Volume 52(12):141149, 2012

Phylogenetic relationshiPs of the genus SibynophiS (serPentes: colubroidea)

hussam Zaher1,6 feliPe g. graZZiotin1,2 roberta graboski1,2 ricardo g. fuentes1 Paola sncheZ-martineZ1 giovanna g. montingelli1 ya-Ping Zhang3,4 robert W. murPhy3,5
AbstrAct We present the results of the first molecular analysis of the phylogenetic affinities of the Asian colubroid genus Sibynophis. We recovered a sister-group relationship between Sibynophis and the New World Scaphiodontophis. Although Liophidium sometimes is associated with these genera, the relationship is distant. Morphological characters that Liophidium shares with Sibynophis and Scaphiodontophis are resolved as homoplasies that probably reflect the similarities of their specialized feeding habits. The traditional subfamily Sibynophiinae is elevated to the family-level, and Scaphiodontophiinae is placed in its synonymy. Key-Words: Sibynophiidae; Sibynophis; Scaphiodontophis; Phylogeny. IntroductIon The genera Liophidium, Sibynophis, and Scaphiodontophis occur on three distinct landmasses Madagascar, Asia, and Central America, respectively. Despite their isolation, these snakes long have been thought to be closely related to each other. In each genus, the dentary bears a peculiar posterior dentigerous process that is completely detached from the compound bone and teeth are numerous and closely set (Dumril et al., 1854; Boulenger, 1890, 1896). Dumril et al. (1854) were the first authors to place the four species that share these morphological characteristics in the subgenus Enicognathus of their genus Ablabes. Later, Boulenger (1890) substituted Enicognathus, preoccupied, with Polyodontophis

1. Museu de Zoologia, Universidade de So Paulo. Caixa Postal 42.494, 04218-970, So Paulo, SP, Brasil. 2. Programa de Ps-Graduao em Zoologia, Universidade Estadual Paulista, Rio Claro, SP, Brasil. 3. Laboratory for Conservation and Utilization of Bio-resources, Yunnan University, Kunming 650091, P.R. China. 4. State Key Laboratory of Genetic Resources and Evolution, Kunming Institute of Zoology, the Chinese Academy of Sciences, Kunming 650223, P.R. China. 5. Centre for Biodiversity and Conservation Biology, Royal Ontario Museum, 100 Queens Park, Toronto, Canada M5S 2C6. 6. E-mail correspondence to: hussam.zaher@gmail.com

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that he recognized as a genus. He added four additional species from India and southeastern Asia to Polyodontophis, as well as P. comorensis (= Liophidium mayottensis) and P. sumichrasti from the Comoros Islands and Central America, respectively. Boulenger (1896) further expanded Polyodontophis with three additional species, and described the genus Liophidium, to accommodate L. trilineatum from Madagascar. Polyodontophis was posteriorly synonymized with Fitzingers (1843) Sibynophis when Stejneger (1910) noted the latter genus has priority over the former, an arrangement followed by all subsequent authors (e.g., Dunn, 1928; Smith, 1943; Taylor & Smith, 1943). Dunn (1928) partially formalized Dumrils and Boulengers perspectives by erecting the subfamily Sibynophiinae to accommodate the Asian and Central American species of the genus Sibynophis, but he did not include the Malagasy taxa. Although Dunn did not explicitly refer to the Malagasy species of Sibynophis, he implicitly considered them to be unrelated to the Asian and Central American species. According to Dunn (1928), both Asian and Central American Sibynophis retain a single-lobed hemipenis with a single sulcus spermaticusa condition strikingly distinct from the bilobed hemipenis with a forked sulcus that occurs in the Malagasy species of Sibynophis. Taken together, both dentitional and hemipenial similarities between the Asiatic and New World species were so compelling that Dunn decided to consider them congeneric (Dunn, 1928: 20). It was only after Taylor & Smith (1943) that the New World species of Sibynophis were allocated in a distinct genus Scaphiodontophis. After Dunn (1928), Bogert (1940) briefly discussed the hemipenial differences between the Malagasy Sibynophis torquatus and its Asiatic and Central American congeners, but he did not remove the taxon from Sibynophiinae. Following Bogert (1940), Leviton & Munsterman (1956) erected the genus Parasibynophis to accommodate the Malagasy and Comoran species Sib. torquatus, Sib. rhodogaster, and Sib. mayottensis, distinguishing them from the Asian and New World taxa on the basis of 11 osteological and hemipenial characters. Like Bogert (1940), these authors considered the mandibular characters to be of greater phylogenetic importance than the hemipenial features, reinforcing the allocation of all three genera Scaphiodontophis, Sibynophis, and Parasibynophis into the subfamily Sibynophiinae. Later, Guib (1958) synonymized Parasibynophis with Liophidium, an arrangement followed by subsequent authors (e.g., Underwood, 1967; Williams & Wallach, 1989; Cadle, 1999).

Several more recent authors recognized either the subfamily Sibynophiinae or tribe Sibynophiini (e.g., Kuhn, 1967; Underwood, 1967; Smith et al., 1977; Ferrarezzi, 1994; Zaher, 1999). Further, Taylor & Smith (1943), Leviton & Munsterman (1956), Underwood (1967), Ferrarezzi (1994), and Zaher (1999) explicitly recognized either the Sibynophiinae or Sibynophiini as a natural assemblage of hingedteeth snakes that includes Scaphiodontophis and Sibynophis but excludes Liophidium. Underwood (1967: 91) stated the issue with clarity: this subfamily [Sibynophinae] as proposed by Dunn included the Madagascar species now put into Liophidium; the relationships of these latter snakes lie elsewhere but the remaining two genera Sibynophis and Scaphiodontophis are certainly related and systematically rather isolated. Ferrarezzi (1994: 90) provided a diagnosis for the tribe Sibynophiini that, according to the author, includes two putative synapomorphies: posterior process of the dentary free and elongate; maxillary teeth small, robust and flattened laterally. Although shared by Scaphiodontophis and Sibynophis, these two characters also are present in Liophidium, in which they have evolved homoplastically. Zaher (1999: 28) further documented that Sibynophis and Scaphiodontophis share an additional putative hemipenial synapomorphyviz., a sharply curved, U-shaped convolution of the sulcus spermaticus in the proximal region of the hemipenial body. More recently, Pyron et al. (2011) erected a new subfamily of colubroid snakes, the Scaphiodontophiinae, to accommodate the New World genus Scaphiodontophis. Their analysis also successfully tested the phylogenetic position of Liophidium, which appears as a member of their subfamily Pseudoxyrhophiinae, and not as the sister-group of Scaphiodontophis. However, monophyly of the traditional subfamily Sibynophiinae, including the genera Sibynophis and Scaphiodontophis (sensu Zaher, 1999), requires testing because Sibynophis has not been sampled in any of the recent molecular phylogenetic analyses. Here, we test this hypothesis by adding Sibynophis collaris to Pyron et al.s (2011) data matrix, and discuss the derived osteological and hemipenial characters shared by these genera. MAterIAl And Methods DNA from Sibynophis collaris was extracted from liver following the protocol of Hillis et al. (1996). Sequences for two nuclear protein-coding genes were amplified via polymerase chain reaction (PCR):

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oocyte maturation factor (c-mos) and recombinationactivating gene 1 (rag1). To amplify c-mos we used the primers described in Zaher et al. (2009); and for rag1 we used the primers Mart.FL1 (5 AGC TGC AGY CAR TAY CAY AAR ATG TA 3) and Amp. R1 (5 AAC TCA GCT GCA TTK CCA ATR TCA 3) as described by Chiari et al. (2004). PCRs were performed using standard protocols with the addition of 0.4% of Triton X-100 (Sigma-Aldrich, Saint Louis, MO, USA) and annealing temperature of 54C. PCRs were purified with shrimp alkaline phosphatase and exonuclease I (GE Healthcare, Piscataway, NJ). Sequences were processed using a BigDye Terminator cycle sequencing kit in an ABI 3700 sequencer (Applied Biosystems, Foster City, CA, USA). Both strands were sequenced and checked. The consensus of the two strands was constructed using Geneious version 5.4.6 (Drummond et al., 2011). The voucher of Sibynophis collaris used in this study was deposited at the Royal Ontario Museum (ROM 25618). Sequences of rag1 and c-mos were submitted to GenBank, receiving accession numbers JQ994296 and JQ994297, respectively. One sequence of Sibynophis chinensis for cytochrome b (cytb) was downloaded from GenBank (accession JN571580). We assumed monophyly of the genus Sibynophis and this allowed the creation of a combined terminal (c-mos and rag of S. collaris and cytb of S. chinensis). We included the sequences of Sibynophis in the matrix of Pyron et al. (2011), while preserving the

existing alignment, by using the command --add available in MAFFT version 6.864 (Katoh et al., 2002). We conducted a maximum likelihood analysis using RAxML 7.2.8 (Stamatakis, 2006). As performed by Pyron et al. (2011), the concatenated data were partitioned by codon position and the GTRGAMMA model was used for all partitions. The rapid bootstrap algorithm was employed, and 500 non-parametric bootstrap replicates were performed using the cluster hosted at the Laboratrio de Alto Desempenho Pontifcia Universidade Catlica do Rio Grande do Sul (LAD-PUCRS). This approach allowed 100 complete searches because it used the tree generated at every fifth bootstrap replicate as the starting tree for an independent LSR (Lazy Subtree Rearrangement) swapping. Nodal support was assessed through bootstrapping (BS). We compared the hemipenial, palato-maxillary, and dentary complexes of Sibynophis chinensis with those of Scaphiodontophis annulatus, Liophidium rhodogaster, and L. torquatus. Taylor & Smith (1943), Leviton & Munsterman (1956) and Zaher (1999) previously described these complexes. Cleared-and-stained skulls were prepared following the technique of Dingerkus & Uhler (1977) in which cartilage is stained with Alcian blue, bone with Alizarin red, and tissue is macerated with Trypsin. Skeletal nomenclature follows that of Cundall & Irish (2008). Methods for hemipenial preparation and terminology followed those of Zaher (1999) and Zaher & Prudente (2003).

FIgure 1: Summary tree showing the major clades of Caenophidia as recovered in the maximum likelihood analysis of Pyron et al.s (2011) data set with Sibynophis sequences added (full topology in Appendix S1). Taxon names in bold indicate high-level taxa (higher than family). Numbers near nodes indicate bootstrap values for unnamed clades. Numbers in parenthesis after a taxon name indicate bootstrap values for that clade.

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FIgure 2: Palatomaxillary arch. A: Dorsal view of Sibynophis chinensis AMNH 34534; b: Ventral view of Sibynophis chinensis AMNH 34534; c: Dorsal view of Scaphiodontophis annulatus KU 191073; d: Ventral view of Scaphiodontophis annulatus KU 191073; e: Dorsal view of Liophidium rhodogaster UMMZ 209427; F: Ventral view of Liophidium rhodogaster UMMZ 209427. Abbreviations: ept = ectopterygoid; mx = maxilla; pal = palatine; pt = pterygoid. Scale bar = 2 mm.

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Institutional codes are, as follow: AMnh, American Museum of Natural History; Ku, Museum of Natural History, University of Kansas; and uMMZ, University of Michigan, Museum of Zoology. The following specimens were examined: Sibynophis chinensis (skull: AMNH 34534; hemipenis: AMNH 34102); Scaphiodontophis annulatus (skull and hemipenis: KU 191073); Liophidium rhodogaster (skull: UMMZ 209427; hemipenis: UMMZ 209424); and L. torquatus (skull: UMMZ 209450). results Our tree-search procedure in RAxML produced a topology with a score of lnL = -376071.295841. A summary of the tree topology is given in Figure 1, and the full tree is provided as supplementary material (Appendix S1). Although we retrieved the same well-supported clades (BS > 70%) as did Pyron et al. (2011), the relationships at poorly supported nodes frequently differed (e.g., affinities between elapoid families sensu Zaher et al., 2009). Our analysis clustered Sibynophis with Scaphiodontophis in a robustly supported clade within Colubroidea (sensu Zaher et al., 2009), with a bootstrap value of 91 (Fig. 1; Appendix S1). In contrast, Liophidium maintained its elapoid affinities (Zaher, 1999; Nagy et al., 2003; Pyron et al., 2011), clustering with the other Malagasy snakes as the sister-group of a clade formed by Heteroliodon, Pseudoxyrhopus, and Liopholidophis (Nagy et al., 2003). This result corroborated the monophyly of the sibynophiines, as previously recognized by Underwood (1967), Ferrarezzi (1994), and Zaher (1999). Sibynophiines, calamariids, and colubrids (including Grayiinae and Colubrinae of Pyron et al., 2011) appeared rooted in an unresolved polytomy, forming a weakly supported clade (BS = 30; Fig. 1) that also was retrieved by Pyron et al. (2011) with a slightly higher bootstrap value (BS = 52). dIscussIon According to the phylogenetic affinities recovered in our molecular analysis (Fig. 1), Scaphiodontophis and Sibynophis share four putative morphological synapomorphies that are absent in Liophidium and all remaining pseudoxyrhophiines. These are, as follow: (1) distally broadened, plate-like maxillary process of the palatine with an anterior edge projecting from the level of the anterior tip of the palatine and covering completely the palatine process of the maxilla (Fig. 2);

FIgure 3: Hemipenis. A: asulcate view of Sibynophis chinensis AMNH 34102; b: sulcate view of Sibynophis chinensis AMNH 34102; c: asulcate view of Scaphiodontophis annulatus KU 191073; d: sulcate view of Scaphiodontophis annulatus KU 191073; e: asulcate view of Liophidium rhodogaster UMMZ 209424; F: sulcate view of Liophidium rhodogaster UMMZ 209424. Scale bar = 2 mm.

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(2) maxilla projects posteriorly to the maxillaryectopterygoid contact, forming a significantly long dentigerous process posterior to the ectopterygoid process of the maxilla (Fig. 2); (3) choanal process of the palatine absent (Fig. 2); and (4) sharply curved U-shaped convolution of the sulcus spermaticus in the proximal region of the hemipenial body (Fig. 3). Alternately, five morphological characters found in Scaphiodontophis and Sibynophis appear to have evolved homoplastically in Liophidium. These characters include: (1) numerous, closely set teeth (Figs. 2, 4); (2) compound bone anterior to the mandibular fossa with a long, tubular and dorsally curved shape (Fig. 4); (3) splenial and angular bones reduced (Fig. 4); (4) mandibular fossa reduced and restricted to the posterior one-fifth of the compound bone (Fig. 4); and (5) posterior dentigerous process of the dentary elongated and detached from the compound bone (Fig. 4). These homoplastic characters likely reflect the specialized durophagous diet of these snakes (Savitzky, 1981, 1983).

Cadle (1999), following Savitzkys (1981) lead, found hinged and peculiarly shaped teeth in Pseudoxyrhopus, Exallodontophis, Heteroliodon, and Pararhadinaea; all of these Malagasy genera are closely related to Liophidium and known to feed on durophagous prey. Cadle (1999) also pointed out that hinged teeth occur in some African and Asian snakes that feed on hard prey (e.g., Lycophidion, Mehelya, Chamaelycus, Tropidonophis). The apparently widespread geographical distribution of hinged teeth represents additional evidence that this peculiar tooth morphology has arisen independently several times. higher level taxonomic ranking of colubroides (sensu Zaher et al., 2009) Pyron et al. (2011) differ from Zaher et al. (2009) in preferring the traditional meaning of the superfamily Colubroidea, including the Xenodermatidae, Pareatidae, Viperidae, Homalopsidae, Elapidae,

FIgure 4: Mandible. A: Medial view of Sibynophis chinensis AMNH 34534; b: Medial view of Scaphiodontophis annulatus KU 191073; c: Medial view of Liophidium rhodogaster UMMZ 209427. Abbreviations: an = angular; cp = compound bone; d = dentary; sp = splenial. Scale bar = 2 mm.

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an expanded Lamprophiidae, and a highly speciose Colubridae. We acknowledge the fact that this scheme promotes taxonomic stability for the long-standing name Colubroidea. However, such traditional taxonomic hierarchy no longer accommodates new knowledge of phylogenetic affinities within the group appropriately (Vidal et al., 2007; Kelly et al., 2009; Zaher et al., 2009). As knowledge of the phylogenetic affinities of colubroideans improves, additional taxonomic changes that create a certain amount of instability will be required to accommodate the newly resolved relationships (Lawson et al., 2005; Vidal et al., 2007; Zaher et al., 2009). Such taxonomic adjustments, provided that they are stated explicitly (Zaher et al., 2009), are necessary to incorporate the diversity and newly discovered monophyletic groupings of the colubroidean radiation. As pointed out by Frost et al. (2006: 143) We expect that regulated nomenclature will increasingly be pushed toward the terminal taxa and that unregulated taxa will increasingly be rankless. The reason for this is that there really is a practical limit to the number of ranks that workers are willing to use So, our observation is that sociological pressures will push workers towards ever smaller families Regardless, we think that this process will correspond with enormous progress in phylogenetic understanding. Zaher et al.s (2009) new taxonomic scheme represents a step in that direction for the largest, most speciose group of snakes. In the present study, Scaphiodontophis and Sibynophis form a well-supported clade rooted in a polytomy along with families Colubridae and Calamariidae (Fig. 1). Therefore, we recognize Sibynophiidae Dunn, 1928 (ex Sibynophiinae) as a distinct family that includes the genera Scaphiodontophis Taylor & Smith, 1943 and Sibynophis Fitzinger, 1843 (type genus) within Zaher et al.s (2009) taxonomic scheme. Because Sibynophiidae Dunn, 1928, has priority over Scaphiodontophiinae Pyron et al., 2011, we synonymize the latter into the former. resuMo Os resultados apresentados correspondem primeira anlise molecular feita acerca das afinidades filogenticas do gnero Sibynophis, um colubrideo de origem asitica. Sibynophis aparece como sendo o grupo-irmo do gnero Neotropical Scaphiodontophis. Embora Liophidium esteja por vezes associado a estes dois gneros, a sua relao apenas distante. Os caracteres morfolgicos

compartilhados entre Liophidium, Sibynophis e Scaphiodontophis correspondem a homoplasias que refletem provavelmente os hbitos alimentares especializados semelhantes, presentes nos trs gneros em questo. A tradicional subfamlia Sibynophiinae elevada ao nvel de famlia, enquanto que Scaphiodontophiinae passa para sua sinonmia. Palavras-Chave: Sibynophiidae; Sibynophis; Scaphiodontophis; Filogenia. AcKnowledgMents The authors wish to thank Charles Myers, Darrel Frost and David Kizirian (AMNH), Ronald Nussbaum and Greg Schneider (UMMZ), William Duellman and Linda Trueb (KU) for their support and for allowing us to prepare and analyze specimens from the collections under their care. We are grateful to the staff of the Laboratrio de Alto Desempenho, Pontifcia Universidade Catlica do Rio Grande do Sul (LAD-PUCRS), who generously allowed access to the cluster under their care. We are also indebted to John Cadle, Linda Trueb, and Gustavo Scrocchi for their insightful review of a previous version of the work. Funding for this study was provided by the Fundao de Amparo Pesquisa do Estado de So Paulo (BIOTA/FAPESP; grants number 02/13602-4 and 11/50206-9) and Conselho Nacional de Desenvolvimento Cientfico e Tecnolgico (CNPq; grants number 565046/2010-1 and 303545/2010-0) to HZ. This study also benefitted from a Visiting Professorship for Senior International Scientists from the Chinese Academy of Sciences and a Natural Sciences and Engineering Research Council of Canada Discovery Grant (3148) to RWM, a Postdoctoral fellowship from CNPq (number 152069/2010-0) to GGM, and a PhD scholarship from FAPESP to FGG (number 07/52781-5). reFerences
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supportIng InForMAtIon Additional supporting Information may be found in the online version of this article: Appendix S1: Maximum likelihood phylogeny of Caenophidia based on the concatenated dataset used by Pyron et al. (2011) with sequences added for Sibynophis. Numbers near nodes are bootstrap values.

Appendix S1
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86 93

Tropidophis haetianus Anilius scytale Boa constrictor Cylindrophis ruffus Xenopeltis unicolor Acrochordus granulatus Achalinus rufescens Achalinus meiguensis Stoliczkaia borneensis Xenodermus javanicus Asthenodipsas vertebralis
98 39 32 31

99 100 47

Pareas nuchalis Aplopeltura boa Pareas macularius

49

99

100

99

64

100

96

74

96

29

Pareas hamptoni Pareas margaritophorus Proatheris superciliaris Eristicophis macmahoni 94 Pseudocerastes persicus 99 39 Pseudocerastes fieldi Macrovipera schweizeri 100 Macrovipera lebetina 100 94 Vipera xanthina 86 Vipera wagneri Vipera bornmuelleri 78 Vipera albizona 35 32 76 Vipera raddei Daboia russelii 71 Vipera palaestinae 72 Macrovipera mauritanica 100 Macrovipera deserti 82 Vipera ammodytes Vipera aspis 98 98 Vipera latastei Vipera kaznakovi 99 55 68 Vipera ursinii 76 Vipera dinniki 82 Vipera seoanei 88 Vipera nikolskii Vipera berus 92 82 Vipera barani Echis carinatus 100 Echis ocellatus 67 Echis pyramidum 52 Echis coloratus 67 Cerastes vipera 99 Cerastes cerastes 37 Causus resimus 100 Causus defilippii 85 Causus rhombeatus 19 Atheris chlorechis Atheris barbouri 99 87 Atheris ceratophora 40 Atheris hispida 93 Atheris squamigera 20 66 Atheris desaixi 31 Atheris nitschei Bitis arietans Bitis worthingtoni 99 Bitis gabonica 100 50 Bitis nasicornis Bitis peringueyi 84 100 Bitis caudalis 96 Bitis xeropaga 99 Bitis atropos 100 Bitis cornuta 100 Bitis rubida Azemiops feae Garthius chaseni Tropidolaemus wagleri 66 Deinagkistrodon acutus 18 Hypnale hypnale 100 98 Calloselasma rhodostoma Trimeresurus puniceus 98 Trimeresurus borneensis 98 Trimeresurus malabaricus 100 Trimeresurus trigonocephalus 100 90 Trimeresurus gramineus Cryptelytrops insularis 99 Cryptelytrops septentrionalis 100 Cryptelytrops albolabris 98 98 Cryptelytrops cantori 100 Cryptelytrops purpureomaculatus 100 95 Cryptelytrops erythrurus Himalayophis tibetanus Viridovipera medoensis 22 43 Cryptelytrops macrops 100 29 Cryptelytrops venustus 57 Viridovipera gumprechti 95 Viridovipera stejnegeri 83 14 Viridovipera vogeli Popeia popeiorum 21 Parias hageni 88 Parias malcolmi 99 Parias flavomaculatus 74 Parias sumatranus 63 Parias schultzei Trimeresurus gracilis 100 Ovophis okinavensis Gloydius halys 42 100 Gloydius shedaoensis 77 100 Gloydius strauchi 65 Gloydius blomhoffii 20 100 Gloydius ussuriensis Ovophis monticola 21 Triceratolepidophis sieversorum Zhaoermia mangshanensis 47 Protobothrops cornutus 83 88 Protobothrops jerdonii 99 Protobothrops tokarensis 100 Protobothrops flavoviridis 61 Protobothrops mucrosquamatus 100 Protobothrops elegans Ophryacus undulatus 95 Ophryacus melanurus 47 Lachesis muta 100 Lachesis stenophrys 14 Bothriechis schlegelii Bothriechis nigroviridis 89 Bothriechis lateralis 100 Bothriechis thalassinus 74 97 Bothriechis marchi 46 100 Bothriechis bicolor 41 Bothriechis rowleyi 61 64 Bothriechis aurifer Agkistrodon contortrix 100 Agkistrodon piscivorus 98 Agkistrodon bilineatus 100 Agkistrodon taylori 25 Crotalus ravus Crotalus pusillus 98 Sistrurus miliarius 96 25 Sistrurus catenatus Crotalus cerastes 24 Crotalus enyo 16 Crotalus horridus 13 Crotalus transversus 24 Crotalus tortugensis 100 Crotalus atrox 55 18 Crotalus durissus 93 Crotalus basiliscus 81 Crotalus totonacus 96 68 29 Crotalus molossus Crotalus willardi Crotalus mitchellii 21 46 Crotalus adamanteus 38 Crotalus tigris 61 Crotalus scutulatus 89 Crotalus viridis 96 Crotalus oreganus Atropoides occiduus 100 Atropoides nummifer 100 Atropoides olmec Atropoides picadoi 100 33 Cerrophidion godmani 84 Cerrophidion tzotzilorum 100 Cerrophidion petlalcalensis 55 Porthidium dunni 96 Porthidium ophryomegas 100 Porthidium yucatanicum Porthidium nasutum 46 100 97 Porthidium porrasi 100 Porthidium lansbergii Bothrocophias campbelli 59 Bothrocophias microphthalmus 100 Bothrocophias hyoprora Bothrops pictus 100 Bothrops ammodytoides Bothrops itapetiningae 94 97 Bothrops alternatus 96 74 Bothrops cotiara 100 Bothrops fonsecai Bothrops jararaca 100 90 Bothrops insularis 99 Bothrops alcatraz 100 Bothrops erythromelas 100 Bothrops neuwiedi 100 Bothrops diporus 96 Bothriopsis bilineata Bothriopsis pulchra 100 66 Bothriopsis chloromelas 93 Bothriopsis taeniata 89 Bothrops jararacussu 100 Bothrops brazili Bothrops punctata 100 Bothrops caribbaeus 63 99 Bothrops lanceolatus Bothrops asper 99 Bothrops colombiensis 49 93 Bothrops marajoensis 97 Bothrops moojeni 39 Bothrops atrox 64 Bothrops leucurus Enhydris matannensis 100 Enhydris plumbea Enhydris enhydris 51 99 Enhydris chinensis Enhydris punctata 41 Myron richardsonii 54 100 Enhydris polylepis Enhydris bocourti 20 75 Homalopsis buccata 54 Cerberus australis 100 Cerberus microlepis 100 25 Cerberus rynchops Erpeton tentaculatum Bitia hydroides 61 27 Cantoria violacea 76 Fordonia leucobalia 59 Gerarda prevostiana Oxyrhabdium leporinum Calliophis bivirgata Sinomicrurus japonicus 89 61 Sinomicrurus kelloggi 100 Sinomicrurus macclellandi 64 Micruroides euryxanthus Micrurus fulvius 100 28 Micrurus corallinus Micrurus mipartitus 99 15 Micrurus surinamensis 54 Micrurus hemprichii 41 Micrurus lemniscatus 84 Micrurus narduccii Micrurus decoratus 20 Micrurus pyrrhocryptus 100 49 Micrurus baliocoryphus Micrurus altirostris 92 19 Micrurus ibiboboca 44 Micrurus spixii 58 100 Micrurus frontalis 72 Micrurus brasiliensis Ophiophagus hannah 45 Hemibungarus calligaster 18 Aspidelaps scutatus Walterinnesia aegyptia 88 Hemachatus haemachatus 13 Naja annulata 73 Naja multifasciata 54 64 Naja nivea 100 Naja annulifera Naja nigricollis 24 96 Naja mossambica 96 Naja pallida 67 Naja nubiae 33 Naja kaouthia Naja naja 45 51 100 Naja atra 17 Naja mandalayensis 100 Naja siamensis Dendroaspis angusticeps 90 Dendroaspis polylepis Bungarus flaviceps 11 19 Bungarus bungaroides 19 Bungarus fasciatus Bungarus caeruleus 100 91 Bungarus sindanus 100 Bungarus niger 88 Bungarus multicinctus 11 98 Bungarus candidus Elapsoidea nigra 100 Elapsoidea sundevallii 100 Elapsoidea semiannulata Laticauda colubrina Toxicocalamus preussi 22 Micropechis ikaheka 2 Demansia vestigiata 100 Demansia papuensis 1 Simoselaps semifasciatus 73 98 Simoselaps anomalus 100 Simoselaps bertholdi Oxyuranus microlepidotus 4 100 Oxyuranus scutellatus 78 Pseudonaja modesta 96 57 Pseudonaja textilis 2 Simoselaps calonotus 53 Vermicella intermedia Aspidomorphus muelleri 3 11 Acanthophis praelongus 100 Acanthophis antarcticus 8 Pseudechis porphyriacus Pseudechis butleri 38 98 Pseudechis australis 100 Pseudechis papuanus 16 Pseudechis guttatus 100 77 Pseudechis colletti Cacophis squamulosus 50 Furina diadema 100 Furina ornata 18 Suta fasciata 91 Suta monachus 98 Suta suta 52 Denisonia devisi Elapognathus coronata 64 58 Rhinoplocephalus nigrescens 79 Rhinoplocephalus bicolor Hemiaspis signata 100 13 Hemiaspis damelii Echiopsis curta 44 Drysdalia mastersii 100 69 Drysdalia coronoides Austrelaps superbus 100 66 Austrelaps labialis 75 Echiopsis atriceps 48 Hoplocephalus bitorquatus 86 49 Notechis scutatus 100 Tropidechis carinatus Emydocephalus annulatus Aipysurus eydouxii 100 Aipysurus laevis 98 100 Aipysurus fuscus 94 Aipysurus apraefrontalis 100 94 Aipysurus duboisii Parahydrophis mertoni Hydrelaps darwiniensis 94 Hydrophis elegans 69 Astrotia stokesii Hydrophis czeblukovi 100 33 Disteira major Acalyptophis peronii 31 59 100 Hydrophis ornatus 23 Disteira kingii 18 Hydrophis brooki 23 33 Hydrophis macdowelli Lapemis curtus Pelamis platura 27 Hydrophis lapemoides 34 64 Hydrophis spiralis Hydrophis cyanocinctus 98 Hydrophis pacificus 95 96 Hydrophis semperi Buhoma depressiceps 69 Buhoma procterae Lycophidion nigromaculatum Lycophidion laterale 100 53 Lycophidion capense 68 Lycophidion ornatum 70 24 Lamprophis swazicus 93 Hormonotus modestus 76 Gonionotophis brussauxi Mehelya nyassae 100 47 Mehelya stenophthalmus 99 63 Mehelya capensis 100 Mehelya poensis Pseudoboodon lemniscatus Bothrolycus ater 81 Bothrophthalmus brunneus 81 100 Bothrophthalmus lineatus Lamprophis virgatus 86 100 Lamprophis fuliginosus Lamprophis lineatus 100 69 Lamprophis olivaceus 74 Lamprophis guttatus 29 Lamprophis fiskii 47 Lamprophis inornatus 84 Lycodonomorphus rufulus 98 46 Lycodonomorphus whytii 100 Lycodonomorphus laevissimus Prosymna ruspolii
100 94

Prosymna janii Prosymna visseri

23

88 99

95

92

61

49 99

7 24 100

100

15 58

14

99

100 27

27

51 84

81

34

Homoroselaps lacteus Atractaspis microlepidota Atractaspis boulengeri 84 Atractaspis bibronii 64 Atractaspis corpulenta 73 Atractaspis micropholis Macrelaps microlepidotus Amblyodipsas dimidiata 100 Xenocalamus transvaalensis Polemon notatus 100 Polemon collaris 100 Polemon acanthias Aparallactus werneri 100 Aparallactus guentheri 100 Aparallactus capensis Psammodynastes pulverulentus Pseudaspis cana Pythonodipsas carinata Rhamphiophis rubropunctatus 97 Malpolon monspessulanus 94 Malpolon moilensis Dipsina multimaculata Psammophylax acutus 87 45 Psammophylax rhombeatus 100 Psammophylax tritaeniatus 100 61 Psammophylax variabilis Mimophis mahfalensis 39 Hemirhagerrhis viperina 100 Hemirhagerrhis hildebrandtii 64 Hemirhagerrhis kelleri Psammophis crucifer 57 Psammophis condanarus 100 Psammophis lineolatus Psammophis trigrammus 99 Psammophis jallae 100 70 Psammophis leightoni 75 Psammophis notostictus 99 Psammophis angolensis Psammophis schokari 71 Psammophis punctulatus 71 59 Psammophis praeornatus 57 Psammophis biseriatus 100 Psammophis tanganicus Psammophis lineatus 64 Psammophis subtaeniatus 99 59 Psammophis sudanensis 96 Psammophis orientalis 92 Psammophis rukwae 73 Psammophis sibilans 57 Psammophis leopardinus 99 Psammophis mossambicus 100 Psammophis phillipsi Ditypophis vivax Amplorhinus multimaculatus Duberria variegata 100 Duberria lutrix Alluaudina bellyi Compsophis albiventris 96 Compsophis boulengeri 99 Compsophis laphystia 83 Compsophis infralineatus Liophidium rhodogaster 98 Liophidium vaillanti 95 Liophidium chabaudi 100 Liophidium torquatum Heteroliodon occipitalis 89 Pseudoxyrhopus ambreensis Liopholidophis dimorphus 99 Liopholidophis sexlineatus 100 Liopholidophis dolicocercus Dromicodryas bernieri 100 Dromicodryas quadrilineatus 49 Bibilava infrasignatus 100 Bibilava epistibes 78 Bibilava stumpffi
51

14

100 100

56

100 85 55 100 29 32 100

100

Bibilava lateralis Leioheterodon geayi Leioheterodon madagascariensis Leioheterodon modestus Micropisthodon ochraceus Langaha madagascariensis Ithycyphus miniatus 100 Ithycyphus oursi Madagascarophis colubrinus Madagascarophis meridionalis Stenophis betsileanus Stenophis pseudogranuliceps Stenophis citrinus 100 Lycodryas sanctijohannis Plagiopholis styani Pseudoxenodon karlschmidti

73

Bibilava martae

Thermophis baileyi Contia tenuis

40

56

43

74

98

28

30

56

84

Heterodon simus 100 Heterodon platirhinos Diadophis punctatus 42 Farancia abacura 90 Carphophis amoenus Tantalophis discolor Amastridium veliferum 61 Coniophanes fissidens 49 Rhadinaea flavilata 60 Rhadinaea fulvivittis 82 Imantodes inornatus Imantodes lentiferus 100 Imantodes gemmistratus 88 100 Imantodes cenchoa 79 66 Leptodeira nigrofasciata Leptodeira frenata 89 Leptodeira punctata 99 36 Leptodeira splendida 53 Leptodeira septentrionalis Leptodeira bakeri 99 98 82 Leptodeira annulata 93 Leptodeira maculata 100 Leptodeira rubricata Pseudoleptodeira latifasciata 73 Hypsiglena slevini Hypsiglena jani 99 63 Hypsiglena ochrorhyncha 100 Hypsiglena torquata 99 74 73 Hypsiglena chlorophaea Adelphicos quadrivirgatus 49 Hydromorphus concolor 100 Tretanorhinus nigroluteus 64 Cryophis hallbergi Atractus elaps 51 99 Atractus wagleri Geophis carinosus 61 Dipsas catesbyi 28 65 Dipsas pratti 63 Ninia atrata 38 Tropidodipsas sartorii 62 Sibon nebulatus Conophis vittatus Hydrodynastes gigas 32 Xenopholis scalaris Apostolepis flavotorquata 1 64 Phalotris nasutus 2 Tomodon dorsatus 64 42 Pseudoeryx plicatilis 91 Hydrops triangularis 86 Helicops angulatus Tropidodryas striaticeps 93 Tropidodryas serra 17 Philodryas baroni 17 Philodryas viridissima 24 24 Philodryas olfersii 4 Philodryas nattereri 3 Xenoxybelis boulengeri 27 Philodryas patagoniensis 61 Pseudablabes agassizii Siphlophis cervinus 1 Oxyrhopus guibei 100 96 Oxyrhopus petola 81 Phimophis iglesiasi 65 Drepanoides anomalus 77 Pseudoboa neuwiedii 93 Boiruna maculata Psomophis joberti Uromacer catesbyi 7 6 82 Uromacer oxyrhynchus 96 Uromacer frenatus 66 Liophis lineatus 35 Erythrolamprus aesculapii 97 Waglerophis merremi 96 Lystrophis semicinctus 92 Xenodon neuwiedii 51 Arrhyton taeniatum 93 Arrhyton supernum Arrhyton vittatum 93 Arrhyton landoi 52 32 Arrhyton dolichura 100 Arrhyton procerum 56 Arrhyton tanyplectum 32 Arrhyton exiguum 50 Alsophis antillensis 95 Alsophis rijgersmaei 94 Alsophis rufiventris 100 Alsophis antiguae 72 Alsophis portoricensis Hypsirhynchus ferox 93 Antillophis parvifrons 85 46 Arrhyton callilaemum 99 Arrhyton polylepis 100 Arrhyton funereum 19 Darlingtonia haetiana 70 Ialtris dorsalis 21 Antillophis andreae 89 Alsophis vudii 100 Alsophis cantherigerus Afronatrix anoscopus 99 Natriciteres olivacea Xenochrophis punctulatus 82 100 Xenochrophis flavipunctatus 94 Xenochrophis vittatus 32 Rhabdophis tigrinus 100 Rhabdophis nuchalis 99 Amphiesma sauteri Natrix natrix 94 Natrix tessellata 78 Natrix maura 48 Sinonatrix annularis 41 Storeria occipitomaculata 91 Storeria dekayi 77 Virginia striatula 38 Clonophis kirtlandii 86 55 Seminatrix pygaea 49 Regina rigida 100 Regina alleni Regina grahami 23 Nerodia floridana 100 Nerodia cyclopion 99 81 Tropidoclonion lineatum 31 Regina septemvittata Nerodia rhombifer 30 100 Nerodia taxispilota 91 Nerodia erythrogaster Nerodia fasciata 66 94 Nerodia harteri 80 100 Nerodia sipedon Thamnophis sirtalis 81 Thamnophis sauritus 100 Thamnophis proximus Thamnophis rufipunctatus Adelophis foxi 91 Thamnophis melanogaster 96 53 100 Thamnophis valida Thamnophis godmani 29 36 Thamnophis exsul 32 Thamnophis scaliger 96 82 Thamnophis mendax 100 Thamnophis sumichrasti Thamnophis chrysocephalus 100 Thamnophis fulvus Thamnophis cyrtopsis 80 Thamnophis eques 100 99 Thamnophis marcianus Thamnophis brachystoma 100 100 Thamnophis radix 100 Thamnophis butleri 59 Thamnophis hammondii Thamnophis ordinoides 36 Thamnophis elegans 64 Thamnophis atratus 92 Thamnophis gigas 94 78 Thamnophis couchii Sibynophis collaris/chinensis 91 Scaphiodontophis annulatus Pseudorabdion oxycephalum 94 Calamaria pavimentata Grayia tholloni 100 Grayia smithii 100 Grayia ornata Chrysopelea paradisi 91 Ahaetulla fronticincta 12 Dendrelaphis caudolineatus Ptyas mucosa 99 Ptyas korros Opheodrys aestivus 100 Opheodrys vernalis Chironius carinatus 24 2 13 Oxybelis aeneus 17 Leptophis ahaetulla 34 Drymobius rhombifer 100 Dendrophidion dendrophis 18 Coluber constrictor 99 Masticophis flagellum 6 Spilotes pullatus 34 Phyllorhynchus decurtatus 39 Trimorphodon biscutatus 41 Drymarchon corais 16 Drymoluber dichrous 100 Mastigodryas melanolomus 100 Mastigodryas boddaerti 7 Salvadora mexicana Chionactis occipitalis 13 86 Sonora semiannulata 30 Chilomeniscus stramineus 47 Tantilla relicta Stenorrhina freminvillei 8 97 Conopsis biserialis 49 98 Conopsis nasus 99 Pseudoficimia frontalis 81 Sympholis lippiens Oligodon cinereus Scaphiophis albopunctatus Gonyosoma oxycephalum 11 100 Gonyosoma jansenii 64 Rhadinophis prasina 100 Rhynchophis boulengeri 100 Rhadinophis frenatum 1 Lytorhynchus diadema Coluber zebrinus 75 Coluber dorri 79 Macroprotodon cucullatus 69 Hemorrhois hippocrepis 100 Hemorrhois algirus 100 Hemorrhois ravergieri 100 79 Hemorrhois nummifer 1 81 Spalerosophis diadema Platyceps karelini 87 42 Platyceps florulentus 100 Platyceps najadum 78 Platyceps collaris 79 36 Platyceps rhodorachis 37 Platyceps rogersi Hemerophis socotrae Dolichophis jugularis 100 43 Dolichophis caspius 100 Dolichophis schmidti 94 Hierophis viridiflavus 100 Hierophis gemonensis Hierophis spinalis 21 1 Pseudocyclophis persicus 18 27 Eirenis aurolineatus 99 Eirenis modestus Eirenis decemlineatus 57 Eirenis lineomaculatus 13 Eirenis coronelloides 73 28 Eirenis rothii 68 Eirenis thospitis 56 Eirenis medus Eirenis levantinus 18 Eirenis punctatolineatus 39 Eirenis barani 54 36 Eirenis collaris 99 Eirenis eiselti Coelognathus radiata 99 Coelognathus helena 71 Coelognathus erythrurus 100 Coelognathus flavolineatus 100 Coelognathus subradiatus Philothamnus heterodermus 98 Hapsidophrys smaragdina 51 Thrasops jacksonii 63 Dispholidus typus 1 100 Thelotornis capensis 5 Lycodon zawi 75 Dinodon rufozonatum 100 Dinodon semicarinatum 39 Crotaphopeltis tornieri 98 Dipsadoboa unicolor 68 Telescopus fallax 4 Boiga pulverulenta 26 33 Boiga dendrophila 43 Dasypeltis scabra 98 Dasypeltis atra Maculophis bella Oreocryptophis porphyraceus 74 Euprepiophis mandarinus 94 Euprepiophis conspicillata 41 Orthriophis hodgsoni 26 Orthriophis taeniurus 98 Orthriophis cantoris 20 53 Orthriophis moellendorffi Zamenis hohenackeri 62 Zamenis persica 91 Rhinechis scalaris 100 86 Zamenis situla 99 Zamenis lineata 100 Zamenis longissimus Elaphe quatuorlineata Elaphe climacophora 100 58 Elaphe bimaculata 99 60 Elaphe dione 13 Elaphe carinata 41 Elaphe schrenckii 68 Elaphe quadrivirgata 61 Coronella girondica 66 Elaphe rufodorsata 61 Coronella austriaca Senticolis triaspis Pantherophis spiloides 100 23 Pantherophis alleghaniensis 99 Pantherophis obsoletus 100 Pantherophis bairdi Pantherophis vulpinus 99 93 53 Pantherophis guttatus 100 Pantherophis slowinskii 100 49 Pantherophis emoryi Pituophis deppei Pituophis lineaticollis 100 Pituophis vertebralis 57 100 Pituophis melanoleucus 51 86 Pituophis ruthveni 100 Pituophis catenifer Rhinocheilus lecontei 24 Pseudelaphe flavirufa 62 Arizona elegans 21 Bogertophis rosaliae 80 Bogertophis subocularis Cemophora coccinea 26 Lampropeltis calligaster 74 Lampropeltis pyromelana 100 Lampropeltis zonata 45 Lampropeltis elapsoides 56 72 Lampropeltis mexicana 98 100 Lampropeltis ruthveni Lampropeltis triangulum Lampropeltis extenuata 4 93 Lampropeltis alterna Lampropeltis getula 88 99 Lampropeltis nigra 94 Lampropeltis holbrooki 71 Lampropeltis splendida 100 Lampropeltis californiae
0.2

44