectosalamandroidei is composed of two taxa, Hydatinosalamandroidei new taxon (composed of Perennibranchia and Treptobranchia new taxon) and Plethosalamandroidei new taxon; (7) Perennibranchia is composed of Proteidae and Sirenidae; (8) Treptobranchia new taxon is composed of two taxa, Ambystomatidae (including Dicamptodontidae) and Salamandridae; (9) Plethosalamandroidei new taxon is composed of Rhyacotritonidae and Xenosalamandroidei new taxon; (10) Xenosalamandroidei is composed of Plethodontidae and Amphiumidae; (11) Anura is monophyletic and composed of two clades, Leiopelmatidae (including Ascaphidae) and Lalagobatrachia new taxon (all other frogs); (12) Lalagobatrachia is composed of two clades, Xenoanura (Pipidae and Rhinophrynidae) and Sokolanura new taxon (all other lalagobatrachians); (13) Bombinatoridae and Alytidae (former Discoglossidae) are each others' closest relatives and in a clade called Costata, which, excluding Leiopelmatidae and Xenoanura, forms the sister taxon of all other frogs, Acosmanura; (14) Acosmanura is composed of two clades, Anomocoela (= 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 forming Acosmanura; (16) Neobatrachia is composed of two clades, Heleophrynidae, and all other neobatrachians, Phthanobatrachia new taxon; (17) Phthanobatrachia is composed of two major units, Hyloides and Ranoides; (18) Hyloides comprises Sooglossidae (including Nasikabatrachidae) and Notogaeanura new taxon (the remaining hyloids); (19) Notogaeanura contains two taxa, Australobatrachia new taxon and Nobleobatrachia new taxon; (20) Australobatrachia is a clade composed of Batrachophrynidae and its sister taxon, Myobatrachoidea (Myobatrachidae and 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 treefrog morphotype, several with intercalary phalangeal cartilages—Hemiphractus (Hemiphractidae) forms the sister taxon of the remaining members of this group, here termed Meridianura new taxon; (22) Meridianura comprises Brachycephalidae (former Eleutherodactylinae + Brachycephalus) and Cladophrynia new taxon; (23) Cladophrynia is composed of two groups, Cryptobatrachidae (composed of Cryptobatrachus and Stefania, previously a fragment of the polyphyletic Hemiphractinae) 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, whose inclusion 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 and relatives) and Chthonobatrachia new taxon; (27) Chthonobatrachia is composed of a reformulated Ceratophryidae (which excludes such genera as Odontophrynus and Proceratophrys and includes other taxa, such as Telmatobius) and Hesticobatrachia new taxon; (28) Hesticobatrachia is composed of a reformulated Cycloramphidae (which includes Rhinoderma) and Agastorophrynia new taxon; (29) Agastorophrynia is composed of Bufonidae (which is partially revised) and Dendrobatoidea (Dendrobatidae and Thoropidae); (30) Ranoides new taxon forms 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 new taxon (the “strange-bedfellows” Brevicipitidae [formerly in Microhylidae] and Hemisotidae) and a more normal-looking group of frogs, Laurentobatrachia new taxon (Hyperoliidae and Arthroleptidae, which includes Leptopelinae and former Astylosternidae); (33) Natatanura new taxon is composed of two taxa, the African Ptychadenidae and the worldwide Victoranura new taxon; (34) Victoranura is composed of Ceratobatrachidae and Telmatobatrachia new taxon; (35) Telmatobatrachia is composed of Micrixalidae and a worldwide group of ranoids, Ametrobatrachia new taxon; (36) Ametrobatrachia is composed of Africanura new taxon and Saukrobatrachia 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 (Mantellidae and Rhacophoridae) and Ranoidea (Nyctibatrachidae and Ranidae, sensu stricto). Many generic revisions are made either to render a monophyle