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Anatomy and Relationships of Pachyrhachis Problematicus, a Primitive Snake with Hindlimbs

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Anatomy and Relationships of Pachyrhachis Problematicus, a Primitive Snake with Hindlimbs Anatomy and relationships of Pachyrhachis problematicus, a primitive snake with hindlimbs Michael S. Y. Lee1* and Michael W. Caldwell2,3 1Zoology Building A08, School of Biological Sciences, University of Sydney, NSW 2006, Australia 2Department of Geology,The Field Museum, Roosevelt Road at Lakeshore Drive, Chicago, IL 60605, USA 3Department of Biological Science, Biological Sciences Center, University of Alberta, Edmonton, Alberta, CanadaT6G 2E9 CONTENTS PAGE 1. Introduction 1522 2. Locality and stratigraphy 1522 3. Associated fauna and depositional environment 1523 4. Systematic palaeontology 1523 (a) Synonymy 1524 (b) Diagnosis 1524 (c) Type locality and horizon 1524 (d) Holotype 1524 (e) Referred specimen 1524 (f ) Remarks 1525 5. Morphology of Pachyrhachis 1527 (a) Cranium 1527 (b) Postcranial elements 1537 6. The a¤nities of Pachyrhachis with other squamates 1544 (a) Squamate features of Pachyrhachis 1544 (b) Pythonomorph features of Pachyrhachis 1547 (c) Ophidian features of Pachyrhachis 1548 (d) Advanced features of modern snakes (Serpentes) absent in Pachyrhachis 1550 (e) Advanced features shared by alethinophidians and Pachyrhachis 1550 7. A phylogenetic taxonomy of Pythonomorpha 1550 (a) Pythonomorpha 1551 (b) Mosasauroidea 1551 (c) Ophidia 1551 (d) Pachyrhachis problematicus 1551 (e) Serpentes 1551 (f ) Scolecophidia 1551 (g) Alethinophidia 1551 References 1551 The anatomy of Pachyrhachis problematicus, an elongate, limb-reduced squamate from the Upper Cretaceous of Israel, is described and evaluated in detail. Previously considered a snake-like `lizard' of uncertain a¤- nities, it is here shown to be the most primitive snake, and the sister-group to all other snakes. Pachyrhachis exhibits numerous derived characters uniting it with modern snakes (scolecophidians and alethinophi- dians): e.g. mobile premaxilla^maxilla articulation, braincase enclosed by frontals and parietals, sagittal parietal crest, absence of tympanic recess, single postdentary bone, over 140 presacral vertebrae, and complete loss of shoulder girdle and forelimb. However, it is more primitive than all modern snakes in retaining some strikingly primitive (lizard-like) features: presence of a jugal, squamosal, normal sacral attachment, and well-developed hindlimb composed of femur, tibia, ¢bula, and tarsals. Pachyrhachis provides additional support for the hypothesis that snakes are most closely related to Cretaceous marine lizards (mosasauroids). Almost all of the derived characters proposed to unite snakes and mosasauroids are highly developed in Pachyrhachis: the mobile mandibular symphysis, intramandibular joint, long and *Author and address for correspondence: Department of Biological Sciences, Monash University, Clayton, Victoria 3168, Australia ([email protected]) Phil. Trans. R. Soc. Lond. B (1998) 353, 1521^1552 1521 & 1998 The Royal Society Received 24 February 1997 Accepted 14 May 1997 1522 M. S.Y. Lee and M.W. Caldwell The primitive snake Pachyrhachis recurved pterygoid teeth, quadrate suspended by the supratemporal, loosely united pelvic elements (ilium, ischium, and pubis), and separate astragalus and calcaneum. Keywords: squamates; Cretaceous; osteology; mosasauroids; snakes; lizards pretation of the crushed skull of Pachyrhachis, and the 1. INTRODUCTION disarticulated skull of Estesius, was therefore extremely Snakes exhibit highly distinctive cranial and postcranial di¤cult. specializations, and are one of the most diverse and impor- Haas (1980b) was uncertain whether the two animals tant groups of living vertebrates. As a result, their a¤nities were related to snakesöand thus intermediate between with other squamatesölizards, amphisbaenians and varanoid lizards and snakesöor were only convergently dibamidsöhave been the subject of numerous investiga- snake-like. Haas also concluded that Pachyrhachis and Este- tions. Most of these studies, as emphasized in recent sius were distinct taxa, and described numerous di¡erences reviews (Rage 1987; Rieppel 1988), were unable to resolve between the two fossils. In view of the potential impor- conclusively the position of snakes within Squamata. The tance of these animals to clarify the a¤nities and origin intractability of the problem was attributed to high levels of snakes it is surprising that they have not been restudied of convergent evolution among the numerous lineages of since the original descriptions were published, and their elongate, limb-reduced squamates. The origin and rela- a¤nities remain enigmatic (Rage 1987; Carroll 1988; tionship of snakes therefore remains one of the main Rieppel 1988). unsolved problems in tetrapod evolution. Here we present a detailed description and reinterpreta- Recently, Caldwell (1998) reanalysed the phylogeny of tion of these two fossils. Further preparation has revealed the entire Squamata, revising and extending the data set much additional information about the morphology of the in Estes et al. (1988) by adding several important fossil skulls of these animals. In particular, preparation of the taxa. Lee (1997a) and Scanlon (1996) analysed relation- ventral surface of the skull of Estesius has revealed much ships within a more restricted group of squamates more of the skull, and demonstrated that many of the (Platynota), supplementing the data set of Pregill et al. elements on this animal were misidenti¢ed in the original (1986) through addition of important fossil taxa and new description. characters. All three studies found strong evidence uniting Our restudy of Pachyrhachis and Estesius indicates that snakes with mosasauroids, a group of Cretaceous marine they belong to the same species and are the most primitive lizards. Until these studies, no rigorous phylogenetic known snakes (Caldwell & Lee 1997). The two specimens analysis of squamate interrelationships had simultaneously possess a striking combination of derived snake-like considered both mosasauroids and snakes. As a result, features (e.g. highly kinetic skull, greatly elongated body) previous studies failed to identify the snake^mosasauroid along with primitive lizard-like features (e.g. functional association and the numerous derived characters pelvis and hindlimbs). This interpretation of Pachyrhachis supporting this arrangement. (including Estesius) as the sister-taxon of all other snakes Despite these studies, many aspects of the problem of clari¢es the lizard^snake transition and the origin of snake relationships remain contentious. In particular, many of the most distinctive specializations of snakes. whereas there was agreement on the mosasauroid^snake grouping (Pythonomorpha), there was disagreement on the position of this clade within Squamata as a whole. 2. LOCALITY AND STRATIGRAPHY Caldwell (1998) found that the mosasauroid^snake clade Both of the known specimens of Pachyrhachis problematicus occupied a rather basal position within Squamata, as the were found in the limestone quarries of Ein Jabrud, near sister-group to scleroglossans (non-iguanian squamates), the West Bank town of Ramallah, 20 km north of Jeru- while Lee (1997a) and Scanlon (1996) both placed Pytho- salem, Israel. Quarrying activities at Ein Jabrud have nomorpha deep within anguimorph scleroglossans, as exposed a sequence of carbonate rocks that have been relatives of Varanus and Lanthanotus (see ¢gure 15). attributed to the Bet-Meir Formation (Lower Cenoma- Another unresolved problem is the phylogenetic posi- nian; Early Upper Cretaceous). The fossil-bearing tion of some enigmatic squamate taxa that have not horizon is composed of ¢nely laminated, platey carbonates been included in any recent cladistic studies because that weather to a pink to reddish-orange colour. Few they were too poorly known. Two such taxa are Pachy- primary sedimentary structures were noted while exam- rhachis and Estesius (formerly `Ophiomorphus': see paper by ining slabs bearing Pachyrhachis or other vertebrates. Wallach (1984)); long-bodied marine squamates from Stratigraphic correlation between the Ein Jabrud the Cretaceous of the disputed West Bank, between section, and the type section of the Bet-Meir Formation at Israel and Jordan. These animals are not only very Nahal-Kesalon, 20 km east of Jerusalem, has not yet been similar, but were discovered in the same locality at completed (Chalifa & Tchernov 1982). However, based on almost the same time. Both are known from well- a review of various elements of the ¢sh faunas, Chalifa & preserved, largely complete, articulated skeletons, and Tchernov (1982) concluded that exposures at Ein Jabrud were described as showing a curious mixture of varanoid are lowermost Cenomanian. Comparisons with other and ophidian characters (Haas 1979, 1980a,b). However, Cenomanian rocks deposited in the late Mesozoic neo- the original descriptions were brief, and written when Tethys suggest that the Ein Jabrud section is slightly older the specimens were only partly prepared. In particular, than similar deposits in Lebanon (Chalifa & Tchernov the ventral surface of the skull of Estesius was not prepared, 1982), Comen, Slovenia, and the English Chalk (Patterson while part of the dorsal surface was covered by ribs. Inter- 1967). Phil. Trans. R. Soc. Lond. B (1998) The primitive snake Pachyrhachis M. S.Y. Lee and M.W. Caldwell 1523 increased global tectonism (Follmi 1989). The platforms 3. ASSOCIATED FAUNA AND DEPOSITIONAL were slowly drowned as water deepened. The mid-Cretac- ENVIRONMENT eous carbonate rocks in Israel and Lebanon record this The Cenomanian deposits at Ein Jabrud contain
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