Palaeontologia Electronica palaeo-electronica.org

Fossil calibration dates for molecular phylogenetic analysis of snakes 2: Caenophidia, Colubroidea, Elapoidea, Colubridae

Jason J. Head, Kristin Mahlow, and Johannes Müller

ABSTRACT

Caenophidia, the snake clade that includes the highest species richness, morpho- logical diversity, and ecological breadth within Serpentes, has been extensively studied with respect to molecular phylogenetic systematics. The majority of the caenophidian fossil record, though dense, has been taxonomically defined on the basis of general anatomical similarity or shared geographic provenance with extant reference taxa. As a result, historical patterns of diversification within the clade are poorly constrained due to a paucity of reliable fossil calibration dates. Here we provide 10 fossil calibration dates for phylogenetic analysis of caenophidian relationships. Calibration points include apomorphy-based systematic justifications based on cranial and precloacal vertebral elements and precise dates for hard minimum divergence timings. Calibrated nodes are for Caenophidia, Acrochordus, Elapoidea, Colubridae, and constituent sub- clades. Hard minimum divergence timings range from late Cretaceous to Miocene. The spatial and temporal distribution of reliable first occurrence of colubroid taxa suggests late Paleogene intercontinental dispersals between Asia, North America, and Africa, followed by rapid diversification and subsequent dispersals into all non-Polar conti- nents by the early Neogene.

Jason J. Head. Department of Zoology and University Museum of Zoology, Downing St., University of Cambridge, CB2 3EJ, England [email protected] Kristin Mahlow. Museum für Naturkunde, Leibniz-Institut für Evolutions- und Biodiversitätsforschung, Invalidenstr. 43, D-10115 Berlin, Germany [email protected] Johannes Müller. Museum für Naturkunde, Leibniz-Institut für Evolutions- und Biodiversitätsforschung, Invalidenstr. 43, D-10115 Berlin, Germany [email protected]

Keywords: Serpentes; fossil; calibration; Caenophidia; Colubroidea; Elapoidea; Colubridae

Submission: 13 January 2016 Acceptance: 16 May 2016

PE Article Number: 19.2.9FC Copyright: Palaeontological Association June 2016 Submission: 13 January 2016. Acceptance: 16 May 2016 Head, Jason J., Mahlow, Kristin, and Müller, Johannes. 2016. Fossil calibration dates for molecular phylogenetic analysis of snakes 2: Caenophidia, Colubroidea, Elapoidea, Colubridae. Palaeontologia Electronica 19.2.2FC: 1-21 palaeo-electronica.org/content/fc-9

Calibrations published in the Fossil Calibration Series are accessioned into the Fossil Calibration Database (www.fossilcalibra- tions.org). The Database is a dynamic tool for finding up-to-date calibrations, and calibration data will be updated and annotated as interpretations change. In contrast, the Fossil Calibration papers are a permanent published record of the information on which the cal- ibrations were originally based. Please refer to the Database for the latest data. HEAD, MAHLOW, & MÜLLER: CAENOPHIDIAN CALIBRATIONS

INTRODUCTION Szyndlar and Schleich, 1993; Szyndlar and Rage, 1999; Holman, 2000 [and references therein]; Iva- The vast majority of extant snake diversity is nov, 2000, 2002; Ivanov and Böhme, 2011), as well contained in Caenophidia, a clade consisting of > as records from South America, Africa, and Asia 2500 species (Vidal et al., 2009). Caenophidia was (e.g., Albino, 1996; Albino and Montalvo, 2006; originally erected by Hoffstetter (1939) to include Rage, 1973, 1976, 2003; Rage and Ginsburg, snakes more derived than “henophidian grade” 1997; Rage and Danilov, 2008; Head, 2005, Head taxa, considered at the time to include boids and et al., 2006; Head et al., 2007; Head and Bell, anilioids. Morphological studies recognized a close 2008). The published record has been used to cali- relationship between relationship between Colu- brate multiple caenophidian molecular phylogenies broidea, itself consisting of viperids, colubrids, ela- (e.g., Noonan and Chippindale, 2006; Burbrink and pids, homalopsids, and other “derived snakes”, and Lawson, 2007; Wüster et al., 2007, 2008; Alfaro et Acrochordus, the genus of file snakes, wart al., 2008; Sanders and Lee, 2008; Sanders et al., snakes, and elephant trunk snakes (e.g., Bellairs 2010; Kelly et al., 2009; Lukoschek et al. 2012; and Underwood, 1951), with explicit morphological Pyron and Burbrink, 2012), with different fossils phylogenetic analyses recovering a sister-taxon employed to produce highly disparate divergence relationship between the two (e.g., Rieppel, 1988; estimates (Lukoschek et al., 2012). Kluge, 1991; Cundall et al., 1993; Lee and Scan- There are multiple problems with calibrating lon, 2000; Tchernov et al., 2000). molecular phylogenies using the published litera- Numerous molecular phylogenetic studies of ture on fossil snakes (Head, 2015), especially for caenophidians have subsequently been con- caenophidians: The absence of discrete apomor- ducted. Research foci associated with these analy- phies in vertebral morphology for most taxa limits ses include molecular divergence timing estimates, testable, reproducible taxonomic hypotheses from biogeographic histories, diversification patterns, isolated fossils. Additionally, considerable intraco- and the evolution of toxic venoms, making them lumnar, individual, and ontogenetic variation exists the most intensely studied squamate clade with in vertebral morphology, and very few studies have respect to molecular phylogenetics (e.g., Keogh, attempted to examine the influence of these factors 1998; Burbrink et al., 2000; Gravlund et al., 2001; in taxonomic assignments (Szyndlar, 2012 [but see Burbrink, 2002; Vidal, 2002; Fry et al., 2003; Kelly Szyndlar, 1984 and LaDuke, 1991a for analyses of et al., 2003; Keogh et al., 2003; Nagy et al., 2003; intracolumnar and individual variation]). Pinou et al., 2004; Lawson et al., 2005; Lukoschek Because of these potential limitations, identity and Keogh, 2006; Burbrink and Lawson, 2007; of snake fossils has traditionally relied on a gener- Vidal et al., 2007; Fry et al., 2008; Sanders et al., alized “vertebral form taxonomy” that uses overall, 2008; Hedges et al., 2009; Kelly et al., 2009; Pyron often proportional, shape to recognize taxa and and Burbrink, 2009a,b,c; Zaher et al., 2009; Bur- implicitly does not follow a phylogenetic taxonomy, brink and Pyron, 2010; Sanders et al., 2010; Vidal despite using the same taxon names (see Szyndlar et al., 2010; Murphy et al., 2011; Pyron et al., et al., [2008] and Szyndlar, [2012] for discussion). 2013a,b). The majority of studies have recovered Other approaches include general similarity/ the same sister-taxon relationship between Acro- “gestalt” approaches (see Hecht and LaDuke, 1997 chordus and taxa traditionally included in Colu- for discussion), unsupported authority statements, broidea (but see Pyron et al., 2013a for an and the geographic provenance of extant taxa alternate hypothesis of sister-taxon relationships of (e.g., Holman, 2000[and references therein]), Acrochordus). which results in circularity in reconstructing tempo- The caenophidian fossil record has been ral and spatial histories of extant clades (Bell et al., more thoroughly documented than for any other 2004; Bell et al., 2010). The caenophidian record squamate clade, with a few Late Cretaceous to does not lack utility, however. Diagnostic vertebral early Paleogene records primarily, but not exclu- characters are observable (e.g., Hoffstetter and sively, from southern continental landmasses (e.g., Gasc, 1969; Slowinski, 1994; Sheil and Grant, Rage, 1975; Rage, 2008; Rage et al., 1992; Rage 2001, Head, 2005), and cranial remains are pre- and Werner, 1999; Rage et al., 2008; Rage et al., served for several key taxa. 2013; Parmley and Holman, 2003; Head et al., Here we provide fossil calibrations for multiple 2005) and hundreds of records from the late Paleo- caenophidian clades based on observable apo- gene to Holocene of mainly North America and morphies. We restrict calibrations to taxa repre- Europe (e.g., Rage, 1984[and references therein]; sented by either diagnostic cranial remains or Szyndlar, 1984, 1985, 1987, 1991a, 1991b, 2012;

2 PALAEO-ELECTRONICA.ORG vertebrae that can be diagnosed by discrete char- Russellophiidae on the basis of brief, ven- acters or unique character combinations. Using trolaterally angled articular facets of the this approach, we are only able to recognize 10 prezygapophyses and compressed prezy- extant caenophidian taxa relative to the many doz- gapophyseal buttresses that form a verti- ens recognized by the aforementioned methods, cal ridge, as well as more ambiguously by but our calibrations are testable observations that an elevated posterior neural arch (Rage allow analysis of systematic, ecological, and bio- and Werner, 1999). Characters that unite geographic hypotheses of extant caenophidians Russellophiidae, including Krebsophis, because their phylogenetic justifications are inde- with Caenophidia include a highly elongate pendent of the histories of those taxa. There are centrum, relatively small, circular cotyle two published comprehensive molecular phyloge- and condyle, and well-developed subcen- nies of Caenophidia that can be used as scaffolds tral paralymphatic channels defining the for node calibration (Pyron et al., 2013a, b). We lateral margins of a distinct haemel keel. use the topology of Pyron et al. (2013a) because it Minimum Age. 66 Ma, latest Maastrich- includes greater taxonomic and sequence sam- tian. pling, but additionally consider the topology of Maximum Age. 72.1 Ma, latest Campan- Pyron (2013b) where appropriate. ian to earliest Maastrichtian. Age Justification. Krebsophis thobanus Institutional Abbreviations was recovered with a taxonomically BSP, Bayerische Staatssammlung Für Paläontolo- diverse snake fauna from the Wadi Abu gie Und Historische Geologie, Munich; H-GSP, Hashim member of the Wadi Milk Forma- Harvard-Geological Survey of Pakistan; Islam- tion of Sudan (Werner and Rage, 1999). abad, Pakistan; MCZ, Museum of Comparative The Wadi Milk Formation was considered Zoology, Harvard University, Massachusetts, Cenomanian based on palynological U.S.A.; MGT, Université Montpellier; MNHN, (Schrank,1990; Schrank and Awad, 1990) Muséum National d’Histoire Naturelle, Paris, and fish data (see Werner and Rage, France; QM F, Queensland Museum, Queensland, 1999). However, the snake fauna of Wadi Australia; UCBL, Université Claude Bernard, Lyon; Abu Hashim is much more biostratigraphi- UNSM, University of Nebraska State Museum, cally consistent with a Maastrichtian age Nebraska, U.S.A. VAS, “R.S. Rana collection from assignment: Nigerophiids and large-bod- Vastan” (Rage et al., 2008); Vb, the abbreviation ied madtsoiids are only present in Maas- “Vb” is not defined in Rage and Werner (1999); trichtian sections of Madagascar and India however, specimens labeled with “Vb” and field (e.g., Prasad and Rage, 1995; Rage et al., numbers were reported to be “…curated at the fos- 2004; LaDuke et al., 2010; Mohabey et al., sil collection of the Technical University of Berlin- 2011; Pritchard et al., 2014), the oldest Special Research Project 69…” (Rage and Werner, record of palaeophiids is from the Maas- 1999: 87), and are now housed in the Museum für trichtian of Morocco (Rage and Wouters, Naturkunde Berlin. 1979), the oldest aniliid anatomically con- sistent with “Coniophis” from Wadi Abu CALIBRATIONS Hashim is Australophis from the late Cam- panian-Early Maastrichtian of Argentina (1) Pan-Caenophidia (Goméz et al., 2008, see Head [2015] for Node Calibrated. Divergence between the discussion of the age of Australophis), and total clade of Caenophidia and its nearest anatomically similar “Coniophis” is known crown sister taxon, Booidea (sensu Head, from the Maastrichtian of India (Rage et 2015). al., 2004). Referral to two snake speci- Fossil Taxon. Krebsophis thobanus (Rage mens from Wadi Abu Hashim to Early Cre- and Werner, 1999). taceous “lapparentophiid-grade snakes” by Specimen. Vb-681, incomplete precloacal Rage and Werner (1999) was admittedly vertebra. based solely on plesiomorphic characters, Additional Materials. Six precloacal ver- which are taxonomically uninformative. A tebrae. Cenomanian age for madtsoiids, niger- Phylogenetic Justification. Krebsophis ophiids, palaeophiids, and “Coniophis” thobanus is unambiguously included within form taxon aniliids would represent at least

3 HEAD, MAHLOW, & MÜLLER: CAENOPHIDIAN CALIBRATIONS

20 million year range extension for all, of Fossil Taxon. Procerophis sahnii (Rage et which there is no additional unambiguous al., 2008). evidence. Additionally, the Shendi Forma- Specimen. VAS 1014, posterior trunk ver- tion of Sudan, which shares a vertebrate tebra. fauna with the Wadi Milk Formation (J.M. Additional Materials. Five precloacal ver- pers. obs.) and previously considered a tebrae, two caudal vertebrae. lateral extension of the Wadi Milk, has Phylogenetic Justification. Procerophis recently been dated as Campanian-Maas- is assigned to Colubroidea on the basis of: trichtian (Salih et al., 2015). Based on elongate, narrow centrum and neural arch, ages of comparable snake faunas from paracotylar foramina, and an anteroposte- other Gondwanan landmasses and the riorly elongate neural spine that possesses age estimates for the Shendi Formation, a uniform width along its length. we assign an age range for Krebsophis Minimum Age. 50.5 Ma, middle Ypresian. based on minima for the Campanian and Maximum Age. 72.1 Ma, earliest Maas- Maastrichtian (Ogg et al., 2012). trichtian. Discussion. The systematic relationships Age Justification. Procerophis was of russellophiids are poorly constrained. recovered from a diverse snake fauna in Russellophis tenius was originally consid- the Cambay Formation, Gujarat, India. The ered a primitive caenophidian by Rage Cambay Formation is minimally dated (1975) on the basis of small prezygapoph- based on the occurrence of the planktonic yseal accessory processes and synapoph- foraminifera taxon Nummulities burdigal- yseal morphology that is anatomically ensis burdigalensis, which corresponds to consistent with “henophidian” taxa. Subse- Shallow Benthic Zone 10 (lower Cuisian, quent records have been placed either Serra-Kiel et al., 1998). SBZ 10 corre- within only Caenophidia (“?Russellophii- sponds to planktonic foraminiferal zone dae” Rage, 2008), or Colubroidea within P6b, which is middle Ypresian, approxi- Caenophidia (e.g., Rage et al., 2008). mately 53-50.5 Ma (Vandenberghe et al., Explicit character support for inclusion of 2012). Maximum age is for the early Maas- Russellophiidae within the colubroid total trichtian based on the first occurrence of clade has not been provided, but a test- Caenophidia from the Wadi Milk Formation able hypothesis for the interrelationships of (Werner and Rage, 1999). the clade is required to calibrate Caeno- Discussion. Among extant colubroids, phidia and potentially Colubroidea. Russel- these characters are characteristic of colu- lophiids share an elongate centrum with brines. However, Procerophis possesses a colubroids to the exclusion of Acrochor- plesiomorphic prezygapophyseal morphol- dus, however, they lack vertebral synapo- ogy (Rage et al., 2008), including prezyga- morphies of crown Caenophidia, including: pophyseal articular facet long axis well-developed prezygapophyseal acces- predominately anteriorly angled, and small sory processes, well-differentiated para- accessory processes. Additionally, the and diapophyseal articular facets of the haemal ridge is poorly differentiated from synapophyses, and pleurocentral hypa- the ventral surface of the central body, pophyses present throughout the precloa- unlike crown colubroids. cal vertebral column. Due to these Thaumastophis missiaeni, also from the character distributions, placement of Rus- Cambray Formation, similarly lacks a sellophiidae within Colubroidea cannot be hypapophysis, and the majority of verte- supported, and the fossil record of the bral morphology is consistent with assign- clade can only calibrate the caenophidian ment to Colubroidea. However, the taxon total clade. possesses vertical, blade-like prezyga- pophyseal accessory processes, which are (2) Pan-Colubroidea otherwise apomorphic for Acrochordus. As Node Calibrated. Divergence between the a result, the taxon is here considered total clade of Colubroidea and its nearest Caenophidia indeterminate, following crown sister taxon, (Acrochordus+Xeno- Rage et al. (2008). dermatidae).

4 PALAEO-ELECTRONICA.ORG

Russellophis crassus, also from the Cam- Kamlial Formation of the Siwalik Group on bay Formation, is a potential alternate the Potwar Plateau of Pakistan, which is anchor taxon for the Pan-Colubroidea the oldest record of Acrochordus dehmi divergence. As previously noted, however, (Head, 2002, 2005). The maximum age the systematic relationships of russellophi- follows Head et al. (2007) based on the ids relative to either the caenophidian first occurrence of the genus from the crown or the colubroid total clade are Aquitanian Kharinadi Formation, Gujarat, poorly constrained. Colubroid characters India. including an elongate, narrow neural spine Discussion. Bayesian molecular diver- of a uniform transverse width that extends gence estimates for Acrochordus javani- from the zygosphene to the posterior cus from (A. arafurae+A. granulatus) median notch of the neural arch, paracoty- based on the calibration points cited here lar foramina, comparatively well-developed model a divergence of 20.3 Ma with a prezygapophyseal accessory processes, range of 6.6-34.0 Ma (95% highest poste- and potentially well-differentiated dia-and rior density values) (Sanders et al., 2010). parapophyseal articular facets, are present The fossil record of Acrochordus also con- in Procerophis but absent in russellophiids strains the divergence timing of Xenoder- (e.g., Rage, 1975; Rage and Werner, matidae following Pyron et al. (2013a); 1999; Rage, 2008), indicating that Procer- however, xenodermatids are more closely ophis is the most appropriate minimum related to colubroids than Acrochordus in divergence point for the colubroid total the topology of Pyron et al. (2013b). clade. (4) Viperinae (3) Acrochordus javanicus Node Calibrated. Divergence between Node Calibrated. Divergence between total clades Crotalinae+Viperinae Acrochordus javanicus and (A. ararfu- Fossil Taxon. “Vipera aspis complex” rae+A. granulatus). (Szyndlar and Rage, 1999). Fossil Taxon. Acrochordus dehmi (Hoff- Specimen. MNHN SG 13732, precloacal stetter, 1964). vertebra. Specimen. H-GSP 41555, two precloacal Additional Materials. MNHN SG 13733, vertebrae. posterior precloacal vertebra (Szyndlar Additional Materials. Five precloacal ver- and Rage, 1999). tebrae, two caudal vertebrae. Phylogenetic Justification. Assignment Phylogenetic Justification. Acrochordus to Viperidae is based on a large, elongate, dehmi is hypothesized to be the sister straight, and posteroventrally angled hypa- taxon to A. javanicus to the exclusion of A. pophyses, laterally short prezygapophy- arafurae or A. granulatus on the basis of seal accessory processes, large cotyle parazygosphenal foramina located just and condyle, low and flattened posterior ventrolaterally to the base of the zygo- neural arch, and elongate, anteroventrally sphene on the anterolateral surface of the angled parapophyseal process (sensu neural arch (Head, 2005; Sanders et al., Head, 2005) (Szyndlar, 1991b; Szyndlar 2010). Acrochordus dehmi is placed within and Rage, 1999). Assignment to Viperinae the genus Acrochordus on the basis of relative to Crotalinae is based on the pres- ventrally elongate and pendant synapoph- ence of low neural spines, which is yses, hemispherical, vertically oriented restricted the “aspis complex: of extant and blade-like prezygapophyseal acces- European viperines (e.g., Szyndlar, 1984, sory processes, and multiple paracotylar 1991b, Szyndlar and Rage, 1999). foramina (Hoffstetter, 1964; Head, 2005). Minimum Age. 20.0 Ma, youngest age for Minimum Age. 18.05 Ma. MN2 (Agustí et al., 2001). Maximum Age. 23.03 ± 0.05 Ma, earliest Maximum Age. 23.8 Ma (Agustí et al., Aquitanian, earliest Miocene (Hilgen et al., 2001), oldest age for MN1 (see below). 2012). Age Justification. The minimum age is for Age Justification. The minimum age is the youngest age for Neogene Mammal based on dating of locality Y846 from the (MN) Biochron 2, based on the age of the

5 HEAD, MAHLOW, & MÜLLER: CAENOPHIDIAN CALIBRATIONS

St-Gérand-le-Puy complex (Szyndlar and bral characters. These record do not mini- Rage, 1999, 2001). The youngest absolute mally calibrate the divergence of viperids, age for MN2 is poorly constrained, but at as they are predated by the first occur- minimum age of 20.0 Ma is estimated, rence of the viperid sister taxon (see based on correlation of the oldest MN3 below). The oldest unambiguous crotaline fossil localities with Geomagnetic Polarity fossil record consists of two maxillae from Timescale (GMPT) chron C6n (Agustí et the late Miocene of Ukraine (Ivanov, 1999), al., 2001). Many St-Gérand-le-Puy locali- and is much younger than the viperine ties are within MN 2a (e.g., Göhlich et al. record we cite to calibrate the viperine-cro- 2005). If the St-Gérand-le-Puy viperid fos- taline divergence. sils are from these localities, then the mini- (5) Colubridae+Elapoidea mum age would be slightly older at the top of GMPT chron 6AAn, dated to approxi- Node Calibrated. Divergence of crown mately 21.8 Ma (Sen, 1997 after Agustí et colubroid lineages. al., 2001). The maximum age is for the Fossil Taxon. Coluber cadurci Rage, base of MN 1, the age of the oldest viperid 1974. fossil from Weisenau, Germany (Szyndlar Specimen. MGT 3505 precloacal vertebra and Böhme, 1993; Szyndlar and Rage, (holotype). 1999, 2002). Additional Materials. MGT 3506, caudal Discussion. Viperids possess a distinct vertebra, “plusieurs vertèbres dorsales et vertebral morphology that includes a caudales” (Rage, 1974:295). straight, elongate, and posteroventrally ori- Phylogenetic Justification. Assignment ented hypapophysis that is present to (Colubridae+Elapoidea) is based on the throughout the prelcoacal vertebral col- presence of: a well-developed, narrow umn, strongly depressed neural arches, haemel keel that is uniform in transverse extremely elongate parapophyseal pro- width and extends from an expanded coty- cesses, relatively short prezygapophyses lar ventral lip anteriorly to terminate poste- with short, blunt accessory processes, and riorly just anterior to the condyle; large cotyle-condyle articulations. An ana- epizygapophyseal spines, and; elongate tomical distinction has been made prezygapophyseal accessory processes between the “oriental vipers” (composed of (Rage, 1974). species of the subgenus Montivipera and Minimum Age. 30.9 ± 0.1 Ma the Macrovipera) and the “Vipera aspis Soft Maximum Age. Indeterminate. complex (composed of primarily V. aspis Age Justification. The minimum age is and V. ammodytes) based on small size, based on the age of the type locality at elongate centra and short neural spines in Mas de Got A, which is correlated to the latter complex (Szyndlar and Rage, Paleogene Mammal (MP) biochron 22. MP 1999). Among extant taxa, these charac- 22 ranges from 32.6 ± .1 Ma to 30.9 ± .1 ters do distinguish the “aspis complex” Ma (Schmidt-Kittler, 1987; İslamoğlu et al., species from other taxa, but there are no 2006; Szyndlar, 2012; Rage, 2006; Augé other vertebral characters that differentiate and Rage, 2014). the majority of other viperine taxa from cro- Discussion. Referral of Coluber cadurci to talines. As a result, the record described the total clade (Colubridae+Elapoidea) is from the St-Gérand-le-Puy complex rep- unambiguously supported by the afore- resents the oldest definitive viperine fossil mentioned character combination. The record. The oldest records of viperids are presence or absence of ventral hypapoph- from Weisenau (Szyndlar and Böhme, yses throughout the precloacal vertebral 1993) and the Harrison Formation of column has traditionally been used to dis- Nebraska (Holman, 1981), and predate the tinguish Colubrinae from Natricinae and/or “V. aspis complex) by up to four million Elapidae (Bell et al., 2003; Szyndlar, years. However, the identities of these 2012), and was used in the original taxo- records as either stem viperids, crown nomic assignment of C. cadurci (Rage, viperines, and/or crown crotalines cannot 1974); however, absence of continuous be unambiguously determined from verte- precloacal hypapophyses occurs in numer-

6 PALAEO-ELECTRONICA.ORG ous elapoid and dipsadine taxa in addition (6) Naja to Colubrinae (Dowling and Duellman, Node calibrated. Divergence between 1978 after Pyron et al., 2013), and the Naja and Haemachatus. character cannot diagnose colubrines to Fossil Taxon. Naja romani (Hoffstetter, the exclusion of other clades. Similarly 1939). Coluber cannot be diagnosed on the basis Specimen. UCBL 92856 partial skeleton of vertebral morphology (Szyndlar, 2012), including maxillae, prefrontal, postorbital, and referral to the genus has been subse- fragmentary parietal, parabasisphenoid, quently recognized as non-phylogenetic otoocipital, supratemporals, quadrates, (Rage, 1988:468). The morphology of the articular, splenial, and dentary (Hoffstetter, haemal keel in C. cadurci is consistent with 1939). colubrids and elapoids that similarly lack a Additional Materials. Supraoccipital (BSP hypapophyses, and is distinct from the 1976 XXII 7668) (Szyndlar and Schleich, morphology of the keel in russelophiids 1993), parabasisphenoid (No. 1984/98), and more basal snakes in which the keel is partial pterygoids (No. 1984/104/1, 1984/ often wide and more poorly defined (Head, 104/2), right dentary (1984/104/3), right 2015). As a result, Coluber cadurci pro- frontal (1984/104/4), left maxilla (1984/99). vides a calibration for the total clade of See Szyndlar and Schleich (1993) and (Colubridae+Elapoidea) but cannot con- Bachmeyer and Szyndlar (1985) for addi- strain divergences within the clade. tional cranial and vertebral elements. Natrix mlynarskii is approximately coeval Phylogenetic Justification. Assignment with C. cadurci, and was assigned to of to the genus Naja is based on an Natrix based on general resemblances anteroposteriorly short and laterally with modern and fossil species of genus recurved maxilla with two large anterior (Rage, 1988). The type specimen of N. venom fangs and two solid posterior teeth mlynarskii is too incomplete for unambigu- (Hoffstetter, 1939; Bogert, 1943) and ous referral to Natrix, but appears to pos- fenestra vestibuli completely or nearly sess a distinct, short hypapophysis similar completely bounded within the otooccipital to natricines, some dipsadines, and most (Hoffstetter, 1939; Szyndlar and Rage, elapoids. The records of Coluber cadurci 1990). and Natrix mlynarskii predate the oldest Minimum Age. 17.0 Ma definitive records of elapoids from the late Soft Maximum Age. Indeterminate. Oligocene by approximately 6 Ma (McCart- Age Justification. The minimum age is ney et al., 2014). based on the maximum age for MN4, the Older colubroid records that have been age of the Petersbuch 2 locality (Szyndlar referred to Colubridae or constituent sub- and Schleich, 1993; Ivanov, 2000; Agustí clades extend into the early Paleogene of et al., 2001). Asia and North America (Rage et al., 1992; Discussion. Hoffstetter (1939) erected the Parmley and Holman, 2003). However, taxon Paleonaja romani based on UCBL these records are too incomplete to distin- 92856. He considered the taxon to be guish from stem Colubroidea and are most closely related to Ophiophagus han- therefore uninformative with respect to nah among extant cobras, with similarities divergence of the (Colubridae+Elapoidea) to extant Naja the result of parallel evolu- total clade. Similarly, additional records tion: “Toutes ces observations et les car- referred to Colubroidea from the Eocene of actères morphologiques de detail Africa and South Asia (Rage et al., 2003, mentionnés plus haut conduisent à 2008; Head et al., 2005; McCartney and admettre que P. r om a ni est plus proche de Seiffert, 2015) demonstrate the occurrence N. hannah que de toute autre espèce actu- of the total clade in the Old World, but can- elle. Cependant, la dysharmonie de ses not constrain the divergence timing of caractères ostéologiques rend improbable crown Colubroidea or the (Colubri- une filiation directe de la forme Miocène au dae+Elapoidea) total clade. type actuel. Il semble plutôt que Palaeo- naja romani représente un rameau par- allèle à celui des Naja, et il convient de le

7 HEAD, MAHLOW, & MÜLLER: CAENOPHIDIAN CALIBRATIONS

designer sous un nom générique nou- Szyndlar and Rage (1990) on the basis of veau.” (Hoffstetter, 1939:65). Bogert neurocranial characters. However, these (1943) recommended assigning P. romani characters are either explicitly recognized to the genus Naja, on the basis of anatom- as plesiomorphic for the genus (Szyndlar ical similarities with extant N. haje, but did and Rage, 1990, Szyndlar, 1992), or are not provide specific character evidence. untested with respect to phylogenetic Szyndlar and Rage (1990) Paleonaja with polarity. Because elapine osteology has Naja, and assigned N. romani to the Asi- not been either rigorously optimized on a atic clade of Naja on the basis of a short molecular phylogenetic topology or been vidian canal with an anterior opening used to construct a phylogenetic hypothe- bounded by the parabasisphenoid and the sis, there is no way to unambiguously fenestra vestibule bounded by the otoocip- place the fossil record within the phylogeny ital. Szyndlar and Zerova (1990) addition- of living species, and we here use the ally proposed an Asian Naja affinity for N. record to only constrain the Naja total romani on the basis of a narrow parabasi- clade (Wallach et al., 2009). sphenoid rostrum. Conversely, Wallach et Fossils attributed to Naja primarily on the al. (2014) assigned N. romani to the genus basis of precloacal vertebral morphology Afronaja as part of the African clade of have been documented throughout the cobras, without justification. Neogene of Europe and Africa (Bach- Based on cranial osteology, Naja romani meyer and Szyndlar, 1985, 1987; Szynd- can be used to unambiguously calibrate lar, 1985, 1991, 2009a,b; Meylan, 1987; the divergence of Naja from Haemachatus Szyndlar and Zerova, 1987; Bailon, 1989; (Pyron et al., 2013a). Calibrating diver- Szyndlar and Rage, 1990; Ivanov, 2000; gences within Naja, however, is problem- Miklas-Tempfer, 2002; Rage, 2003; Dax- atic. Of the characters used to unite N. ner-Höck et al., 2004; Camora et al., 2010; romani with Asian Naja (Naja subgenus of Rage and Bailon, 2011; Blain et al., 2013); Wallach et al., 2009), none are unambigu- however, vertebral morphology is not diag- ous synapomorphies of that clade: Enclo- nostic for the genus with respect to other sure of the fenestra vestibule within the elapid taxa (e.g., Smith, 1975; McCartney otoocipital occurs in Naja naja but only et al., 2014). The oldest record of the polymorphically in other Asian species as genus based on cranial elements is Naja well as African N. haje (Szyndlar and romani from the early Miocene Petersbuch Rage, 1990); the anterior opening of the 2 locality of Germany (Szyndlar and Schle- vidian canal within the parabasisphenoid ich, 1993). This record consists of a supra- additionally occurs in Pseudohaje and occipital, frontal, dentary fragment, and Aspidelaps (Szyndlar, 1992); short vidian partial compound bone. The supraoccipital canals occur in Pseudohaje, Aspidelaps, is the only element explicitly discussed and and N. haje (Szyndlar, 1992); and a com- is described as being morphology indiffer- parably narrow parabasisphenoid occurs ent from supraoccipitals of extant Naja in Aspidelaps, and N. haje (Szyndlar, species (Szyndlar and Schleich, 1993). 1992). Additionally, N. romani possess the (7) Oxyuraninae same maxillary tooth formula of two venom fangs and two solid posterior teeth as Afri- Node Calibrated. Divergence between can Naja. Laticauda+Oxyuraninae. Other Neogene Naja species have been Fossil Taxon. Incongruelaps iteratus described on the basis of neurocranial Scanlon et al. (2003). anatomy. Naja antiqua, represented by a Specimen. QM F23085, right maxilla. partial neurocranium and precloacal verte- Additional Materials. Six precloacal ver- brae from the middle Miocene (MN 7) of tebrae. Morocco (Rage, 1976) and Naja iberica, Phylogenetic Justification. Assignment represented by a partial neurocranium and to Oxyuraninae is based on the presence skull roof from the latest Miocene (MN 13) of five posterior maxillary teeth and of Spain (Szyndlar, 1985). Both taxa have absence of a distinct palatine articular been referred to the “African complex” of

8 PALAEO-ELECTRONICA.ORG

facet on the palatine process of the maxilla Minimum Age. 10.215 Ma (Barry et al., (Scanlon et al., 2003). 2002). Minimum Age. ~ 10 Ma (Myers et al., Maximum Age. Indeterminate. 2001; Scanlon et al., 2003). Age Justification. The minimum age is Maximum Age. Indeterminate. based on the maximum age estimate for Age Justification. The minimum age is locality Y-450, the oldest record of Bun- based on a combination of mammalian garus from the Siwalik Group of the Potwar biostratigraphy and phylogenetic relation- Plateau, Pakistan (Barry et al., 2002; ships of mammals from the Encore Local Head, 2005). Precise magnetostrati- Fauna relative to the late Miocene Alcoota graphic analysis combined with sedimen- Local Fauna and the middle Miocene Sys- tation rate estimates has resolved Siwalik tem C Local Fauna from Riversleigh Group fossil localities to a temporal resolu- (Myers et al., 2001). tion of 104 years (e.g., Flynn et al., 1990; Discussion. Scanlon et al. (2003) cited Barry et al., 2002). multiple qualitative characters of the max- Discussion. Bungarus is one of the few illa that unite Incongruelaps with oxyura- snake taxa that can be diagnosed to sub- nines (sensu Sanders and Lee, 2008) and generic levels on the basis of vertebral other elapids, and the aforementioned synapomorphies (Hoffstetter, 1939; Slow- characters unite the taxon with Oxyura- inski, 1994). The hypertrophied, wing-like ninae to the exclusion of Laticauda. The prezygapophyseal accessory processes Australian fossil record of Elapids extends are diagnostic for the genus, and the pos- from the Quaternary through the Neogene session of the wing-like lateral postzyga- (e.g., Smith, 1976; Scanlon, 2003). The pophyseal processes diagnoses Bungarus oldest record was previously considered to species as more derived than B. flaviceps be latest Paleogene based on a precloacal and B. bungaroides (McDowell, 1970; vertebra from the RSO site of Riversleigh Slowinski, 1994). Presence of the posterior (Scanlon et al., 2003); however, RSO has processes unites the Siwalik Group Bun- been radiometrically dated to 16.55 ± 0.29 garus with the unresolved polytomy of Ma (Woodhead et al., 2016). A maximum derived species from Slowinski (1994) or age for the divergence of the total clade the clade subtended by B. faciatus and B. Hydrophiinae is potentially determined multicinctus from Pyron et al. (2013b). from the first occurrences of Elapidae (e.g., McCartney et al., 2014 vs. Kuch et (9) Heterodon + Farancia al., 2006), but we refrain from such a cali- Node Calibrated. Divergence between the bration due to the coarse phylogenetic res- clade subtended by Heterodon and Faran- olution of those records. cia. (8) Bungarus Fossil Taxon. Paleheterodon tiheni (see discussion). Node Calibrated. Divergence between Specimen. UNSM 46504, partial skull and Bungaurs bungaroides, B. flaviceps, and associated vertebrae. the B. fasciatus clade. Additional Materials. None (see discus- Fossil Taxon. Bungarus sp. Head (2005). sion). Specimen. H-GSP 53026, partial precloa- Phylogenetic Justification. Assignment cal vertebra. of UNSM 46504 to a clade including Het- Additional Materials. Six precloacal ver- erodon to the exclusion of Diadophis and tebrae. Pseudoboa is based on the character com- Phylogenetic Justification. Assignment bination of: 1) a quadrate with a narrow to the clade consisting of Bungarus spe- and strongly recurved distal shaft and a cies more closely related to each other wide, narrow suprastapedial crest; 2) a than to B. bungaroides or B. flaviceps is narrow ventrally curved compound bone; based on the presence of both expanded 3) A parietal with a broad, well-defined prezygapophyseal accessory processes skull table; 4) a supraoccipital with a well- and postzygapophyseal accessory pro- defined sagittal crest. cesses (McDowell, 1970; Slowinski, 1994). Minimum Age. ~ 12.08 Ma.

9 HEAD, MAHLOW, & MÜLLER: CAENOPHIDIAN CALIBRATIONS

Maximum Age. Indeterminate. recurved. Conversely, the basicranium and Age Justification. The minimum age is skull roof are radically different between based on the Swallow Ash of the lower- the two taxa. Heterodon possesses an most Ash Hollow Formation, which suc- apomorphically short posterior skull, ceeds the Valentine Formation (Tedford et whereas cranial elements of Paleohetero- al., 2005). The Myers Farm fauna is coeval don include a comparatively elongate pari- with the Valentine Formation based on etal and supratemporal with well- mammalian faunal composition and is con- developed muscle attachment crests. The sidered latest Barstovian (e.g., Janis et al., parabasiphenoid of Heterodon is abbrevi- 1998; Bair, 2011). ated posterior to the sella turcica, whereas Discussion. Paleoheterodon tiheni was the same region is elongate in Paleohet- originally described on the basis of three erodon. precloacal vertebrae from the Barstovian Morphology of vertebrae and cranial ele- Nordern Bridge Quarry of Nebraska (Hol- ments referred to Paleoheterodon is con- man, 1964). Holman (1964:633) stated sistent with both Heterodon and Farancia “The vertebrae of Paleoheterodon are (e.g., Cundall and Rossman, 1984). There undoubtedly closer to Heterodon than to are four possibilities for the identity of the any other North American genus” but did taxon: 1) it is sister-taxon to Heterodon; 2) provide any character evidence in support it is sister taxon to Farancia; 3) it is sister and did not make any taxonomic compari- taxon to Heterodon+Farancia; and 4) sons in the description of the holotype. UNSM 46504 is a chimera of multiple taxa. Holman (2000) noted that vertebral mor- The possibility that cranial elements phology of extant Heterodon differs from referred to Paleoheterodon tiheni repre- closely related dipsadine Farancia only in sent multiple taxa is supported by the possessing a more depressed neural arch taphonomy of the Myers Farm site. Contra and a less anterorposteriorly undercut Holman (1977) there is almost no articula- neural spine; however, there is no appre- tion or association of microvertebrate ciable difference the amount of undercut- remains from the locality. Among squa- ting between the two taxa as illustrated by mates, only two partial snake precloacal Holman (2000). Both Heterodon and skeletons were preserved in articulation Farancia do possess comparatively flat- and direct association. P. tiheni cranial tened and depressed neural arches. specimens show damage consistent with Whether this character is useful for recog- transport, and the possibility that associa- nizing Dipsadinae or constituent subclades tion of elements is a postmortem assem- will require additional taxonomic sampling. blage of multiple individual animals. Holman (1977) described a partial skull Additionally, isolated snake cranial ele- and associated vertebrae from the late ments of similar sizes to P. tiheni cranial Barstovian Myers Farm locality of southern specimens have been recovered from the Nebraska as Paleoheterodon tiheni, unit- locality (JJH pers. obs.), and the absence ing the taxon with Heterodon based on of articulation between any of the elements vertebral similarities but noting very differ- described by Holman (1977, 2000) limits ent cranial morphologies. Holman (2000) the ability to unambiguous assign the noted that vertebral morphology of Paleo- remains to a single individual or taxon. heterodon differed from Heterodon in hav- Because of this, we restrict the elements ing a less depressed neural arch, which, assigned to UNSM 46504 to only calibrate as previously noted, is the condition in the most exclusive clade including Faran- Farancia. cia and Heterodon to the exclusion of Cranial elements referred to Paleohetero- (Nothopsis+Pseudoboa). don tiheni do show several similarities to The oldest unambiguous record of Hetero- extant Heterodon, contra Holman (1977, don is H. plionasicus from the middle Plio- 2000). The distal quadrate is narrow and cene Fox Canyon Fauna of Kansas is recurved in both taxa and the suprastape- represented by a maxilla that is anatomical dial crest is similarly well-developed, and identical to H. nasicus (Peters, 1953; Hol- the compound bone is similarly narrow and man, 2000).

10 PALAEO-ELECTRONICA.ORG

(10) Pantherophis+Pituophis. UNSM 125457 calibrates the Panth- erophis+Pituophis divergence, regardless Node Calibrated. Divergence between the of the identities of younger Pantherophis/ extant genera Pantherophis and Pituophis. Elaphe records. The oldest reports of Pitu- Fossil Taxon. Pantherophis. ophis are based on four precloacal verte- Specimen. UNSM 125457, complete, brae from the late Miocene (Hemphillian) articulated skull and anterior ~ 30 of pre- of Nebraska (Parmley and Holman, cloacal vertebral column. 1995:84). Assignment to Pituophis was Additional Materials. None. based on ambiguous vertebral morphology Phylogenetic Justification. Assignment (e.g., “neural spines high; neural arches to Pantherophis is based on a premaxilla vaulted”…) and a differential comparison with thin, dorsomedially angled maxillary with Pantherophis obsoleta. This identifica- processes, a blunt, rounded anterior mar- tion additionally appears to include the dis- gin, and laterally expanded ascending pro- tribution of extant Pituophis, which cesses forming a keyhole shape in anterior potentially introduces circularity in identifi- view. cations and analysis of faunal histories Minimum Age. 11.93 Ma (Tucker et al., (see Bell et al., 2010). 2014). Maximum Age. Indeterminate. DISCUSSION Age Justification. USNM 125457 was encased in a local ash deposit that is geo- Other Possible Fossil Calibrations chemically matched with the Ibex Hollow The Neogene and Quaternary fossil record of Tuff, radiometrically dated to 11.93 Ma colubrids includes several taxa described by cra- (Tucker et al., 2014). nial remains that have the potential to calibrate Discussion. USNM 125457 is a complete, divergence timings of extant taxa, but are problem- slightly crushed and disarticulated skull of atic with respect to systematics or anatomical inter- a colubrine snake. It possesses homodont pretations. Malpolon mynarskii was described on maxillary dentition, a sharp, distinct lateral the basis of a partial braincase from the late Plio- crest of the quadrate, and pterygoid denti- cene of Spain and was assigned to the genus on tion terminating well anterior to the quad- the basis of: “considerable posterior expansion of rate ramus. Articulations of skull roofing the parietal, a very acute angle between the pari- elements, margins of the nasals, and mor- etal crests throughout the bone, relatively very phology of the parabasisphenoid are iden- short basisphenoid portion of basiparasphenoid, tical to extant Pantherophis, and the lateral ventral expansion of the middle of the basisphe- expansion of the premaxillary ascending noid, elongation of the vertebrae, a thin and sharp process is uniquely shared between haemal keel, and straight posterior margins of the USNM 125457 and extant Pantherophis neural arch“ (Szyndlar, 1988:693). However, Szyn- species. dlar (1988) noted other anatomical similarities with Holman (1982) described a well-preserved Elaphe s.l. and Coluber s.l. Natrix longivertebrata skeleton from the latest Miocene Santee has been described on the basis of vertebrae and Local Fauna as Elaphe vulpina, and pro- cranial elements from the middle Miocene through vided a definition of the species on the Pliocene of western and central Europe (Szyndlar, basis maxillary and dentary tooth counts, 1984; Rage and Szyndlar, 1986; Szyndlar, 2012). ectopterygoid shape, and quadrate mor- Referral of N. longivertebrata to Natricinae is phology; however, none of these charac- based on vertebral morphology (Szyndlar, 1984), ters is apomorphic with respect to other and no unambiguous apomorphies nesting the Pantherophis species (e.g. P. obsoleta). taxon within extant natricine taxa have been pro- Elaphe buisi from the early Pliocene of vided. Oklahoma was described on the basis of Hierophis viridiflavus has been described as cranial remains (Holman, 1973), but the Coluber robertmertensi and Coluber viridiflavus interrelationships of the taxon to Boger- from multiple late Pliocene and Pleistocene Euro- tophis relative to Pantherophis are unde- pean localities (e.g., Mlynarski, 1964; Szyndlar, termined (Holman, 2000), and the taxon is 1984; Ivanov, 1995; Szyndlar, 2012). A single char- currently uninformative with respect to acter, a strongly posteriorly inclined anterior border divergence timings.

11 HEAD, MAHLOW, & MÜLLER: CAENOPHIDIAN CALIBRATIONS

of the vomerine process of the palatine, has been Due to the lack of information on vertebral mor- used to refer a specimen to H. viridiflavus (Szynd- phology in extant coral snakes, it is currently not lar, 1984); however, most of the described record possible to calibrate divergence timings with this for the species consists of vertebrae or other cra- undoubtedly important fossil record. nial elements. As a result, we do not formally Comparisons with Previous Fossil Calibrations include the taxon as a calibration point, but recog- for Caenophidians nize its potential utility following reassessment and phylogenetic analysis. Fossil calibrations have been applied to Two fossil genera based partially on cranial molecular phylogenetic analyses of most caeno- remains have the potential for constraining inclu- phidian clades, with little consensus on particular sive colubroid clades. Proptychophis achoris from fossils. Noonan and Chippindale (2006) used the the late Miocene of California includes a right max- fossil record of nigerophiid snakes to calibrate a illa possessing a unique combination of dental Paleogene divergence for Acrochordus. This cali- characters (Whistler and Wright, 1989), and Dry- bration is highly problematic because the fossil inoides oxyrhachis from the middle Miocene of record of nigerophiids extends into the Cretaceous Montana includes a partial skull roof and suspen- and because there is no evidence to support sorium (Auffenberg et al., 1958). Determination of monophlyly of Acrochordus and Nigerophiidae the phylogenetic relationships of these taxa will (see Sanders et al., 2010 for additional discus- very likely be important for understanding the evo- sion). Sanders et al. (2010) calibrated divergence lution of modern North American colubrids. timings for Acrochordus species as well as single- The published fossil record of coral snakes ton representatives of Colubridae and Elapidae consists of specimens from the Neogene and Qua- and two viperids based on the Acrochordus fossil ternary of North America and Europe. All have record described here and the early Miocene been assigned to Micrurus (Holman, 1977; Rage viperid and elapid records of Kuch et al. (2006). and Holman, 1984; Holman, 2000; Ivanov, 2000; Lukoschek et al. (2012) iteratively used different Szyndlar, 2009; Ivanov and Böhme, 2011; Venczel, calibrations ranging from 34-80 Ma to calibrate the 2011). Holman (1977) and Rage and Holman divergence of Acrochordus based on correct ages (1984) distinguish Micrurus gallicus from the Asta- of nigerophiids and early records of colubroids. racien of France and Micrurus sp. indet. from the Wüster et al. (2008) employed similar records Barstovian of Nebraska from Micruroides on the to those described here to minimally calibrate the basis of relatively taller neural spines in extant divergence of Eurasian viperines, but used a Micrurus and fossil specimens. Vertebral morphol- reported record of late Miocene Sistrurus (Parmley ogy cannot distinguish Micrurus from Sinomicrurus and Holman, 2007) that we do not recognize due to (Holman, 1977; Dowling and Duellman, 1978; absence of character support for assignment Roze, 1996; Ikeda, 2007), and the records of M. beyond Viperidae. Wüster et al. (2007, 2008), and gallicus and North American indeterminate species Kelly et al. (2009) followed the interpretation of records cannot be unambiguously assigned to Naja romani as a member of the Asian Naja clade genus. (Szyndlar and Rage, 1990) to calibrate the diver- Vertebral anatomy of “Elapidae gen. et sp. gence of Asian and African species. Conversely indet.” (Ivanov, 2002) from the Merkur-North local- this analysis restricts calibrations of N. romani to ity (early Miocene, MN3) of the Czech Republic is only the Naja total clade (see also Lukoschek et anatomically most similar to Micruroides and Lep- al., 2012). tomicrurus in possessing an extremely short neural Fossil calibrations for Hydrophiinae have pri- spine (Holman, 1977; Roze, 1996); however, verte- marily employed an early Miocene record referred bral morphologies for Maticora and Calliophis, to Laticauda by Scanlon et al. (2003) (Wüster et which are either considered the sister taxon to al., 2007). Both the age and identity of the record Sinomicrurus+(Micrurus + Micruroides) in the case have been revised (see Sanders and Lee, 2008 for of Maticora, or resolved as the sister taxon to all discussion), and our recommended use of Incon- other elapids in the case of Calliophis (Pyron et al., gruelaps as the minimum calibration for Laticauda 2013a, b), are undocumented. If morphologies for and Oxyuraninae is temporally consistent with the these taxa are indistinguishable from Sinomicru- divergence estimated by Sanders and Lee (2008) rus, Micrurus, and Micruroides, then the fossil using other dates. records described here may only minimally con- Calibrations for Colubroidea and Colubridae strain the divergence of crown Elapidae (Figure 1). are highly divergent (e.g., Wüster et al., 2007;

12 PALAEO-ELECTRONICA.ORG

FIGURE 1. Phylogeny of Caenophidia from Pyron et al. (2013a) temporally calibrated on minimum ages reported here. Taxon names in grey have not been described in the fossil record. Taxon names in black have been described from fossils. See Holman (2000) and Szyndlar (2012) for records. Taxa labeled with two identifiers represent the most inclusive clades subtended by those identifiers following Pyron et al. (2013a).

13 HEAD, MAHLOW, & MÜLLER: CAENOPHIDIAN CALIBRATIONS

Alfaro et al. 2008; Lukoschek et al., 2012), and rely cene and consists of elapoid remains (Scanlon et on reports of colubroids as early as Cenomanian al., 2003 after Woodhead et al., 2016). (Rage and Werner, 1999, but see Head et al., Among colubroid subclades, the temporal and 2005; Head, 2015; this study) to the first occur- geographic origins of Elapoidea and Viperidae are rence of Coluber cadurci (Lukoschek et al., 2012). most poorly understood. The high diversity of Pyron and Burbrink (2012) employ the same cali- Elapoidea, as well as endemicity of many sub- bration as advocated here for Colubroidea, the clades, in Africa is suggestive of an African origin Paleogene taxon Procerophis. They calibrate the for the clade, and the oldest fossils referred to Ela- stem-group age of Colubridae using the Oligocene pidae are from the late Oligocene of Africa (McCa- taxon Texasophis. The identity of Texasophis as a rtney et al., 2014). However, an African origin member of the Colubridae+Elapoidea crown has requires either an early Paleogene immigration into not been determined by unambiguous apomor- Africa with subsequent isolation or a Gondwanan phies, however, and we recommend the slightly origin of the clade, which would require an Early younger Coluber cadurci as the calibration of that Cretaceous divergence from Colubridae. This sec- clade. tion scenario is highly unlikely given everything that is known about the fossil record of caenophidians, Biogeographic Histories Inferred from the the fossil records of “henophidian” sister taxa, and Fossil Record rates of molecular evolution. A direct reading of the of Caenophidia fossil The origin and earliest evolution of Viperidae record indicates a latest Late Cretaceous origin is unknown in the fossil record. Viperids first likely in Gondwanan landmasses based on African appear in the early Miocene of Europe and then and South American russellophiids (Rage and the late early Miocene of North America, Asia, and Werner, 1999; Rage, 2008) with the oldest colu- Africa (Szyndlar and Rage, 1999). Immigration into broids occurring in continental sediments of the South America occurred by the middle Miocene Cambray Formation of northern India by the early (Albino and Montalvo, 2006). Despite the distinc- Eocene (Rage et al., 2008). Whether or not the tive morphology of both cranial and axial osteology Cambray colubroid record represents a Gondwa- in viperids, there is no fossil evidence of the clade nan fauna subsequently docked with Asia or an in the Paleogene. The sister-taxon relationships Asian fauna dispersing into India is indeterminate with Colubridae+Elapoidea requires at least a mid- due to the Laurasian composition of the local mam- Paleogene divergence of the viperid lineage, and mal faunas (Rana et al., 2008; Rose et al., 2008) the absence of identifiable viperids from approxi- and early Paleogene records of European russello- mately-aged sediments in Europe, North America, phiids (Rage, 1976). Unambiguous pan-colubroids and North Africa suggests that the evolution of the disperse across Europe and Asia and into North viperid crown clade and its diagnostic skeletal mor- America and Africa by the late Eocene (Rage et al., phology may have been a comparatively recent 1992; Parmley and Holman, 2003; Head et al., event relative to colubrids and elapoids. 2005; McCartney and Seiffert, 2015). Colubroids For caenophidians, as well as other squa- anatomically consistent with the crown clade of mates, the last occurrence of archaic taxa and the Colubridae+Elapoidea appear in North America first occurrence of specimens referable to extant and Europe during the early to middle Oligocene taxa is during the Miocene for the majority of docu- (Holman, 1999; Szyndlar, 2012), and appear in mented clades. Whether the timing of moderniza- Sub-Saharan Africa by the late Oligocene (McCart- tion in squamate faunas results from climatic ney et al., 2014). changes from the Paleogene world, biotic changes Dispersal of caenophidians into South Amer- in ecosystem trophic structures (Rabb and Marx, ica from North America and Australia from Asia 1973; Parmley and Holman, 1995), or the evolution occurred during the Neogene. Colubroid fossils are of highly toxic venoms (e.g, Savitzky, 1980), present in South America from the middle Miocene remains to be determined, but will require combin- on (Hoffstetter and Rage, 1977; Albino, 1996; ing fossil, sedimentological, and molecular data in Albino and Montalvo, 2006; Head et al., 2006; a comprehensive study. Albino and Brizuela, 2014), consistent with an early to middle Miocene immigration conduit between ACKNOWLEDGEMENTS Central and South America, as evidenced by other For discussion and encouragement, we thank snake taxa (Head et al., 2012). The first occur- J. Parham and D. Ksepka. We thank C. Bell for rence of colubroids in Australia is late early Mio- access to obscure literature. This research was

14 PALAEO-ELECTRONICA.ORG funded by by the Deutsche Forschungsgemein- Barry, J.C., Morgan, M.E., Flynn, L.J., Pilbeam, D., Beh- schaft (MU 1760/4-1; to JM and JJH). JJH was rensmeyer, A.K., Raza, S.M., Khan, I.A., Badgley, C., additionally funded by National Science Founda- Hicks, J., and Kelley, J. 2002. Faunal and environ- tion grant EAR-1338028. mental change in the Late Miocene Siwaliks of North- ern Pakistan. Paleobiology, 28(suppl. To 2):1-71. Bell, C.J., Gauthier, J.A., and Bever, G.S. 2010. Covert REFERENCES biases, circularity, and apomorphies: A critical look at Agustí, J., Cabrera, L., Garcés, M., Krijgsman, W., Oms, the North American Quaternary herpetofaunal stabil- O. and Parés, J.M. 2001. A calibrated mammal scale ity hypothesis. Quaternary International, 217:30-36. for the Neogene of Western Europe. State of the art. Bell, C.J., Head, J.J., and Mead, J.I. 2004. Synopsis of Earth-Science Reviews, 52:247-260. the herpetofauna from Porcupine Cave, p. 117-126. Albino, A.M. 1996. Snakes from the Miocene of Patago- In Barnosky, A.D. (ed.), Biodiversity Response to Cli- nia (Argentina) Part II: The Colubroidea. Neues Jahr- mate Change in the Middle Pleistocene. The Porcu- buch fur Geologie und Palaontologie-Abhandlungen, pine Cave Fauna from Colorado. Berkeley: 200:353-360. University of California Press. Albino, A.M. and Brizuela, S. 2014. An overview of the Bellairs, A.A. and Underwood, G. 1951. The origin of South American fossil squamates. The Anatomical snakes. Biological Reviews, 26:193-237. Record, 297:349-368. Blain, H.A., Agustí, J., López-García, J.M., Haddoumi, Albino, A.M. and Montalvo, C.I. 2006. Snakes from the H., Aouraghe, H., Hammouti, K.E., Pérez-González, Cerro Azul Formation (Upper Miocene), central A., Chacón, M.G., and Sala, R. 2013. Amphibians Argentina, with a review of fossil viperids from South and squamate reptiles from the late Miocene America. Journal of Vertebrate Paleontology, 26:581- (Vallesian) of eastern Morocco (Guefaït-1, Jerada 587. Province). Journal of Vertebrate Paleontology, Alfaro, M.E., Karns, D.R., Voris, H.K., Brock, C.D., and 33:804-816. Stuart, B.L. 2008. Phylogeny, evolutionary history, Bogert, C.M. 1943. Dentitional phenomena in cobras and biogeography of Oriental–Australian rear-fanged and other elapids, with notes on adaptive modifica- water snakes (Colubroidea: Homalopsidae) inferred tions of fangs. Bulletin of the American Museum of from mitochondrial and nuclear DNA sequences. Natural History, 81:285-360. Molecular Phylogenetics and Evolution, 46:576-593. Burbrink, F.T. 2002. Phylogeographic analysis of the Auffenberg, W., Mook, C.C., and Williams, C.S. 1958. A cornsnake (Elaphe guttata) complex as inferred from new genus of colubrid snake from the Upper Mio- maximum likelihood and Bayesian analyses. Molecu- cene of North America. American Museum Novi- lar Phylogenetics and Evolution, 25:465-476. tates,1874:1-16. Burbrink, F.T., Fontanella, F., Pyron, R.A., Guiher, T.J., Bachmayer, F. and Szyndlar, Z., 1985. Ophidians (Rep- and Jimenez, C. 2008. Phylogeography across a tilia: Serpentes) from the Kohfidisch fissures of Bur- continent: the evolutionary and demographic history genland, Austria. Annalen des Naturhistorischen of the North American racer (Serpentes: Colubridae: Museums in Wien, 87:79-100. Coluber constrictor). Molecular Phylogenetics and Bachmayer, F. and Szyndlar, Z. 1987. A second contribu- Evolution, 47:274-288. tion to the ophidian fauna (Reptilia: Serpentes) of Burbrink, F.T. and Lawson, R. 2007. How and when did Kohfidisch, Austria. Annalen des Naturhistorischen Old World ratsnakes disperse into the New World? Museums in Wien, 88:25-39. Molecular Phylogenetics and Evolution, 43:173-189. Bailon, S. 1989. Les amphibiens et les reptiles du Burbrink, F.T., Lawson, R., and Slowinski, J.B. 2000. Pliocène supérieur de Balaruc II (Hérault, France). Mitochondrial DNA phylogeography of the polytypic Palaeovertebrata, 19:7-28. North American rat snake (Elaphe obsoleta): a cri- Bair, A.R. 2011. Description of a new species of the tique of the subspecies concept. Evolution, 54:2107- North American archaic pika Hesperolagomys (Lago- 2118. morpha: Ochotonidae) from the middle Miocene Burbrink, F.T. and Pyron, R.A. 2010. How does ecologi- (Barstovian) of Nebraska and reassessment of the cal opportunity influence rates of speciation, extinc- genus Hesperolagomys. Palaeontologia Electronica, tion, and morphological diversification in New World Vol. 14:6A:49p;?http://palaeo-electronica.org/2011_1/ ratsnakes (tribe Lampropeltini)?. Evolution, 64:934- 202/index.html 943. Bajpai, S., Kapur, V.V., Das, D.P., Tiwari, B.N., Sarava- Carmona, R., Alba, D.M., Delfino, M., Robles, J.M., Rot- nan, N., and Sharma, R., 2005. Early Eocene land gers, C., Mengual, J.V.B., Balaguer, J., Galindo, J., mammals from the Vastan Lignite Mine, District Surat and Moyà-Solà, S. 2010. Snake fossil remains from (Gujarat), western India. Journal of the Palaeontolog- the Middle Miocene stratigraphic series of Abocador ical Society of India, 50:101-113. de Can Mata (els Hostalets de Pierola, Catalonia, Spain). Cidaris, 30:77-83.

15 HEAD, MAHLOW, & MÜLLER: CAENOPHIDIAN CALIBRATIONS

Cernansky, A., Rage, J.-C., and Klembara, J. 2014. The Head, J.J. and Bell, C.J. 2008. Snakes from Lemud- early Miocene squamates of Amöneburg (Germany): ong'o, Kenya Rift Valley. Kirtlandia, 56:177-179. the first stages of modern squamates in Europe. Head, J.J., Holroyd, P.A., Hutchison, J.H., and Ciochon, Journal of Systematic Palaeontology, http:// R.L. 2005. First report of snakes (Serpentes) from dx.doi.org/10.1080/14772019.2014.897266 the late middle Eocene Pondaung Formation, Myan- Cundall, D. and Rossman, D.A. 1984. Quantitative com- mar. Journal of Vertebrate Paleontology, 25:246-250. parisons of skull form in the colubrid snake genera Head, J.J., Mohabey, D.M., and Wilson, J A. 2007. Acro- Farancia and Pseudoeryx. Herpetologica, 40:388- chordus Hornstedt (Serpentes, Caenophidia) from 405. the Miocene of Gujarat, Western India: temporal con- Daxner-Höck, G., Milas-Tempfer, P.M., Gölich, U.B., Hut- straints on dispersal of a derived snake. Journal of tunen, K., Kazàr, E., Nagel, D., Roessner, G.E., Vertebrate Paleontology, 27:720-723. Schultz, O., and Ziegler, R. 2004. Marine and terres- Head, J.J., Rincon, A., Suarez, C., Montes C., and Jara- trial vertebrates from the middle Miocene of Grund millo, C. 2012. Evidence for American interchange (lower Austria). Geologica Carpathica, 55:1-7. during the earliest Neogene: Boa from the Miocene Dowling, H.G., and Duellman, W.E. 1978. Systematic of Panama. Journal of Vertebrate Paleontology, herpetology: a synopsis offamilies and higher catego- 32:1328-1334. ries. HISS Publications, New York. Head, J.J., Sánchez-Villagra, M.R., and Aguilera, O. Flynn, L.J., Pilbeam, D., Jacobs, L.L., Barry, J.C., Beh- 2006. Fossil snakes from the Neogene of Venezuela rensmeyer, A.K., and Kappelman, J.W. 1990. The (Falcón State). Journal of Systematic Palaeontology, Siwaliks of Pakistan: time and faunas in a Miocene 4:233-240. terrestrial setting. The Journal of Geology, 98:589- Hedges, S.B., Couloux, A., and Vidal, N. 2009. Molecu- 604. lar phylogeny, classification, and biogeography of Fry, B.G., Scheib, H., van der Weerd, L., Young, B., West Indian racer snakes of the Tribe Alsophiini McNaughtan, J., Ramjan, S. F.R., Vidal, N., Poel- (Squamata, Dipsadidae, Xenodontinae). Zootaxa, mann, R.E., and Norman, J.A. 2008. Evolution of an 2067:1-28. arsenal structural and functional diversification of the Hilgen, F.J., Lourens, L.J., and Van Dam, J.A. 2012. The venom system in the advanced snakes (Caeno- Neogene Period, p. 923-978. In Gradstein, F. Ogg, phidia). Molecular & Cellular Proteomics, 7:215-246. J.G., Schmitz, M., and Ogg, G (eds.), The Geologic Fry, B.G., Wüster, W., Kini, R.M., Brusic, V., Khan, A., Time Scale 2012. Elsevier, Amsterdam. Venkataraman, D., and Rooney, A.P. 2003. Molecular Hoffstetter, R. 1939. Contribution a l’étude des Elapidae evolution and phylogeny of elapid snake venom actuels et fossiles et de l’ostéologie des ophidians. three-finger toxins. Journal of Molecular Evolution, Archives du Muséum d'Histoire Naturelle de Lyon, 57:110-129. 15:1-78. Göhlich, U.B. and Mourer‐Chauviré, C. 2005. Revision of Hoffstetter, R. 1964. Les serpents du Néogène du Paki- the phasianids (Aves: Galliformes) from the lower stan (couches des Siwaliks). Bulletin de la Société Miocene of Saint‐Gérand‐le‐Puy (Allier, France). Géologique de France, Série 7, 6:467-474. Palaeontology, 48:1331-1350. Hoffstetter, R. and Gasc, J.-P. 1969. Vertebrae and ribs Gómez, R.O., Báez, A.M., and Rougier, G.W. 2008. An of modern reptiles, p. 201-310. In Gans, C. (ed.), anilioid snake from the Upper Cretaceous of northern Biology of the Reptilia, Volume 1: Morphology. Aca- Patagonia. Cretaceous Research, 29:481-488. demic Press, London. Gravlund, P. 2001. Radiation within the advanced Hoffstetter, R. and Rage J.-C. 1977. Le gisement de snakes (Caenophidia) with special emphasis on Afri- vertébrés Miocènes de La Venta (Colombie) et sa can opistoglyph colubrids, based on mitochondrial faune de serpents. Annales de Paléontologie, sequence data. Biological Journal of the Linnean 63:161-190. Society, 72:99-114. Holman, J.A. 1973. A new Pliocene snake, genus Head, J.J. 2002. Snake paleontology of the Siwalik Elaphe, from Oklahoma. Copeia, 1973:574-580. Group (Miocene) of Pakistan: Correlation of a rich Holman, J.A. 1977. Upper Miocene snakes (Reptilia, fossil record to environmental histories. Ph.D. disser- Serpentes) from Southeastern Nebraska. Journal of tation, Southern Methodist University, Dallas, TX, Herpetology, 11:323-335. USA. Holman, J.A., 1982. A fossil snake (Elaphe vulpina) from Head, J.J. 2005. Snakes of the Siwalik Group (Miocene a Pliocene ash bed in Nebraska. Transactions of the of Pakistan): systematics and relationship to environ- Nebraska Academy of Science, 10:37-42. mental change. Palaeontologia Electronica, Holman, J.A. 1999. Early Oligocene (Whitneyan) snakes 8(1):16A. from Florida (USA), the second oldest colubrid Head, J.J. 2015. Fossil calibration dates for molecular snakes in the North America. Acta Zoologica Cra- phylogenetic analysis of snakes 1: Serpentes, Alethi- coviensia, 42:447-454. nophidia, Boidae, Pythonidae. Palaeontologia Elec- Holman, J.A. 2000. The fossil snakes of North America. tronica, 18:1-17. Indiana University Press, Indianapolis.

16 PALAEO-ELECTRONICA.ORG

Ikeda, T. 2007. A comparative morphological study of the LaDuke, T.C., Krause, D.W., Scanlon, J.D., and Kley, vertebrae of snakes occurring in Japan and adjacent N.J. 2010. A Late Cretaceous (Maastrichtian) snake regions. Current Herpetology, 26:13-34. assemblage from the Maevarano Formation, Maha- Ivanov, M. 1995. Pleistocene Reptiles at the Locality of janga Basin, Madagascar. Journal of Vertebrate the Stránská Skála Hill, p. 93-109. In Musil, R. (ed.), Paleontology, 30:109-138. Stránská Skála Hill. Excavation of open-air sedi- Lawson, R., Slowinski, J.B., Crother, B.I., and Burbrink, ments 1964-1972. Moravian Museum, Brno, Anthro- F.T. 2005. Phylogeny of the Colubroidea (Serpentes): pos series, 26. new evidence from mitochondrial and nuclear genes. Ivanov, M. 1999. The first European pit viper from the Molecular Phylogenetics and Evolution, 37:581-601. Miocene of Ukraine. Acta Palaeontologica Polonica, Lukoschek, V. and Keogh, J.S. 2006. Molecular phylog- 44:327-334. eny of sea snakes reveals a rapidly diverged adap- Ivanov, M. 2000. Snakes of the lower/middle Miocene tive radiation. Biological Journal of the Linnean transition at Vieux Collonges (Rhône, France), with Society, 89:523-539. comments on the colonisation of western Europe by Lukoschek, V., Keogh, J.S., and Avise, J.C. 2012. Evalu- colubroids. Geodiversitas, 22:559-588. ating fossil calibrations for dating phylogenies in light Ivanov, M. 2002. The oldest known Miocene snake fauna of rates of molecular evolution: a comparison of three from Central Europe: Merkur−North locality, Czech approaches. Systematic Biology, 61:22-43. Republic. Acta Palaeontologica Polonica, 47:513- McCartney, J.A. and Seiffert, E.R. 2015. A late Eocene 534. snake fauna from the Fayum Depression, Egypt. Ivanov, M. and Böhme, M. 2011. Snakes from Gries- Journal of Vertebrate Paleontology, p.e1029580. beckerzell (Langhian, Early Badenian), North Alpine McCartney, J.A., Stevens, N.J., and O’Connor. P.M. Foreland Basin (Germany), with comments on the 2014. The Earliest Colubroid-Dominated Snake evolution of snake faunas in Central Europe during Fauna from Africa: Perspectives from the Late Oligo- the Miocene Climatic Optimum. Geodiversitas, cene Nsungwe Formation of Southwestern Tanzania. 33:411-449. PLoS ONE 9(3): e90415. doi:10.1371/jour- Janis, C.M., Scott, K.M., and Jacobs, L.L. 1998. Evolu- nal.pone.0090415 tion of Tertiary Mammals of North America: Terres- McDiarmid, R.W., Campbell, J.A., and Touré, T’s.A. trial carnivores, ungulates, and ungulatelike 1999. Snake Species of the World. A Taxonomic and mammals (Vol. 1). Cambridge University Press. Geographic Reference, Volume 1. The Herpetolo- Kelly, C.M., Barker, N.P., and Villet, M.H. 2003. Phyloge- gists’ League. Washington. netics of advanced snakes (Caenophidia) based on McDowell, S.B. 1970. On the status and relationships of four mitochondrial genes. Systematic Biology, the Solomon Island elapid snakes. Journal of Zool- 52:439-459. ogy, 161:145-190. Kelly, C.M., Barker, N.P., Villet, M.H., and Broadley, D. G. Meylan, P.A. 1987. Fossil snakes from Laetoli, p. 78-82. 2009. Phylogeny, biogeography and classification of In Leakey, M.D. and Harris, J.M. (eds.), The Pliocene the snake superfamily Elapoidea: a rapid radiation in Site of Laetoli, northern Tanzania. Oxford University the late Eocene. Cladistics, 25:38-63. Press. Keogh, J.S. 1998. Molecular phylogeny of elapid snakes Miklas-Tempfer, P.M. 2002. The Miocene Herpetofaunas and a consideration of their biogeographic history. of Grund (Caudata; Chelonii, Sauria, Serpentes) and Biological Journal of the Linnean Society, 63:177- Mühlbach am Manhartsberg (Chelonii, Sauria, 203. Amphisbaenia, Serpentes), Lower Austria. Annalen Keogh, S.J., Scott, I.A., Fitzgerald, M., and Shine, R. des Naturhistorischen Museums in Wien, 104:195- 2003. Molecular phylogeny of the Australian venom- 235. ous snake genus Hoplocephalus (Serpentes, Elapi- Młynarski, M. 1964. Die jungpliozäne Reptilienfauna von dae) and conservation genetics of the threatened H. Rebielice Królewskie, Polen. Senckenbergiana Bio- stephensii. Conservation Genetics, 4:57-65. logica, 45:325-347. Kuch, U., Müller, J., Mödden, C., and Mebs, D. 2006. Mohabey, D.M., Head, J.J., and Wilson, J.A. 2011. A new Snake fangs from the Lower Miocene of Germany: species of the snake Madtsoia from the Upper Creta- evolutionary stability of perfect weapons. Naturwis- ceous of India and its paleobiogeographic implica- senschaften, 93:84-87. tions. Journal of Vertebrate Paleontology, 31:588- LaDuke, T.C. 1991a. Morphometric variability of the pre- 595. caudal vertebrae of Thamnophis sirtalis sirtalis (Ser- Murphy, J.C., Mumpuni, and Sanders, K.L. 2011. First pentes: Colubridae), and implications for molecular evidence for the phylogenetic placement interpretation of the fossil record. Unpubl. Ph.D. of the enigmatic snake genus Brachyorrhos (Ser- diss., City Univ. of New York, New York. pentes: Caenophidia). Molecular Phylogenetics and LaDuke, T.C. 1991b. The fossil snakes of Pit 91, Rancho Evolution, 61:953-957. La Brea, California. Natural History Museum of Los Angeles County Contributions in Science, 424:1-28.

17 HEAD, MAHLOW, & MÜLLER: CAENOPHIDIAN CALIBRATIONS

Myers, T., Crosby, K., Archer, M., and Tyler, M. 2001. Pyron, R.A. and Burbrink, F.T. 2009a. Neogene diversifi- The Encore local Fauna, a late Miocene assemblage cation and taxonomic stability in the snake tribe Lam- from Riversleigh, northwestern Queensland. Mem- propeltini (Serpentes: Colubridae). Molecular oirs of the Association of Australasian Palaeontolo- Phylogenetics and Evolution, 52:524-529. gists, 25:147-154. Pyron, R.A. and Burbrink, F.T. 2009b. Can the tropical Nagy, Z.T., Joger, U., Wink, M., Glaw, F., and Vences, M. conservatism hypothesis explain temperate species 2003. Multiple colonization of Madagascar and richness patterns? An inverse latitudinal biodiversity Socotra by colubrid snakes: evidence from nuclear gradient in the New World snake tribe Lampropeltini. and mitochondrial gene phylogenies. Proceedings of Global Ecology and Biogeography, 18:406-415. the Royal Society of London B, 270:2613-2621. Pyron, R.A. and Burbrink, F.T. 2009c. Systematics of the Noonan, B.P. and Chippindale, P.T. 2006. Vicariant origin Common Kingsnake (Lampropeltis getula; Ser- of Malagasy reptiles supports Late Cretaceous Ant- pentes: Colubridae) and the burden of heritage in arctic land bridge. The American Naturalist, 168:730- taxonomy. Zootaxa, 2241:22-32. 741. Pyron, R.A. and Burbrink, F.T. 2012. Extinction, ecologi- Ogg, J.G., Hinnov, L.A., and Huang, C. 2012. Creta- cal opportunity, and the origins of global snake diver- ceous, p. 793-854. In Gradstein, F. Ogg, J.G., sity. Evolution, 66:163-178. Schmitz, M., and Ogg, G. (eds.), The Geologic Time Pyron, R.A., Burbrink, F.T., and Wiens, J.J. 2013a. A Scale 2012. Elsevier, Amsterdam. phylogeny and revised classification of Squamata, Parham, J.F., Donoghue, P.C.J., Bell, C.J., Calway, T.D., including 4161 species of lizards and snakes. BMC Head, J.J., Holroyd, P.A., Inoue, J.G., Irmis, R.B., Evolutionary Biology, 13:93. Joyce, W.G., Ksepka, D.T., Patańe, J.S.L.N., Smith, Pyron, R.A., Burbrink, F.T., Colli, G.R., De Oca, A.N.M., D., Tarver, J.E., van Tuinen, M., Yang, Z., Angielczyk, Vitt, L.J., Kuczynski, C. A., and Wiens, J.J. 2011. The K.D., Greenwood, J., Hipsley, C.A., Jacobs, L.L., phylogeny of advanced snakes (Colubroidea), with Makovicky, P.J., Müller, J., Smith, K.T., Theodor, discovery of a new subfamily and comparison of sup- J.M., Warnock, R.C.M., and Benton, M.J. 2012. Best port methods for likelihood trees. Molecular Phyloge- practices for applying paleontological data to molecu- netics and Evolution, 58:329-342. lar divergence dating analyses. Systematic Biology, Pyron, R.A., Kandambi, H.D., Hendry, C.R., Pushpamal, 61:346-359. V., Burbrink, F.T., and Somaweera, R. 2013b. Genus- Parmley, D. and Holman, J.A., 1995. Hemphillian (late level phylogeny of snakes reveals the origins of spe- Miocene) snakes from Nebraska, with comments on cies richness in Sri Lanka. Molecular Phylogenetics Arikareean through Blancan snakes of midcontinen- and Evolution, 66:969-978. tal North America. Journal of Vertebrate Paleontol- Rabb, G.B. and Marx, H. 1973. Major ecological and ogy, 15:79-95. geographic patterns in the evolution of colubroid Parmley, D. and Holman, J.A. 2003. Nebraskophis Hol- snakes. Evolution, 27:69-83. man from the Late Eocene of Georgia (USA), the old- Rage, J.-C. 1973. Fossil snakes from Olduvai, Tanzania. est known North American colubrid snake. Acta Fossil vertebrates of Africa, 3:1-6. Zoologica Cracoviensia, 46:1-8. Rage, J.-C. 1975. Un Caenophidien primitif (Reptilia, Parmley, D. and Holman, J.A. 2007. Earliest fossil record Serpentes) dans l’Eocene inferieur. Compte Rendu of a pigmy rattlesnake (Viperidae: Sistrurus Gar- Sommaire des Séances de la Société Géologique de man). Journal of Herpetology, 41:141-144. France, 2:46-47. Peters, J.A. 1953. A fossil snake of the genus Heterodon Rage, J.-C. 1976. Les squamates du Miocène de Béni from the Pliocene of Kansas. Journal of Paleontol- Mellal, Maroc. Géologie Méditerranéene, 2:57-70. ogy, 27:328-331. Rage, J.-C. 1984. Encyclopedia of Paleoherpetology, Pinou, T., Vicario, S., Marschner, M., and Caccone, A. part 11, Serpentes. Gustav Fischer Verlag, Stuttgart. 2004. Relict snakes of North America and their rela- Rage, J.-C. 2003. Squamate reptiles from the early Mio- tionships within Caenophidia, using likelihood-based cene of Arrisdrift (Namibia) p. 43- 50. In Senut, B. Bayesian methods on mitochondrial sequences. and Pickford, M. (eds.), Geology and Palaeobiology Molecular Phylogenetics and Evolution, 32:563-574. of the central and southern Namib. Vol. 2: Palaeon- Prasad, G.V.R. and Rage, J.-C. 1995. Amphibians and tology of the Orange River valley, Namibia. Memoir squamates from the Maastrichtian of Naskal, India. of the Geology Survey of Namibia (Ministry of Mines Cretaceous Research, 16:95-107. and Energy, Windhoeck),19. Pritchard, A.C., McCartney, J.A., Krause, D.W., and Kley, Rage, J.-C. 2008. Fossil snakes from the Paleocene of N.J. 2014. New snakes from the Upper Cretaceous São José de Itaboraí, Brazil. Part III. Ungaliophiinae, (Maastrichtian) Maevarano Formation, Mahajanga boiids incertae sedis, and Caenophidia. Summary, Basin, Madagascar. Journal of Vertebrate Paleontol- update and discussion of the snake fauna from the ogy, 34:1080-1093 locality Palaeovertebrata, 36:37-73. Rage, J.C. and Augé, M. 1993. Squamates from the Cai- nozoic of the western part of Europe. A review. Revue de Paléobiologie, 7:99-216.

18 PALAEO-ELECTRONICA.ORG

Rage, J.-C. and Bailon, S. 2005. Amphibians and squa- Rose, K.D., DeLeon, V.B., Missiaen, P., Rana, R.S., mate reptiles from the late early Miocene (MN 4) of Sahni, A., Singh, L., and Smith, T. 2008. Early Béon 1 (Montréal-du-Gers, southwestern France). Eocene lagomorph (Mammalia) from Western India Geodiversitas, 27:413-441. and the early diversification of Lagomorpha. Pro- Rage, J.C. and Bailon, S. 2011. Amphibia and Squa- ceedings of the Royal Society of London B, mata, p. 467-478. In Harrison, T. (ed.), Paleontology 275:1203-1208. and geology of Laetoli: Human evolution in context. Roze, J. A. 1996. Coral snakes of the Americas: Biology, Volume 2. Springer Netherlands. identification, and venoms. Krieger Publishing, Mala- Rage, J.-C., Bajpai, S., Thewissen, J.G. and Tiwari, B.N. bar, Fl. 2003. Early Eocene snakes from Kutch, Western Salih, K.A.O., Evans, D.C., Bussert, R., Klein, N., Nafi, India, with a review of the Palaeophiidae. Geodiversi- M., and Müller, J. 2015. First record of Hyposaurus tas, 25:695-716. (Dyrosauridae, Crocodyliformes) from the Upper Cre- Rage, J.-C., Buffetaut, E., Buffetaut-Tong, H., Chai- taceous Shendi Formation of Sudan. Journal of Ver- manee, Y., Ducrocq, S., Jaeger, J.J. and Suteethorn, tebrate Paleontology, e1115408. V. 1992. A colubrid snake in the late Eocene of Thai- Sanders, K.L. and Lee, M.S. 2008. Molecular evidence land: the oldest known Colubridae (Reptilia, Ser- for a rapid late-Miocene radiation of Australasian pentes). Comptes rendus de l'Académie des venomous snakes (Elapidae, Colubroidea). Molecu- sciences. Série 2, Mécanique, Physique, Chimie, lar Phylogenetics and Evolution, 46:1165-1173. Sciences de l'univers, Sciences de la Terre, Sanders, K.L., Lee, M.S.Y., Leys, R., Foster, R., and 314:1085-1089. Keogh, J.S. 2008. Molecular phylogeny and diver- Rage, J.-C. and Danilov, I.G. 2008. A new Miocene fauna gence dates for Australian elapids and sea snakes of snakes from eastern Siberia, Russia: Was the (hydrophiinae): evidence from seven genes for rapid snake fauna largely homogenous in Eurasia during evolutionary radiations. Journal of Evolutionary Biol- the Miocene?. Comptes Rendus Palevol, 7:383-390. ogy, 21:682-695. Rage, J.-C., Folie, A., Rana, R S., Singh, H., Rose, K.D. Sanders, K.L., Mumpuni, Hamidy, A., Head, J.J., and and Smith, T. 2008. A diverse snake fauna from the Gower, D.J. 2010. Phylogeny and divergence times early Eocene of Vastan Lignite Mine, Gujarat, India. of filesnakes (Acrochordus): Inferences from mor- Acta Palaeontologica Polonica, 53:391-403. phology, fossils and three molecular loci. Molecular Rage, J.-C. and Ginsburg, L. 1997. Amphibians and Phylogenetics and Evolution, 56:857-867. squamates from the early Miocene of Li Mae Long, Savitzky, A.H. 1980. The role of venom delivery strate- Thailand: The richest and most diverse herpetofauna gies in snake evolution. Evolution, 34:1194-1204. from the Cainozoic of Asia, p. 167-168. In Rocek, Z. Scanlon, J.D., Lee, M.S.Y., and Archer, M. 2003. Mid- and Hart, S. (eds.), Herpetology ’97. Ministry of Envi- Tertiary elapid snakes (Squamata, Colubroidea) from ronment of the Czech Republic, Prague. Riversleigh, northern Australia: early steps in a conti- Rage, J.-C. and Holman, J.A. 1984. Des serpents (Rep- nent-wide adaptive radiation. Geobios, 36:573-601. tilia, Squamata) de type nord-américain dans le Schrank, E. 1990. Palynology of the clastic Cretaceous Miocène Français. Évolution parallèle ou disper- sediments between Dongola and Wadi Muqaddam, sion?. Geobios, 17:89-104. northern Sudan. Berliner Geowissenschaftliche Rage, J.-C., Prasad, G.V., and Bajpai, S. 2004. Addi- Abhandlungen, Reihe A, 120:149-168. tional snakes from the uppermost Cretaceous (Maas- Schrank, E. and Awad, M.Z. 1990. Palynological evi- trichtian) of India. Cretaceous Research, 25:425-434. dence for the age and depositional environment of Rage, J.-C. and Werner, C. 1999. Mid-Cretaceous the Cretaceous Omdurman Formation in the Khar- (Cenomanian) snakes from Wadi Abu Hashim, toum area, Sudan. Berliner Geowissenschaftliche Sudan: The earliest snake assemblage. Palaeontolo- Abhandlungen, Reihe A, 120:169-182. gia Africana, 35:85-110. Sen, S. 1997. Magnetostratigraphic calibration of the Rage, J.-C. and Wouters, G. 1979. Découverte du plus European Neogene mammal chronology. Palaeoge- ancien Palaeopheidé (Reptilia, Serpentes) dans le ography, Palaeoclimatology, Palaeoecology, Maestrichtien du Maroc. Geobios, 12:293-296. 133:181-204. Rana, R.S., Kumar, K., Escarguel, G., Sahni, A., Rose, Sheil, C.A. and Grant, T. 2001. A new species of colubrid K.D., Smith, T., Singh, H., and Singh, L. 2008. An snake (Synophis) from western Colombia. Journal of ailuravine rodent from the lower Eocene Cambay Herpetology, 35:204-209. Formation at Vastan, western India, and its palaeo- Slowinski, J.B. 1994. A phylogenetic analysis of Bun- biogeographic implications. Acta Palaeontologica garus (Elapidae) based on morphological characters. Polonica, 53:1-14. Journal of Herpetology, 28:440-446. Smith, M.J. 1975. The vertebrae of 4 Australian elapid snakes (Squamata: Elapidae). Transactions of the Royal Society of South Australia, 99:71-84.

19 HEAD, MAHLOW, & MÜLLER: CAENOPHIDIAN CALIBRATIONS

Smith, M.J. 1976. Small fossil vertebrates from Victoria Szyndlar Z., Smith, R., and Rage, J.-C. 2008. A new Cave, Naracoorte, South Australia. IV. Reptiles. dwarf boa (Serpentes, Booidea, “Tropidophiidae”) Transactions of the Royal Society of South Australia, from the Early Oligocene of Belgium: a case of the 100:39-51. isolation of Western European snake faunas. Zoolog- Szyndlar, Z. 1984. Fossil snakes from Poland. Acta Zoo- ical Journal of the Linnaean Society, 152:393-406. logica Cracoviensia, 28:1-156. Tedford, R H., Albright, B. III, Barnosky, A.D., Fer- Szyndlar, Z. 1985. Ophidian fauna (Reptilia, Serpentes) rusquia-Villafranca, I., Hunt, R.M. jr., Storer, J.E., from the uppermost Miocene of Algora (Spain). Estu- Swisher, C.C. III, Voorhies, M.R., Webb, S.D., and dios Geologicos, 41:447-465. Whistler, D.P. 2004. Mammalian Biochronology of the Szyndlar, Z. 1987. Snakes from the lower Miocene local- Arikareean Through Hemphillian Interval (Late Oligo- ity of Dolnice (Czechoslovakia). Journal of Vertebrate cene Through Early Pliocene Epochs), p. 169-231. In Paleontology, 7:55-71. Woodburne, M.O. (ed.), Late Cretaceous and Ceno- Szyndlar, Z. 1988. Two new extinct species of the gen- zoic Mammals of North America: Biostratigraphy and era Malpolon and Vipera (Reptilia, Serpentes) from Geochronology. Columbia University Press, New the Pliocene of Layna (Spain). Acta Zoologica Cra- York. coviensia, 31:687-706. Tucker, S.T., Otto, R.E., Joeckel, R.M., and Voorhies, Szyndlar, Z. 1991a. A review of Neogene and Quater- M.R. 2014. The geology and paleontology of Ashfall nary snakes of central and eastern Europe. Part I: Fossil Beds, a late Miocene (Clarendonian) mass- Scolecophidia, Boidae, Colubrinae. Estudios Geolog- death assemblage, Antelope Country and adjacent icos, 47:103-126. Knox Country, Nebraska, USA. GSA Field Guides, Szyndlar, Z. 1991b. A review of Neogene and Quater- 36:1-22. nary snakes of central and eastern Europe. Part II: Vandenberghe, N., Hilgen, F.J., and Speijer, R.P. 2012. Natricinae, Elapidae, Viperidae. Estudios Geologi- The Paleogene Period, p. 855-921. In Gradstein, F., cos, 47:237-266. Ogg, J., Schmitz, M., and Ogg, G. (eds.), The Geo- Szyndlar, Z. 1992. Osteology of African cobras: prelimi- logic Time Scale 2012. Elsevier Press. nary observations, p. 425-428. In Korsós, Z. and Venczel, M. 2011. Middle-Late Miocene snakes from the Kiss, I. (eds.), Proceedings of the Sixth Ordinary Pannonian Basin. Acta Palaeontologica Romaniae, General Meeting of the Societas Europaea Herpeto- 7:343-349. logica. Hungarian Natural History Museum, Buda- Vidal, N. 2002. Colubroid systematics: evidence for an pest. early appearance of the venom apparatus followed Szyndlar, Z. 1994. Oligocene snakes of southern Ger- by extensive evolutionary tinkering. Toxin Reviews, many. Journal of Vertebrate Paleontology, 14:24-37. 21:21-41. Szyndlar, Z. 2009a. Snake fauna (Reptilia: Serpentes) Vidal, N., Delmas, A.S., David, P., Cruaud, C., Couloux, from the Early/Middle Miocene of Sandelzhausen A., and Hedges, S.B. 2007. The phylogeny and clas- and Rothenstein 13 (Germany). Paläontologische sification of caenophidian snakes inferred from seven Zeitschrift, 83:55-66. nuclear protein-coding genes. Comptes Rendus Biol- Szyndlar, Z. 2009b. The snakes (Reptilia, Serpentes) of ogies, 330:182-187. the Miocene of Portugal. Ciencias da Terra, 14. Vidal, N., Dewynter, M., and Gower, D.J. 2010. Dissect- Szyndlar, Z. 2012. Early Oligocene to Pliocene Colubri- ing the major American snake radiation: a molecular dae of Europe: a review. Bulletin de la Société phylogeny of the Dipsadidae Bonaparte (Serpentes, Géologique de France, 183:661-681. Caenophidia). Comptes Rendus Biologies, 333:48- Szyndlar, Z. and Rage, J.C. 1990. West Palearctic 55. cobras of the genus Naja (Serpentes: Elapidae): Vidal, N., Lecointre, G., Vie, J.C., and Gasc, J.P. 1999. interrelationships among extinct and extant species. What can mitochondrial gene sequences tell us Amphibia-Reptilia, 11:385-400. about intergeneric relationships of pitvipers. Kaupia, Szyndlar, Z. and Rage, J.-C. 1999. Oldest fossil vipers 8:107-112. (Serpentes: Viperidae) from the Old World. Kaupia. Wallach, V., Williams, K.L., and Boundy, J. 2014. Snakes Darmstädter Beiträge zur Naturgeschichte, 8:9-20. of the World: A catalogue of living and extinct spe- Szyndlar, Z. and Rage, J.-C. 2002. Fossil record of the cies. CRC Press. true vipers, p. 419-444. In Schuett, G.W., Höggren, Wallach, V., Wüster, W., and Broadley, D.G. 2009. In M., Douglas, M.E., and Greene, H.W. (eds.), Biology praise of subgenera: taxonomic status of cobras of of the Vipers. Eagle Mountain Publishing, Utah. the genus Naja Laurenti (Serpentes: Elapidae). Zoot- Szyndlar, Z. and Schleich, H.H. 1993. Description of Mio- axa, 2236:26-36. cene snakes from Petersbuch 2 with comments on West, R.M., Hutchison, J.H., and Munthe, J. 1991. Mio- the lower and middle Miocene ophidian faunas of cene vertebrates from the Siwalik Group, western southern Germany. Stuttgarter Beitrage zur Nepal. Journal of Vertebrate Paleontology, 11:108- Naturkunde, Series B. Geologie und Palaontologie, 129. 192:1-47.

20 PALAEO-ELECTRONICA.ORG

Whistler, D.P. and Wright, J.W. 1989. A late Miocene Wüster, W., Peppin, L., Pook, C.E., and Walker, D.E. rear-fanged colubrid snake from California with com- 2008. A nesting of vipers: phylogeny and historical ments on the phylogeny of North American snakes. biogeography of the Viperidae (Squamata: Ser- Herpetologica, 45:350-367. pentes). Molecular Phylogenetics and Evolution, Woodhead, J., Hand, S.J., Archer, M., Graham, I., Snid- 49:445-459. erman, K., Arena, D.A., Black, K.H., Godthelp, H., Zaher, H., Grazziotin, F.G., Cadle, J.E., Murphy, R.W., Creaser, P., and Price, E. 2016. Developing a radio- Moura-Leite, J.C.D., and Bonatto, S.L. 2009. Molecu- metrically-dated chronologic sequence for Neogene lar phylogeny of advanced snakes (Serpentes, biotic change in Australia, from the Riversleigh World Caenophidia) with an emphasis on South American Heritage Area of Queensland. Gondwana Research, Xenodontines: a revised classification and descrip- 29:153-167. tions of new taxa. Papéis Avulsos de Zoologia (São Wüster, W., Crookes, S., Ineich, I., Mané, Y., Pook, C.E., Paulo), 49:115-153. Trape, J.F., and Broadley, D.G. 2007. The phylogeny of cobras inferred from mitochondrial DNA sequences: evolution of venom spitting and the phy- logeography of the African spitting cobras (Ser- pentes: Elapidae: Naja nigricollis complex). Molecular Phylogenetics and Evolution, 45:43-453.

21