Snakes (Serpentes)

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Snakes (Serpentes) Snakes (Serpentes) Nicolas Vidala,b,*, Jean-Claude Ragec, Arnaud Coulouxd, snakes such as boas, pythons, and caenophidians and S. Blair Hedgesb (advanced snakes) (2, but see 4). Macrostomatans are aUMR 7138, Systématique, Evolution, Adaptation, Département able to ingest very large prey, oJ en greater in diameter Systématique et Evolution, C. P. 26, Muséum National d’Histoire than the snake itself (5), and the monophyly of the mac- b Naturelle, 43 Rue Cuvier, Paris 75005, France; Department of rostomatan condition is supported by several unambigu- Biology, 208 Mueller Laboratory, Pennsylvania State University, ous shared-derived characters (6). All venomous snakes University Park, PA 16802-5301, USA;c UMR 5143, Paléobiodiversité & Paléoenvironnements, Département Histoire de la Terre, C. P. 38, are found within Caenophidia, which includes the great Muséum National d’Histoire Naturelle, 8 rue Buffon, Paris 75005, majority of extant snakes (~2500 sp.) (1). France; dCentre national de séquençage, Genoscope, 2 rue Gaston- Previously, caenophidians were thought to comprise Crémieux, CP5706, 91057 Evry cedex, France A ve families: the aquatic acrochordids, the atractas- *To whom correspondence should be addressed (nvidal@mnhn.fr) pidids (now a subfamily; some of them with a front- fanged venom system), the elapids, and the viperids (all of them with a front-fanged venom system), and the large Abstract and paraphyletic family Colubridae (now split into eight Snakes have a Gondwanan origin and their early evolu- families), which includes rear-fanged snakes and the vast tion occurred mainly on West Gondwana, the supercontin- majority of caenophidians (~1900 sp.) (7–12). Here, the ent comprising South America and Africa. New data from relationships and fossil record of snakes are reviewed nine genes indicate that the divergence of Amerophidia and new data from nine nuclear protein-coding genes and Afrophidia occurred 106 (116–97) million years ago are analyzed, resulting in a timetree of snake families (Ma), supporting their origin by continental breakup. Most with new biogeographic implications. (~85%) living snakes are afrophidians and are globally dis- Several higher-level snake phylogenies using nuclear tributed now, but their initial radiation can be explained genes, including some that incorporated mitochondrial by dispersal out of Africa through Laurasia or India. Most genes, have been published since 2002 (13–21). 7 ey basal afrophidian families (Henophidia) diverged in the Cretaceous, 104–70 Ma, while most advanced afrophid- ian families (Caenophidia), diverged in the early Cenozoic, 63–33 Ma. Snakes are among the most successful groups of rep- tiles, numbering about 3070 extant species (1). 7 ey are divided into two main groups. 7 e fossorial scolecophid- ians (~370 sp.) are small snakes with a limited gape size and feed on small prey (mainly ants and termites) on a frequent basis. 7 e alethinophidians, or typical snakes (~2700 sp.), are more ecologically diverse and most spe- cies feed on relatively large prey, primarily vertebrates, on an infrequent basis (2, 3). According to most morpho- logical studies, a distinctive evolutionary trend within living snakes is the increase of the gape size from fossor- Fig. 1 Typhlops arator from Cuba, Typhlopidae (upper left); ial scolecophidians (Typhlopidae, Leptotyphlopidae, and Rhinocheilus lecontei from southwestern United States, Anomalepididae) and fossorial alethinophidians (Anilii- Colubridae (upper right); Cryptelytrops albolabris, from dae, Cylindrophiidae, Uropeltidae, and Anomochilidae) southeastern Asia, Viperidae (lower left); and Tropidophis feicki to ecologically diverse macrostomatan alethinophidian from Cuba, Tropidophiidae (lower right). Credits: S. B. Hedges. N. Vidal, J.-C. Rage, A. Couloux, and S.B. Hedges. Snakes (Serpentes). Pp. 390–397 in e Timetree of Life, S. B. Hedges and S. Kumar, Eds. (Oxford University Press, 2009). HHedges.indbedges.indb 339090 11/28/2009/28/2009 11:28:45:28:45 PPMM Eukaryota; Metazoa; Vertebrata; Sauropsida; Squamata; Serpentes 391 Dipsadidae 21 Pseudoxenodontidae 20 Colubridae 19 Natricidae 16 Elapidae 18 15 Lamprophiidae Homalopsidae 14 13 Viperidae 11 Pareatidae 8 Xenodermatidae Afrophidia Acrochordidae Alethinophidia Pythonidae 17 5 Loxocemidae 12 10 Xenopeltidae 7 Boidae 4 6 Uropeltidae Bolyeriidae 2 Tropidophiidae 9 Aniliidae 1 Anomalepididae Amerophidia Typhlopidae 3 Leptotyphlopidae Scolecophidia J Early K Late KPaleogene Ng MESOZOIC CENOZOIC 150 100 50 0 Million years ago Fig. 2 A timetree of snakes. Divergence times are shown in Table 1. Abbreviations: J (Jurassic), Ng (Neogene), and K (Cretaceous). all agree on the monophyly of alethinophidians, but a 7 e alethinophidians were therefore primitively striking result is the paraphyly of the macrostomatan macrostomatan, and this condition was secondarily condition. 7 e fossorial small-gaped Aniliidae (South lost twice by Aniliidae and Uropeltoidea, in connec- American genus Anilius) and the terrestrial large-gaped tion with burrowing (13, 17, 20). From a biogeographic (macrostomatan) Tropidophiidae (Neotropical genera point of view, the deep split between the Aniliidae– Trachyboa and Tropidophis) cluster together, and form Tropidophiidae clade, which is of South American ori- the most basal alethinophidian lineage (13, 16, 17, 19, gin, and all remaining alethinophidians was recently 20). 7 egenus Anilius is therefore not closely related to hypothesized to represent a vicariant event: the sep- the Asian families formerly placed in “Anilioidea.” We aration of South America from Africa in the mid- propose that Uropeltoidea Müller be used to describe the Cretaceous. Accordingly, those two clades were named monophyletic group (22) that includes Cylindrophiidae, Amerophidia and Afrophidia (20). Among alethi- Uropeltidae, and Anomochilidae. Also, we provisionally nophidians, the monophyly of the group including the use the taxon Henophidia HoB stetter to describe all non- Pythonidae, Xenopeltidae, and Loxocemidae is found in caenophidian Afrophidia, which usually form a mono- most molecular studies (13, 15–17, 20), with Loxocemidae phyletic group in molecular phylogenetic analyses. as the closest relative to Pythonidae. Another large group HHedges.indbedges.indb 339191 11/28/2009/28/2009 11:28:47:28:47 PPMM HHedges.indb 392 e d g e s . i n d b 3 9 2 Table 1. Divergence times (Ma) and their confi dence/credibility intervals (CI) among snakes (Serpentes). Timetree Estimates Node Time This study Ref. (19) Ref. (56) Ref. (58) Ref. (59) Ref. (60) Ref. (61) Ref. (62) Time CI Time CI Time CI Time Time CI Time CI Time Time CI 1 159.9 159.9 166–148 – – 102.3 113–94 – 131.1 138–124 109.0 119–99 – 144.2 – 2155.6155.6164–144–––– ––––– ––– 3151.9151.9163–137–––– ––––– –109.3– 4 105.8 105.8 116–97 121 129–106 62.1 75–49 – – – 50.0 56–44 – 76.1 87–69 5103.7103.7114–95112119–99–– –93.5–––––– 696.996.9108–87–––– ––––– ––– 792.092.0102–82–––– ––––– ––– 890.790.7104–78––54.966–44––––––58.771–54 989.189.1100–78110123–93–– ––––– –63.1– 1086.386.396–77–––– ––––– ––– 1182.282.296–69–––– ––––– –48.7– 1270.170.181–59–––– ––––– –51.3– 1364.064.077–526882–53–– –35.6–––––– 1454.354.367–43––38.545–3346.0––––74.3–– 1549.249.261–39–––– –––––69.4–– 1646.346.358–36––––42.5––––––– 1743.743.756–33–––– ––––– –37.1– 1841.541.553–32––––40.5––––62.934.0– 1939.839.850–31–––– –––––61.238.2– 2036.636.646–28–––– ––––– ––– 21 32.9 32.9 43–25 – – – – – – – – – – – – Note: Node times in the timetree are from the new analyses presented here. Other published estimates are also shown for comparison. 11/28/2009 1:28:47 PM / 2 8 / 2 0 0 9 1 : 2 8 : 4 7 P M Eukaryota; Metazoa; Vertebrata; Sauropsida; Squamata; Serpentes 393 includes Calabaria, “boines,” “erycines,” and ungali- caenophidian exemplar (Acrochordidae) was used and ophiines (genera Ungaliophis and Exiliboa), with North interfamilial caenophidian splits were not dated. American erycines and ungaliophiines as closest rela- Divergence times among all major groups of snakes tives (13, 17, 19, 20). Unfortunately, several higher-level are estimated here using nine nuclear protein-coding henophidian relationships are still unresolved (20), a genes (C-mos, RAG1, RAG2, R35, HOXA13, BDNF, JUN, situation contrasting with our better state of knowledge AMEL, and NT3). 7 ese were sequenced in 49 snake of the interfamilial relationships among caenophidian taxa representing all families with the exception of the snakes. Xenophidiidae, Anomochilidae, and Cylindrophiidae As recently as 2007, a study using seven nuclear (Alethinophidia). Tissue samples were obtained from the protein-coding genes (C-mos, RAG1, RAG2, R35, tissue collections of N. V. and S. B. H. (see 13, 14, 16, 20, HOXA13, JUN, and AMEL) resolved with strong sup- 24, 25 for details of the samples used). 7 e taxa included port the relationships of all families of caenophidians Iguanidae: Cyclura, Helodermatidae: Heloderma, Anom- (21). Caenophidians devoid of a front-fanged venom alepididae: Liotyphlops, Typhlopidae: Ramphotyphlops, system were traditionally lumped into a large (~1900 Typhlops, Leptotyphlopidae: Leptotyphlops, Aniliidae: sp.) family, “Colubridae,” including several subfamilies. Anilius, Tropidophiidae: Tropidophis, Trachyboa, Uro- Because this family was shown to be paraphyletic, most peltidae: Rhinophis, Uropeltis, Bolyeriidae: Casarea, of the subfamilies were elevated to a familial rank to Loxocemidae: Loxocemus, Xenopeltidae: Xenopeltis, reP ect their evolutionary distinctiveness, and the name Pythonidae:
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