Volume 52(12):141‑149, 2012

Phylogenetic relationships of the (Serpentes: Colubroidea)

1,6 Hussam Zaher 1,2 Felipe G. Grazziotin 1,2 Roberta Graboski 1 Ricardo G. Fuentes 1 Paola Sánchez-Martinez 1 Giovanna G. Montingelli 3,4 Ya-Ping Zhang 3,5 Robert W. Murphy

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 . 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 simi- larities 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 process that is completely detached from the com- pound bone and teeth are numerous and closely set The genera Liophidium, Sibynophis, and Scaphi- (Duméril et al., 1854; Boulenger, 1890, 1896). odontophis occur on three distinct landmasses— Duméril et al. (1854) were the first authors to Madagascar, Asia, and Central America, respectively. place the four that share these morphologi- Despite their isolation, these long have been cal characteristics in the subgenus Enicognathus of thought to be closely related to each other. In each ge- their genus Ablabes. Later, Boulenger (1890) substi- nus, the dentary bears a peculiar posterior dentigerous tuted Enicognathus, preoccupied, with Polyodontophis

1. Museu de Zoologia, Universidade de São Paulo. Caixa Postal 42.494, 04218‑970, São Paulo, SP, Brasil. 2. Programa de Pós-Graduação em Zoologia, Universidade Estadual Paulista, Rio Claro, SP, Brasil. 3. Laboratory for Conservation and Utilization of Bio-resources, 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 Queen’s Park, Toronto, Canada M5S 2C6. 6. E‑mail correspondence to: [email protected] 142 Zaher, H. et al.: Phylogenetic affinities of Sibynophis

that he recognized as a genus. He added four addi- Several more recent authors recognized either tional species from India and southeastern Asia to the subfamily Sibynophiinae or tribe Sibynophiini Polyodontophis, as well as P. comorensis (= Liophidium (e.g., Kuhn, 1967; Underwood, 1967; Smith et al., mayottensis) and P. sumichrasti from the Comoros Is- 1977; Ferrarezzi, 1994; Zaher, 1999). Further, Tay- lands and Central America, respectively. Boulenger lor & Smith (1943), Leviton & Munsterman (1956), (1896) further expanded Polyodontophis with three Underwood (1967), Ferrarezzi (1994), and Zaher additional species, and described the genus Liophid- (1999) explicitly recognized either the Sibynophiinae ium, to accommodate L. trilineatum from Madagas- or Sibynophiini as a natural assemblage of hinged- car. Polyodontophis was posteriorly synonymized with teeth snakes that includes Scaphiodontophis and Sib- Fitzinger’s (1843) Sibynophis when Stejneger (1910) ynophis but excludes Liophidium. noted the latter genus has priority over the former, an Underwood (1967: 91) stated the issue with arrangement followed by all subsequent authors (e.g., clarity: “this subfamily [Sibynophinae] as proposed by Dunn, 1928; Smith, 1943; Taylor & Smith, 1943). Dunn included the Madagascar species now put into Dunn (1928) partially formalized Duméril’s and Liophidium; the relationships of these latter snakes Boulenger’s perspectives by erecting the subfamily lie elsewhere but the remaining two genera Sibyno- Sibynophiinae to accommodate the Asian and Cen- phis and Scaphiodontophis are certainly related and tral American species of the genus Sibynophis, but he systematically rather isolated.” Ferrarezzi (1994: 90) did not include the Malagasy taxa. Although Dunn provided a diagnosis for the tribe Sibynophiini that, did not explicitly refer to the Malagasy species of Sib- according to the author, includes two putative syn- ynophis, he implicitly considered them to be unrelated apomorphies: “posterior process of the dentary free to the Asian and Central American species. Accord- and elongate; maxillary teeth small, robust and flat- ing to Dunn (1928), both Asian and Central Ameri- tened laterally.” Although shared by Scaphiodontophis can Sibynophis retain a single-lobed hemipenis with and Sibynophis, these two characters also are present a single sulcus spermaticus—a condition strikingly in Liophidium, in which they have evolved homoplas- distinct from the bilobed hemipenis with a forked tically. Zaher (1999: 28) further documented that sulcus that occurs in the Malagasy species of Sibyno- Sibynophis and Scaphiodontophis share an additional phis. Taken together, both dentitional and hemipenial putative hemipenial synapomorphy—viz., a sharply similarities between the Asiatic and New World spe- curved, U‑shaped convolution of the sulcus spermati- cies were so compelling that Dunn decided to con- cus in the proximal region of the hemipenial body. sider them congeneric (Dunn, 1928: 20). It was only More recently, Pyron et al. (2011) erected a after Taylor & Smith (1943) that the New World spe- new subfamily of colubroid snakes, the Scaphiodon- cies of Sibynophis were allocated in a distinct genus tophiinae, to accommodate the New World genus Scaphiodontophis. Scaphiodontophis. Their analysis also successfully test- After Dunn (1928), Bogert (1940) briefly dis- ed the phylogenetic position of Liophidium, which cussed the hemipenial differences between the Mala- appears as a member of their subfamily Pseudoxy- gasy Sibynophis torquatus and its Asiatic and Central rhophiinae, and not as the sister-group of Scaphiodon- American congeners, but he did not remove the tophis. However, monophyly of the traditional sub- taxon from Sibynophiinae. Following Bogert (1940), family Sibynophiinae, including the genera Sibynophis Leviton & Munsterman (1956) erected the genus and Scaphiodontophis (sensu Zaher, 1999), requires Parasibynophis to accommodate the Malagasy and testing because Sibynophis has not been sampled in Comoran species Sib. torquatus, Sib. rhodogaster, and any of the recent molecular phylogenetic analyses. Sib. mayottensis, distinguishing them from the Asian Here, we test this hypothesis by adding Sibynophis col- and New World taxa on the basis of 11 osteological laris to Pyron et al.’s (2011) data matrix, and discuss and hemipenial characters. Like Bogert (1940), these the derived osteological and hemipenial characters authors considered the mandibular characters to be of shared by these genera. greater phylogenetic importance than the hemipenial features, reinforcing the allocation of all three genera Scaphiodontophis, Sibynophis, and Parasibynophis into Material and Methods the subfamily Sibynophiinae. Later, Guibé (1958) synonymized Parasibynophis with Liophidium, an ar- DNA from was extracted from rangement followed by subsequent authors (e.g., Un- liver following the protocol of Hillis et al. (1996). Se- derwood, 1967; Williams & Wallach, 1989; Cadle, quences for two nuclear protein-coding genes were 1999). amplified via polymerase chain reaction (PCR): Papéis Avulsos de Zoologia, 52(12), 2012 143

oocyte maturation factor (c‑mos) and recombination- existing alignment, by using the command “‑‑add” activating gene 1 (rag1). To amplify c‑mos we used available in MAFFT version 6.864 (Katoh et al., 2002). the primers described in Zaher et al. (2009); and for We conducted a maximum likelihood analysis using rag1 we used the primers Mart.FL1 (5’ AGC TGC RAxML 7.2.8 (Stamatakis, 2006). As performed by Py- AGY CAR TAY CAY AAR ATG TA 3’) and Amp. ron et al. (2011), the concatenated data were partitioned R1 (5’ AAC TCA GCT GCA TTK CCA ATR TCA by codon position and the GTRGAMMA model was 3’) as described by Chiari et al. (2004). PCRs were used for all partitions. The rapid bootstrap algorithm performed using standard protocols with the addition was employed, and 500 non-parametric bootstrap rep- of 0.4% of Triton X‑100 (Sigma-Aldrich, Saint Louis, licates were performed using the cluster hosted at the MO, USA) and annealing temperature of 54°C. Laboratório de Alto Desempenho – Pontifícia Univer- PCRs were purified with shrimp alkaline phos- sidade Católica do Rio Grande do Sul (LAD‑PUCRS). phatase and exonuclease I (GE Healthcare, Piscat- This approach allowed 100 complete searches because away, NJ). Sequences were processed using a BigDye it used the tree generated at every fifth bootstrap repli- Terminator cycle sequencing kit in an ABI 3700 se- cate as the starting tree for an independent LSR (Lazy quencer (Applied Biosystems, Foster City, CA, USA). Subtree Rearrangement) swapping. Nodal support was Both strands were sequenced and checked. The con- assessed through bootstrapping (BS). sensus of the two strands was constructed using Ge- We compared the hemipenial, palato-maxillary, neious version 5.4.6 (Drummond et al., 2011). and dentary complexes of Sibynophis chinensis with The voucher of Sibynophis collaris used in this those of Scaphiodontophis annulatus, Liophidium rho- study was deposited at the Royal Ontario Museum dogaster, and L. torquatus. Taylor & Smith (1943), (ROM 25618). Sequences of rag1 and c‑mos were Leviton & Munsterman (1956) and Zaher (1999) submitted to GenBank, receiving accession numbers previously described these complexes. JQ994296 and JQ994297, respectively. One sequence Cleared-and-stained skulls were prepared fol- of Sibynophis chinensis for cytochrome b (cytb) was lowing the technique of Dingerkus & Uhler (1977) downloaded from GenBank (accession JN571580). in which cartilage is stained with Alcian blue, bone We assumed monophyly of the genus Sibynophis and with Alizarin red, and tissue is macerated with Tryp- this allowed the creation of a combined terminal sin. Skeletal nomenclature follows that of Cundall & (c‑mos and rag of S. collaris and cytb of S. chinensis). Irish (2008). Methods for hemipenial preparation and We included the sequences of Sibynophis in the terminology followed those of Zaher (1999) and Za- matrix of Pyron et al. (2011), while preserving the her & 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. 144 Zaher, H. et al.: Phylogenetic affinities of Sibynophis

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 = ectopter- ygoid; mx = maxilla; pal = palatine; pt = pterygoid. Scale bar = 2 mm. Papéis Avulsos de Zoologia, 52(12), 2012 145

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 fol- lowing 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. tor- quatus (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 mate- rial (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 Scaphi- odontophis in a robustly supported clade within Colubroidea (sensu Zaher et al., 2009), with a boot- strap value of 91 (Fig. 1; Appendix S1). In contrast, Liophidium maintained its elapoid affinities (Zaher, 1999; Nagy et al., 2003; Pyron et al., 2011), cluster- ing with the other Malagasy snakes as the sister-group of a clade formed by Heteroliodon, Pseudoxyrhopus, and Liopholidophis (Nagy et al., 2003). This result cor- roborated the monophyly of the sibynophiines, as pre- viously 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 recov- ered in our molecular analysis (Fig. 1), Scaphiodonto- phis and Sibynophis share four putative morphological synapomorphies that are absent in Liophidium and all remaining pseudoxyrhophiines. These are, as follow: Figure 3: Hemipenis. A: asulcate view of Sibynophis chinensis (1) distally broadened, plate-like maxillary process of AMNH 34102; B: sulcate view of Sibynophis chinensis AMNH the palatine with an anterior edge projecting from the 34102; C: asulcate view of Scaphiodontophis annulatus KU 191073; D: sulcate view of Scaphiodontophis annulatus KU 191073; E: asul- level of the anterior tip of the palatine and covering cate view of Liophidium rhodogaster UMMZ 209424; F: sulcate completely the palatine process of the maxilla (Fig. 2); view of Liophidium rhodogaster UMMZ 209424. Scale bar = 2 mm. 146 Zaher, H. et al.: Phylogenetic affinities of Sibynophis

(2) maxilla projects posteriorly to the maxillary- Cadle (1999), following Savitzky’s (1981) lead, ectopterygoid contact, forming a significantly long found hinged and peculiarly shaped teeth in Pseudoxy- “dentigerous process” posterior to the ectopterygoid rhopus, Exallodontophis, Heteroliodon, and Pararhadi- process of the maxilla (Fig. 2); (3) choanal process of naea; all of these Malagasy genera are closely related to the palatine absent (Fig. 2); and (4) sharply curved Liophidium and known to feed on durophagous prey. U‑shaped convolution of the sulcus spermaticus in Cadle (1999) also pointed out that hinged teeth occur the proximal region of the hemipenial body (Fig. 3). in some African and Asian snakes that feed on hard Alternately, five morphological characters prey (e.g., Lycophidion, Mehelya, Chamaelycus, Tropi- found in Scaphiodontophis and Sibynophis appear to donophis). The apparently widespread geographical have evolved homoplastically in Liophidium. These distribution of hinged teeth represents additional evi- characters include: (1) numerous, closely set teeth dence that this peculiar tooth morphology has arisen (Figs. 2, 4); (2) compound bone anterior to the man- independently several times. dibular 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 Higher level taxonomic ranking of to the posterior one-fifth of the compound bone Colubroides (sensu Zaher et al., 2009) (Fig. 4); and (5) posterior dentigerous process of the dentary elongated and detached from the compound Pyron et al. (2011) differ from Zaher et al. bone (Fig. 4). These homoplastic characters likely re- (2009) in preferring the traditional meaning of the flect the specialized durophagous diet of these snakes superfamily Colubroidea, including the Xenoderma- (Savitzky, 1981, 1983). tidae, 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. Papéis Avulsos de Zoologia, 52(12), 2012 147

an expanded Lamprophiidae, and a highly speciose compartilhados entre Liophidium, Sibynophis e Sca- . We acknowledge the fact that this scheme phiodontophis correspondem a homoplasias que refle- promotes taxonomic stability for the long-stand- tem provavelmente os hábitos alimentares especializados ing name Colubroidea. However, such traditional semelhantes, presentes nos três gêneros em questão. A tra- taxonomic hierarchy no longer accommodates new dicional subfamília Sibynophiinae é elevada ao nível de knowledge of phylogenetic affinities within the group família, enquanto que Scaphiodontophiinae passa para appropriately (Vidal et al., 2007; Kelly et al., 2009; sua sinonímia. Zaher et al., 2009). As knowledge of the phylogenetic affinities of Palavras-Chave: Sibynophiidae; Sibynophis; Scaphi- colubroideans improves, additional taxonomic chang- odontophis; Filogenia. es that create a certain amount of instability will be required to accommodate the newly resolved relation- ships (Lawson et al., 2005; Vidal et al., 2007; Zaher Acknowledgments et al., 2009). Such taxonomic adjustments, provided that they are stated explicitly (Zaher et al., 2009), are The authors wish to thank Charles Myers, Darrel necessary to incorporate the diversity and newly dis- Frost and David Kizirian (AMNH), Ronald Nussbaum covered monophyletic groupings of the colubroidean and Greg Schneider (UMMZ), William Duellman and radiation. Linda Trueb (KU) for their support and for allowing us As pointed out by Frost et al. (2006: 143) “We to prepare and analyze specimens from the collections expect that regulated nomenclature will increasingly under their care. We are grateful to the staff of the Lab- be pushed toward the terminal taxa and that unregu- oratório de Alto Desempenho, Pontifícia Universidade lated taxa will increasingly be rankless. The reason for Católica do Rio Grande do Sul (LAD‑PUCRS), who this is that there really is a practical limit to the num- generously allowed access to the cluster under their ber of ranks that workers are willing to use … So, care. We are also indebted to John Cadle, Linda Trueb, our observation is that sociological pressures will push and Gustavo Scrocchi for their insightful review of a workers towards ever smaller families … Regardless, previous version of the work. Funding for this study we think that this process will correspond with enor- was provided by the Fundação de Amparo à Pesquisa do mous progress in phylogenetic understanding.” Za- Estado de São Paulo (BIOTA/FAPESP; grants number her et al.’s (2009) new taxonomic scheme represents 02/13602‑4 and 11/50206‑9) and Conselho Nacional a step in that direction for the largest, most speciose de Desenvolvimento Científico e Tecnológico (CNPq; group of snakes. grants number 565046/2010‑1 and 303545/2010‑0) In the present study, Scaphiodontophis and Sib- to HZ. This study also benefitted from a Visiting Pro- ynophis form a well-supported clade rooted in a poly- fessorship for Senior International Scientists from the tomy along with families Colubridae and Calamari- Chinese Academy of Sciences and a Natural Sciences idae (Fig. 1). Therefore, we recognize Sibynophiidae and Engineering Research Council of Canada Discov- Dunn, 1928 (ex Sibynophiinae) as a distinct family ery Grant (3148) to RWM, a Postdoctoral fellowship that includes the genera Scaphiodontophis Taylor & from CNPq (number 152069/2010‑0) to GGM, and Smith, 1943 and Sibynophis Fitzinger, 1843 (type ge- a PhD scholarship from FAPESP to FGG (number nus) within Zaher et al.’s (2009) taxonomic scheme. 07/52781‑5). Because Sibynophiidae Dunn, 1928, has priority over Scaphiodontophiinae Pyron et al., 2011, we synony- mize the latter into the former. 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

Tropidophis haetianus 99 Anilius scytale Boa constrictor 86 Cylindrophis ruffus 93 Xenopeltis unicolor Acrochordus granulatus Achalinus rufescens 99 Achalinus meiguensis 100 Stoliczkaia borneensis 47 Xenodermus javanicus Asthenodipsas vertebralis 98 Pareas nuchalis 39 Aplopeltura boa 32 Pareas macularius 31 Pareas hamptoni 49 Pareas margaritophorus Proatheris superciliaris Eristicophis macmahoni 99 94 Pseudocerastes persicus 99 39 Pseudocerastes fieldi Macrovipera schweizeri 100 Macrovipera lebetina 94 100 Vipera xanthina 86 Vipera wagneri

78 Vipera bornmuelleri 35 Vipera albizona 32 76 Vipera raddei Daboia russelii 71 Vipera palaestinae 72 Macrovipera mauritanica 100 82 Macrovipera deserti Vipera ammodytes Vipera aspis 100 98 98 Vipera latastei Vipera kaznakovi 99 55 68 Vipera ursinii 76 82 Vipera dinniki Vipera seoanei 88 Vipera nikolskii 92 Vipera berus 82 Vipera barani Echis carinatus 100 Echis ocellatus 67 Echis pyramidum 52 67 Echis coloratus Cerastes vipera 99 Cerastes cerastes 37 Causus resimus 100 Causus defilippii 85 Causus rhombeatus 19 Atheris chlorechis Atheris barbouri 99 87 Atheris ceratophora 99 40 Atheris hispida 93 Atheris squamigera 20 66 Atheris desaixi 31 Atheris nitschei Bitis arietans

99 Bitis worthingtoni Bitis gabonica 64 50 100 Bitis nasicornis

84 Bitis peringueyi 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 99 100 Cryptelytrops septentrionalis

98 Cryptelytrops albolabris 98 Cryptelytrops cantori 100 Cryptelytrops purpureomaculatus 100 95 Cryptelytrops erythrurus Himalayophis tibetanus

22 Viridovipera medoensis 43 Cryptelytrops macrops 100 29 57 Cryptelytrops venustus Viridovipera gumprechti 95 Viridovipera stejnegeri 14 83 Viridovipera vogeli Popeia popeiorum 21 Parias hageni 88 Parias malcolmi 99 Parias flavomaculatus 74 Parias sumatranus 63 Parias schultzei Trimeresurus gracilis 100 Ovophis okinavensis 42 Gloydius halys 100 Gloydius shedaoensis 77 100 Gloydius strauchi 65 20 Gloydius blomhoffii 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 100 100 Protobothrops elegans Ophryacus undulatus 95 Ophryacus melanurus 47 Lachesis muta 100 14 Lachesis stenophrys Bothriechis schlegelii 89 Bothriechis nigroviridis Bothriechis lateralis 100 Bothriechis thalassinus 74 97 Bothriechis marchi 46 100 41 Bothriechis bicolor 61 Bothriechis rowleyi 64 Bothriechis aurifer Agkistrodon contortrix 100 Agkistrodon piscivorus 98 Agkistrodon bilineatus 100 25 Agkistrodon taylori 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 96 Crotalus totonacus 29 68 Crotalus molossus Crotalus willardi Crotalus mitchellii 21 46 Crotalus adamanteus 38 61 Crotalus tigris 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 55 Cerrophidion petlalcalensis Porthidium dunni 96 Porthidium ophryomegas 100 Porthidium yucatanicum

46 100 Porthidium nasutum 97 Porthidium porrasi 100 Porthidium lansbergii Bothrocophias campbelli 59 Bothrocophias microphthalmus 100 Bothrocophias hyoprora Bothrops pictus 100 Bothrops ammodytoides

94 Bothrops itapetiningae 97 Bothrops alternatus 96 74 Bothrops cotiara 100 Bothrops fonsecai Bothrops jararaca 100 90 Bothrops insularis 99 100 Bothrops alcatraz Bothrops erythromelas 100 Bothrops neuwiedi 100 Bothrops diporus 96 Bothriopsis bilineata

100 Bothriopsis pulchra 66 Bothriopsis chloromelas 93 Bothriopsis taeniata 89 Bothrops jararacussu 100 Bothrops brazili

100 Bothrops punctata Bothrops caribbaeus 63 99 Bothrops lanceolatus

99 Bothrops asper Bothrops colombiensis 93 49 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 54 Myron richardsonii 100 Enhydris polylepis Enhydris bocourti 20 75 Homalopsis buccata 54 Cerberus australis 100 Cerberus microlepis 100 25 Cerberus rynchops Erpeton tentaculatum

61 Bitia hydroides 27 Cantoria violacea 76 Fordonia leucobalia 59 Gerarda prevostiana Oxyrhabdium leporinum Calliophis bivirgata Sinomicrurus japonicus 96 61 89 Sinomicrurus kelloggi 100 Sinomicrurus macclellandi 64 Micruroides euryxanthus Micrurus fulvius 100 28 Micrurus corallinus Micrurus mipartitus 99 15 Micrurus surinamensis 54 Micrurus hemprichii 41 84 Micrurus lemniscatus Micrurus narduccii Micrurus decoratus 74 20 Micrurus pyrrhocryptus 49 100 Micrurus baliocoryphus 92 Micrurus altirostris 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

45 Naja naja 100 51 Naja atra 17 Naja mandalayensis 100 Naja siamensis Dendroaspis angusticeps 90 Dendroaspis polylepis

11 Bungarus flaviceps 96 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 1 Demansia papuensis Simoselaps semifasciatus 98 73 Simoselaps anomalus 100 Simoselaps bertholdi

4 Oxyuranus microlepidotus 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 16 100 Pseudechis guttatus 77 Pseudechis colletti Cacophis squamulosus 50 Furina diadema 100 Furina ornata 18 Suta fasciata 91 Suta monachus 98 52 Suta suta Denisonia devisi

29 64 Elapognathus coronata 58 Rhinoplocephalus nigrescens 79 Rhinoplocephalus bicolor Hemiaspis signata 100 13 Hemiaspis damelii Echiopsis curta 44 Drysdalia mastersii 100 69 Drysdalia coronoides Austrelaps superbus 66 100 Austrelaps labialis 75 Echiopsis atriceps 48 Hoplocephalus bitorquatus 49 86 Notechis scutatus 100 Tropidechis carinatus Emydocephalus annulatus

100 Aipysurus eydouxii

98 Aipysurus laevis 100 Aipysurus fuscus 94 100 Aipysurus apraefrontalis 94 Aipysurus duboisii Parahydrophis mertoni Hydrelaps darwiniensis 94 Hydrophis elegans 69 Astrotia stokesii Hydrophis czeblukovi 100 33 Disteira major 31 Acalyptophis peronii 59 100 Hydrophis ornatus 23 Disteira kingii 18 Hydrophis brooki 23 33 Hydrophis macdowelli Lapemis curtus

27 Pelamis platura

34 Hydrophis lapemoides 64 Hydrophis spiralis

98 Hydrophis cyanocinctus 95 Hydrophis pacificus 96 Hydrophis semperi Buhoma depressiceps 69 Buhoma procterae Lycophidion nigromaculatum

100 Lycophidion laterale 53 Lycophidion capense 68 Lycophidion ornatum 24 70 Lamprophis swazicus 93 Hormonotus modestus 76 Gonionotophis brussauxi

100 Mehelya nyassae 47 99 Mehelya stenophthalmus 63 Mehelya capensis 100 Mehelya poensis Pseudoboodon lemniscatus Bothrolycus ater 81 81 Bothrophthalmus brunneus 100 Bothrophthalmus lineatus Lamprophis virgatus 86 100 Lamprophis fuliginosus 100 Lamprophis lineatus 69 74 Lamprophis olivaceus Lamprophis guttatus 29 Lamprophis fiskii 47 Lamprophis inornatus 84 Lycodonomorphus rufulus 46 98 Lycodonomorphus whytii 100 Lycodonomorphus laevissimus Prosymna ruspolii 100 Prosymna janii 94 Prosymna visseri Homoroselaps lacteus 88 Atractaspis microlepidota 23 99 Atractaspis boulengeri 84 Atractaspis bibronii 64 Atractaspis corpulenta 73 95 Atractaspis micropholis Macrelaps microlepidotus 92 Amblyodipsas dimidiata 100 Xenocalamus transvaalensis 61 Polemon notatus 100 Polemon collaris 100 49 Polemon acanthias

99 Aparallactus werneri 100 Aparallactus guentheri 100 Aparallactus capensis 7 Psammodynastes pulverulentus 24 Pseudaspis cana 100 Pythonodipsas carinata Rhamphiophis rubropunctatus 97 Malpolon monspessulanus 94 Malpolon moilensis Dipsina multimaculata Psammophylax acutus 45 87 Psammophylax rhombeatus 100 100 Psammophylax tritaeniatus 100 61 Psammophylax variabilis Mimophis mahfalensis 39 Hemirhagerrhis viperina 15 100 58 Hemirhagerrhis hildebrandtii 64 Hemirhagerrhis kelleri Psammophis crucifer 57 Psammophis condanarus 100 Psammophis lineolatus Psammophis trigrammus 99 100 Psammophis jallae 70 Psammophis leightoni 75 Psammophis notostictus 99 Psammophis angolensis Psammophis schokari 71 Psammophis punctulatus 14 71 59 Psammophis praeornatus 57 Psammophis biseriatus 100 Psammophis tanganicus Psammophis lineatus 64 Psammophis subtaeniatus 99 59 Psammophis sudanensis 96 92 Psammophis orientalis Psammophis rukwae 73 Psammophis sibilans 57 Psammophis leopardinus 99 Psammophis mossambicus 100 Psammophis phillipsi Ditypophis vivax Amplorhinus multimaculatus 99 Duberria variegata 100 Duberria lutrix 100 Alluaudina bellyi

27 Compsophis albiventris 96 Compsophis boulengeri 99 27 Compsophis laphystia 83 Compsophis infralineatus Liophidium rhodogaster 98 Liophidium vaillanti 95 Liophidium chabaudi 51 100 84 Liophidium torquatum Heteroliodon occipitalis 89 Pseudoxyrhopus ambreensis 81 Liopholidophis dimorphus 99 Liopholidophis sexlineatus 100 Liopholidophis dolicocercus

34 Dromicodryas bernieri 100 Dromicodryas quadrilineatus 49 Bibilava infrasignatus 100 Bibilava epistibes 78 Bibilava stumpffi 51 Bibilava martae 73 14 Bibilava lateralis Leioheterodon geayi 100 Leioheterodon madagascariensis 100 Leioheterodon modestus Micropisthodon ochraceus 56 100 Langaha madagascariensis 85 Ithycyphus miniatus 100 55 Ithycyphus oursi Madagascarophis colubrinus 100 Madagascarophis meridionalis 29 Stenophis betsileanus 32 Stenophis pseudogranuliceps 100 Stenophis citrinus 100 Lycodryas sanctijohannis Plagiopholis styani 100 Pseudoxenodon karlschmidti Thermophis baileyi Contia tenuis 44 Heterodon simus 100 Heterodon platirhinos 56 40 Diadophis punctatus 42 Farancia abacura 90 Carphophis amoenus Tantalophis discolor Amastridium veliferum 43 61 Coniophanes fissidens 49 Rhadinaea flavilata 60 Rhadinaea fulvivittis 82 Imantodes inornatus Imantodes lentiferus 100 88 Imantodes gemmistratus 100 Imantodes cenchoa 79 66 Leptodeira nigrofasciata 74 89 Leptodeira frenata Leptodeira punctata 99 36 Leptodeira splendida 53 Leptodeira septentrionalis 99 Leptodeira bakeri 98 82 Leptodeira annulata 93 Leptodeira maculata 100 Leptodeira rubricata Pseudoleptodeira latifasciata 73 Hypsiglena slevini

99 Hypsiglena jani 63 Hypsiglena ochrorhyncha 100 Hypsiglena torquata 99 73 74 Hypsiglena chlorophaea Adelphicos quadrivirgatus 49 Hydromorphus concolor 100 Tretanorhinus nigroluteus 64 Cryophis hallbergi Atractus elaps 51 99 Atractus wagleri

61 Geophis carinosus Dipsas catesbyi 28 65 Dipsas pratti 63 Ninia atrata 38 Tropidodipsas sartorii 62 Sibon nebulatus Conophis vittatus Hydrodynastes gigas 32 Xenopholis scalaris

1 Apostolepis flavotorquata 64 Phalotris nasutus 2 Tomodon dorsatus 64 42 Pseudoeryx plicatilis 91 Hydrops triangularis 86 Helicops angulatus Tropidodryas striaticeps 93 Tropidodryas serra 17 17 Philodryas baroni 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

98 Uromacer catesbyi 7 6 82 Uromacer oxyrhynchus 96 66 Uromacer frenatus Liophis lineatus 35 Erythrolamprus aesculapii 97 Waglerophis merremi 96 Lystrophis semicinctus 92 Xenodon neuwiedii 51 Arrhyton taeniatum 93 Arrhyton supernum

93 Arrhyton vittatum

52 Arrhyton landoi 32 Arrhyton dolichura 100 Arrhyton procerum 56 32 Arrhyton tanyplectum Arrhyton exiguum 50 Alsophis antillensis 95 Alsophis rijgersmaei 94 Alsophis rufiventris 100 72 Alsophis antiguae Alsophis portoricensis Hypsirhynchus ferox 93 Antillophis parvifrons 85 46 Arrhyton callilaemum 99 Arrhyton polylepis 100 19 Arrhyton funereum Darlingtonia haetiana 70 Ialtris dorsalis 21 Antillophis andreae 89 Alsophis vudii 100 Alsophis cantherigerus Afronatrix anoscopus 99 Natriciteres olivacea 82 Xenochrophis punctulatus 100 Xenochrophis flavipunctatus 94 Xenochrophis vittatus 32 Rhabdophis tigrinus 100 Rhabdophis nuchalis 99 Amphiesma sauteri Natrix natrix 94 Natrix tessellata 78 Natrix maura 48 41 Sinonatrix annularis 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

30 Nerodia rhombifer 100 Nerodia taxispilota 91 Nerodia erythrogaster

66 Nerodia fasciata 94 Nerodia harteri 80 100 Nerodia sipedon Thamnophis sirtalis 81 Thamnophis sauritus 100 Thamnophis proximus Thamnophis rufipunctatus

91 Adelophis foxi 28 Thamnophis melanogaster 96 53 100 Thamnophis valida Thamnophis godmani 29 36 Thamnophis exsul 32 96 Thamnophis scaliger 82 Thamnophis mendax 100 Thamnophis sumichrasti Thamnophis chrysocephalus 100 Thamnophis fulvus

80 Thamnophis cyrtopsis Thamnophis eques 100 99 Thamnophis marcianus Thamnophis brachystoma 100 100 Thamnophis radix 100 Thamnophis butleri 59 Thamnophis hammondii

36 Thamnophis ordinoides

64 Thamnophis elegans

92 Thamnophis atratus 94 Thamnophis gigas 78 Thamnophis couchii Sibynophis collaris/chinensis 91 Scaphiodontophis annulatus 4 Pseudorabdion oxycephalum 94 Calamaria pavimentata Grayia tholloni 100 Grayia smithii 100 Grayia ornata

30 Chrysopelea paradisi 91 Ahaetulla fronticincta 12 Dendrelaphis caudolineatus Ptyas mucosa 99 Ptyas korros Opheodrys aestivus 100 56 Opheodrys vernalis 24 Chironius carinatus 2 13 Oxybelis aeneus 17 Leptophis ahaetulla 34 Drymobius rhombifer 100 Dendrophidion dendrophis 18 Coluber constrictor 99 Masticophis flagellum 6 84 Spilotes pullatus 34 Phyllorhynchus decurtatus 39 Trimorphodon biscutatus 41 Drymarchon corais 16 Drymoluber dichrous 100 Mastigodryas melanolomus 100 7 Mastigodryas boddaerti Salvadora mexicana Chionactis occipitalis 13 86 Sonora semiannulata 30 Chilomeniscus stramineus 47 Tantilla relicta

8 Stenorrhina freminvillei 97 49 Conopsis biserialis 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 79 Platyceps collaris 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 27 18 Eirenis aurolineatus 99 Eirenis modestus

57 Eirenis decemlineatus Eirenis lineomaculatus 13 Eirenis coronelloides 73 28 Eirenis rothii 68 Eirenis thospitis 56 Eirenis medus

18 Eirenis levantinus Eirenis punctatolineatus 39 54 Eirenis barani 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 26 Boiga pulverulenta 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 58 100 Elaphe bimaculata 60 99 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

99 Pantherophis vulpinus 93 53 Pantherophis guttatus 100 Pantherophis slowinskii 100 49 Pantherophis emoryi Pituophis deppei

100 Pituophis lineaticollis

57 Pituophis vertebralis 100 51 Pituophis melanoleucus 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 56 Lampropeltis elapsoides 72 Lampropeltis mexicana 98 100 Lampropeltis ruthveni Lampropeltis triangulum Lampropeltis extenuata 4 93 Lampropeltis alterna 88 Lampropeltis getula 99 Lampropeltis nigra 94 Lampropeltis holbrooki 71 Lampropeltis splendida 100 Lampropeltis californiae

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