The Oldest Known Snakes from the Middle Jurassic-Lower Cretaceous Provide Insights on Snake Evolution

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The Oldest Known Snakes from the Middle Jurassic-Lower Cretaceous Provide Insights on Snake Evolution ARTICLE Received 1 Oct 2014 | Accepted 1 Dec 2014 | Published 27 Jan 2015 DOI: 10.1038/ncomms6996 The oldest known snakes from the Middle Jurassic-Lower Cretaceous provide insights on snake evolution Michael W. Caldwell1, Randall L. Nydam2, Alessandro Palci3 & Sebastia´n Apesteguı´a4 The previous oldest known fossil snakes date from B100 million year old sediments (Upper Cretaceous) and are both morphologically and phylogenetically diverse, indicating that snakes underwent a much earlier origin and adaptive radiation. We report here on snake fossils that extend the record backwards in time by an additional B70 million years (Middle Jurassic-Lower Cretaceous). These ancient snakes share features with fossil and modern snakes (for example, recurved teeth with labial and lingual carinae, long toothed suborbital ramus of maxillae) and with lizards (for example, pronounced subdental shelf/gutter). The paleobiogeography of these early snakes is diverse and complex, suggesting that snakes had undergone habitat differentiation and geographic radiation by the mid-Jurassic. Phylogenetic analysis of squamates recovers these early snakes in a basal polytomy with other fossil and modern snakes, where Najash rionegrina is sister to this clade. Ingroup analysis finds them in a basal position to all other snakes including Najash. 1 Department of Biological Sciences, & Department of Earth and Atmospheric Sciences, University of Alberta, Edmonton, Alberta T6G2E9, Canada. 2 Department of Anatomy, Midwestern University, Glendale, Arizona 85308, USA. 3 Earth Sciences Section, South Australian Museum, North Terrace, Adelaide, South Australia 5000, Australia. 4 Fundacio´nFe´lix de Azara, CEBBAD (CONICET), Universidad Maimo´nides, Buenos Aires 1405, Argentina. Correspondence and requests for materials should be addressed to M.W.C. (email: [email protected]). NATURE COMMUNICATIONS | 6:5996 | DOI: 10.1038/ncomms6996 | www.nature.com/naturecommunications 1 & 2015 Macmillan Publishers Limited. All rights reserved. ARTICLE NATURE COMMUNICATIONS | DOI: 10.1038/ncomms6996 he previous understanding of the fossil record of early extending from tooth position 4 to tooth position 16/17; anterior snake evolution (Late Mesozoic) relies on isolated superior alveolar foramen large, positioned at front of ascending Tvertebrae from Africa1 (100 Myr ago), isolated jaws and process; prominent premaxillary process, narrow and turned vertebrae from North America2,3 (98–65 Myr ago), a number of medially; supradental shelf narrow and thin with prominent nearly complete snakes, some with rear limbs4–7, from the palatine process adjacent to posterior end of ascending process; circum-Mediterranean region (98–95 Myr ago), and two taxa margin of palatine process damaged; long, tooth-bearing of relatively complete snakes, one with rear limbs, from suborbital ramus with 10 tooth positions posterior to prefrontal Argentina (94–92 Myr ago8,9 and 86–80 Myr ago10,11). This facet and palatine process; maxillary tooth positions defined by morphologically, ecologically and phylogenetically diverse three-sided alveolus with no medial border; preserved teeth assemblage of snakes appears in the fossil record around the attached to rims of alveoli; presence of tooth in alveolus closes world almost simultaneously (B100–94 Myr ago). The long small posterolingual notch forming basal nutrient foramen; teeth standing questions in snake palaeontology have centred on when, conical, circular cross sections, recurved, with labial and lingual where and how snakes evolved and radiated from within carinae. Squamata before the early part of the Late Cretaceous. Here we report on four new species of significantly older fossil aff. Parviraptor estesi snakes (167–143 Myr ago) recognized from cranial and post- (Figs 1b,2s and 3a; Supplementary Figs 3a–d and 4a–i). cranial remains found in the United Kingdom, Portugal Referred Material. Right frontal, atlas and associated and the United States. These new data extend the known precloacal vertebrae on multispecimen block NHMUK geological range of snakes by nearly 70 million years into the R8551 (specimen originally assigned to Parviraptor estesi15). mid-Mesozoic, indicating that their origin was coincident with Locality, horizon and age. Swanage, Dorset, England; the known radiation of most other major groups of squamates in Purbeck Limestone Formation (Upper Jurassic; Tithonian/ the mid-Jurassic12,13 during the final stages of the break-up of Lower Cretaceous; Berriasian). Pangaea into Laurasia and Gondwana. It is also important to note that this new record for early snakes, co-occurring Description. Right frontal (NHMUK R8551) in lateral view with early anguimorphs such as Dorsetisaurus12,13, fills a major 14 with well-developed prefrontal and postfrontal facets and deep, chronological gap predicted by molecular phylogenetics . medially curved descensus frontalis with well-developed suboptic In stratigraphic order, the oldest snake recognized here is shelves on posteroventral margin forming posterior portion of found in rocks dated as Bathonian (B167 Myr ago), Middle 15 optic nerve foramen (Cranial Nerve II); closely associated Jurassic, from Southern England , followed by a North vertebrae with tall neural spines, massive, vertical synapophyses American record dated as Kimmeridgian (B155 Myr ago, 16 with distinct, posteriorly expanded parapophyseal and diapophy- Upper Jurassic, Colorado, USA) , which appears to be a seal facets; complete neural arch with short zygosphenes; contemporary of another taxon from the Kimmerdigian (Upper 17 posterior margin lacks incised median notch; elevated, round Jurassic, Guimarota, Portugal) . The youngest snake taxon condyles with weakly constricted necks; centrum narrow poster- and materials recognized here are found in rocks dated as B iorly and wide anteriorly in ventral view; inferior margin of Tithonian ( 150 Myr ago; Upper Jurassic) to Berriasian centrum, no development of haemal keel; possible sacral vertebra (B140 Myr ago; Lower Cretaceous) outcropping near Swanage, 15 with robust transverse processes; left neural arch from an atlas Dorset, Southern England . with narrow, posteriorly directed neural spine; no notochordal canal. Results Remarks. Because of the loss of the provenance of this block with Systematic palaeontology. respect to the block NHMUK 48388, the lack of articulation of the elements, and the polytaxonomic composition of the Purbeck Order Squamata Opell, 1811 blocks, we do not feel that there is sufficient evidence to support Suborder Serpentes Linnaeus, 1758 referral of the frontal to type maxilla of Parviraptor estesi, although Parviraptor estesi gen. et sp. we do recognize that such a referral is a strong possibility. (Figs 1a and 2a; Supplementary Figs 1 and 2a–e). Diablophis gilmorei gen. nov., new combination Holotype. Left maxilla on block NHMUK R48388, Natural (Figs 1c–f and 2b,j; Supplementary Figs 10a–k and 11a–n; History Museum, London. Supplementary Videos 1–9). Locality horizon and age. Durlston Bay, Swanage, Dorset, England; Purbeck Limestone Formation (Upper Jurassic; Etymology.‘Diablo’, ‘devil’ (Spanish); ophis, snake (Greek); Tithonian/Lower Cretaceous; Berriasian). in recognition of type locality near Devil’s Canyon, Emended Diagnosis. Long low, ascending process of Colorado. maxilla; premaxillary process turned medially; narrow Holotype. LACM 4684/140572 (Los Angeles County prefrontal facet on ascending process of maxilla. Differs Museum), broken right maxilla, broken right mandible, from maxilla of Coniophis precedens in lacking medial and broken axis vertebra (revised holotype). process at anterior end, in having greater degree of Referred Specimens. Several precloacal vertebrae and one recurvature of teeth. Differs from Dinilysia patagonica in possible sacral vertebra LACM 4684/140572; broken right having gracile maxilla, relatively smaller teeth, less pro- dentary LACM 5572/120732 (all specimens originally 16 nounced medial deviation at anterior tip and relatively referred to Parviraptor gilmorei ); LACM 4684/120472, smaller palatine process. Differs from Portugalophis lignites four precloacal vertebrae, one caudal vertebra with large in having narrower premaxillary process. Differs from transverse processes. Diablophis gilmorei in having larger palatine process and Locality, horizon and age. From Fruita locality, Morrison in lacking medial curvature of anterior end of maxilla. Formation, Mesa County, Colorado, USA (Upper Jurassic; Kimmeridgian). Revised Description. Maxilla exposed in medial and dorsal views; Diagnosis. Small-bodied snake that differs from Parviraptor long, 24 tooth positions preserved, bearing low ascending process estesi and Portugalophis lignites in having smaller palatine 2 NATURE COMMUNICATIONS | 6:5996 | DOI: 10.1038/ncomms6996 | www.nature.com/naturecommunications & 2015 Macmillan Publishers Limited. All rights reserved. NATURE COMMUNICATIONS | DOI: 10.1038/ncomms6996 ARTICLE ab m Palaeocene Laurasia Gondwana England Maastrichtian Sanajeh Indophis Madtsoia Campanian Kelyophis Coniophis Menarana Cerberophis Australophis ?Scolecophidia Late Santonian c g Coniacian Turonian Dinylisia Unnamed ‘alethnophidian’ Cenomanian d h Najash Albian Mesophis Pouitella Pachyophis Eupodophis Haasiophis Cretaceous Simoliophis Simoliophis ‘Coniophis’ Pachyrachis Lapparentophis e i Aptian Early Portugal Colorado Eur NA Afr India Barremian SA ME Mad Hauterivian f j Valanginian Berriasian Tithonian Kimmeridgian Oxfordian kl Parviraptor Callovian Parviraptor aff. Bathonian
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