Michael W. Caldwell

ADRIOSAURUS AND THE AFFINITIES OF MOSASAURS, DOLICHOSAURS, AND SNAKES

Abstract The poorly-known, long bodied, limb-reduced marine lizard Adriosaurus suessi Seeley, 1881, is reassessed. Adriosaurus and a number of other marine lizards are known from Upper Cretaceous (Upper Cenomanian-Lower Turonian) marine carbonate rocks exposed along the Dalmatian coast of the Adriatic Sea, from Komen, Slovenia, to Hvar Island, Croatia. A revised vertebral count reveals 10 cervical, 29 dorsal, and at least 65 caudal vertebrae. The projections previously interpreted as hypapophyses are instead transverse processes. Openings on the anterior part of the skull, previously described as external nares, are probably internal nares. Important features not noted previously include accessory articulations on all presacral vertebrae, pachyostosis of dorsal vertebrae and ribs, and the presence of two pygal vertebrae. Phylogenetic analysis of 258 osteological characters and all the major squamate lineages suggests that Adriosaurus and dolichosaurs are successive sister-taxa to snakes. This is consistent with their long-bodied, limb-reduced morphology being intermediate between typical marine squamates (e.g., mosasaurs) and primitive marine snakes (pachyophiids). The analysis further reveals that up to five successive outgroups to living snakes (pachyophiids, Adriosaurus, dolichosaurs, Aphanizocnemus, and mosasauroids) are all marine, suggesting a marine (or at least, semi-aquatic) phase in snake origins. These phylogenetic results are robust whether multistate characters are ordered or unordered, thus refuting recent suggestions that snakes cluster with amphisbaenians and dibamids (rather than aquatic lizards) if multistate characters are left unordered. Also, the recent suggestion that Pachyrhachis shares synapomorphies with advanced snakes (macrostomatans) is shown to be poorly supported, because the reinterpretations of the relevant skull elements are unlikely and, even if accepted, the character states proposed to unite Pachyrhachis and advanced snakes are also present in more basal snakes and/or the nearest lizard outgroups, and are consequently primitive for snakes.

The origin of snake feeding

Snakes are renowned for their ability to engulf extremely large prey, and their highly flexible skulls and extremely wide gape are among the most striking adaptations found in vertebrates. However, the evolutionary transition from the relatively inflexible lizard skull to the highly mobile snake skull remains poorly understood, as they appear to be fundamentally different and no obvious intermediate stages have been identified,. Here we present evidence that mosasaurs — large, extinct marine lizards related to snakes — represent a crucial intermediate stage. Mosasaurs, uniquely among lizards, possessed long, snake-like palatal teeth for holding prey. Also, although they retained the rigid upper jaws typical of lizards, they possessed highly flexible lower jaws that were not only morphologically similar to those of snakes, but also functionally similar. The highly flexible lower jaw is thus inferred to have evolved before the highly flexible upper jaw — in the macrophagous common ancestor of mosasaurs and snakes — for accommodating large prey. The mobile upper jaw evolved later — in snakes — for dragging prey into the oesophagus. Snakes also have more rigid braincases than lizards, and the partially fused meso- and metakinetic joints of mosasaurs are transitional between the loose joints of lizards and the rigid joints of snakes. Thus, intermediate morphologies in snake skull evolution should perhaps be sought not in small burrowing lizards, as commonly assumed, but in large marine forms.

On the aquatic squamate Dolichosaurus longicollis Owen, 1850 (Cenomanian, Upper Cretaceous), and the evolution of elongate necks in Squamates

Abstract The marine squamate, Dolichosaurus longicollis, from the Upper Cretaceous (Cenomanian) Chalk deposits of southeast England is redescribed. The elongate neck of D. longicollis is produced by an increased number of cervical vertebrae. Cervical peduncles are elongate, curved and are not fused to the hypapophyses. There is no scapulocoracoid fenestra, the coracoid is not emarginated, and the scapula and coracoid are not fused. The splenial and angular articulate in a ball-and-socket joint similar to that of mosasaurs and Coniasaurus crassidens. The forelimb and pectoral girdle elements show evidence of reduction as compared to the pelvic girdle and rearlimb. Cladistic analysis of six mosasaur taxa, three ‘aigialosaur’ taxa, Coniasaurus crassidens, Coniasaurus gracilodens, and D. longicollis, using 66 characters, found 27 most parsimonious cladograms (MPCs): 122 steps; C.I. 0.648; H.I. 0.352; R.I. 0.669. A Strict Consensus Tree found support for the monophyly of the Mosasauridae and Aigialosauridae; sister-group relationships between coniasaurs, Dolichosaurus, Aigialosauridae and Mosasauridae are an unresolved polytomy. A Majority Rule Consensus Tree finds Dolichosaurus as sistergroup to (C. crassidens, C. gracilodens (Aigialosauridae (Mosasauridae))) in nine (33%) of the MPCs. Lack of support for a more inclusive Dolichosauridae composed of Dolichosaurus + (C. crassidens, C. gracilodens) is attributed to the incompleteness of the fossil remains of these three taxa. Presence/absence of a pectoral girdle currently defines the presence/absence of a neck. This definition is insufficient and hypapophyses are found more informative regarding taxic differences and transformational scenarios. The paleobiology of Dolichosaurus is reconstructed as similar to coniasaurs, nothosaurs, and modern sea snakes.

Convergent evolution in aquatic tetrapods: insights from an exceptional fossil mosasaur.

Mosasaurs (family Mosasauridae) are a diverse group of secondarily aquatic lizards that radiated into marine environments during the Late Cretaceous (98–65 million years ago). For the most part, they have been considered to be simple anguilliform swimmers – i.e., their propulsive force was generated by means of lateral undulations incorporating the greater part of the body – with unremarkable, dorsoventrally narrow tails and long, lizard-like bodies. Convergence with the specialized fusiform body shape and inferred carangiform locomotory style (in which only a portion of the posterior body participates in the thrust-producing flexure) of ichthyosaurs and metriorhynchid crocodyliform reptiles, along with cetaceans, has so far only been recognized in Plotosaurus, the most highly derived member of the Mosasauridae. Here we report on an exceptionally complete specimen (LACM 128319) of the moderately derived genus Platecarpus that preserves soft tissues and anatomical details (e.g., large portions of integument, a partial body outline, putative skin color markings, a downturned tail, branching bronchial tubes, and probable visceral traces) to an extent that has never been seen previously in any mosasaur. Our study demonstrates that a streamlined body plan and crescent-shaped caudal fin were already well established in Platecarpus, a taxon that preceded Plotosaurus by 20 million years. These new data expand our understanding of convergent evolution among marine reptiles, and provide insights into their evolutions tempo and mode.

The pectoral girdle and forelimb of Carsosaurus marchesetti (Aigialosauridae), with a preliminary phylogenetic analysis of mosasauroids and varanoids

ABSTRACT The aigialosaur Carsosaurus marchesetti is represented by a nearly complete skeleton from the Upper Cretaceous (Cenomanian-Turonian) of Slovenia. Dermal girdle elements include portions of the clavicles and a small interclavicle with a short anterior process. Endochondral girdle elements include a small scapula and large unfenestrated coracoid. A mineralized sternum is also present. The carpus is anguid-like and consists of ten ossified elements. Reduction of the procoelous nature of centrum articular surfaces is restricted to the caudal series. The type of C. marchesetti is the largest aigialosaur specimen known (> 1.5 m) and has proportionally larger propodials than any other aigialosaur. Phylogenetic reconstruction places Carsosaurus within a polytomous clade composed of all known aigialosaurs. Aigialosaurs are the sister-group to Mosasauridae, forming the Mosasauroidea, and are within Anguimorpha but distinct from Varanoidea. Supposed synapomorphies of varanids and mosasauroids are identified...

Live birth in Cretaceous marine lizards (mosasauroids).

Although live-bearing (viviparity) has evolved around 100 times within reptiles, evidence of it is almost never preserved in the fossil record. Here, we report viviparity in mosasauroids, a group of Cretaceous marine lizards. This is the only known fossil record of live-bearing in squamates (lizards and snakes), and might represent the oldest occurrence of the trait in this diverse group; it is also the only known fossil record of viviparity in reptiles other than ichthyosaurs. An exceptionally preserved gravid female of the aigialosaur Carsosaurus (a primitive mosasauroid) contains at least four advanced embryos distributed along the posterior two-thirds of the long trunk region (dorsal vertebrae 9-21). Their orientation suggests that they were born tail-first (the nostrils emerging last) to reduce the possibility of drowning, an adaptation shared with other highly aquatic amniotes such as cetaceans, sirenians and ichthyosaurs; the orientation of the embryos also suggests that they were not gut contents because swallowed prey are usually consumed head-first. One embryo is located within the pelvis, raising the possibility that the adult died during parturition. Viviparity in early medium-sized amphibious aigialosaurs may have freed them from the need to return to land to deposit eggs, and permitted the subsequent evolution of gigantic totally marine mosasaurs.

A new basal mosasauroid from the Cenomanian (U. Cretaceous) of Slovenia with a review of mosasauroid phylogeny and evolution

Abstract A new genus and species of basal mosasauroid reptile from the Cenomanian (Upper Cretaceous) of Slovenia, previously referred to as the “Trieste aigialosaur,” is described. The new taxon is known from only a single specimen including a well-preserved postcranial skeleton and parts of the skull (i.e., left quadrate, left surangular-prearticular complex, and left angular and splenial). Morphological characters of the quadrate and postcranial skeleton distinguish this new taxon from other basal mosasauroids such as Aigialosaurus dalmaticus, Aigialosaurus (=Opetiosaurus) bucchichi and Carsosaurus marchesettii. Cladistic parsimony analysis of a taxon character matrix composed of 135 characters and 31 terminal taxa resulted in the recovery of 12 equally parsimonious cladograms of 351 steps (CI = 0.48, HI = 0.52, and RI = 0.73). From these cladograms we present a phylogenetic hypothesis on the interrelationships of mosasauroids. Species assigned to Aigialosaurus form the basalmost mosasauroid clade. The new genus described here is reconstructed with Carsosaurus marchesettii in a clade that is the sistergroup to the following clade: (Haasiasaurus ((Halisaurinae, (Tethysaurus nopcsai (Yaguarasaurus columbianus, Russellosaurus coheni)) (Russellosaurina)))); the “Dallas aigialosaur,” Dallasaurus turneri, is found to be the basal-most mosasaurine. Arguments supporting the importance of pelvic evolution to the aquatic adaptations of mosasaurs are given along with a discussion of recent hypotheses of limb evolution in mosasauroids.

EXCEPTIONALLY PRESERVED SKELETONS OF THE CRETACEOUS SNAKE DINILYSIA PATAGONICA WOODWARD, 1901

For over one hundred years the Upper Cretaceous snake Dinilysia patagonica has been known from only the holotype skull and associated vertebrae (Smith-Woodward, 1901; Estes et al., 1970; Frazetta, 1970; Hecht, 1982; Rage and Albino, 1989; Albino, 1996). Recent fieldwork near Neuquen, Argentina, has produced a large number of exceptionally well-preserved skulls and skeletons of Dinilysia that preserve osteological features missing in the holotype. This new information is timely as recent studies of snake phylogeny have relied upon incomplete descriptions of Dinilysia (Caldwell, 1999; Scanlon and Lee, 2000; Tchernov et al., 2000). Our study of the new fossils indicates that Dinilysia was a large-bodied snake with an aniliid/ xenopeltid-like middle-ear osteology, and an anguimorph-like hypapophyseal/intercentrum anatomy. These new data will certainly impact future studies of snake phylogeny. We provide the first diagnosis of Dinilysia patagonica Smith-Woodward, 1901, along with a preliminary description of the new material, followed by discussion of two important osteological features (i.e., postorbital vs. jugal, absence of a crista circumfenestralis). The holotype and all new specimens of Dinilysia described here were found at three localities in or near Neuquén, Neuquén Province, Argentina. The fossil-producing units are redto white-weathering, coarse-grained sandstones assigned to the Bajo de la Carpa Member, Rio Colorado Formation (?Coniacian, Upper Cretaceous; Caldwell and Albino, 2001). The holotype specimen (Smith-Woodward, 1901; Estes et al., 1970) and two fragmentary skulls were found at Boca del Sapo, just north of Neuquén. Another fragmentary skull, assigned here to Dinilysia, was collected in the 1980s from outcrops just north of the Universidad Nacional del Comahue in Neuquén. The most recent collection of excellent skulls and articulated postcranial skeletons is from outcrops of the Rı́o Colorado Formation exposed at the ‘‘Tripailao Farm Locality.’’ These sections are located on the south side of the Rio Negro approximately 8.5 km to the west of the bridge at Paso Córdoba, or approximately 23 km to the southeast of Neuquén on the south side of the river (Caldwell and Albino, 2001). Institutional Abbreviations MACN, Museo Argentino de Ciencias Naturales ‘‘Bernardino Rivadavia,’’ Buenos Aires, Argentina; MLP, Museo de La Plata, La Plata, Argentina; MPCA-PV, Museo de la Ciudad de Cipoletti, Cipoletti, Rı́o Negro Province, Argentina; MUCP, Museo de Geologı́a y Paleontologı́a, Universidad Nacional del Comahue, Neuquén, Argentina. SYSTEMATIC PALEONTOLOGY

Limb osteology and ossification patterns in Cryptoclidus (Reptilia: Plesiosauroidea) with a review of sauropterygian limbs

ABSTRACT Limb osteology and ontogenetic patterns of limb ossification are described for the plesiosaur Cryptoclidus eurymerus (Upper Jurassic: Callovian), and compared to those of other sauropterygians. Major features of limb ossification in Cryptoclidus are identified: 1) delayed mesopodial ossification; 2) alterations to the ossification sequence of the radius/ulna, tibia/fibula, and some metacarpals and metatarsals; 3) the loss of perichondral bone from the margins of the radius/ulna, tibia/fibula, and some metacarpals and metatarsals; 4) altered bone morphology is correlated with loss of perichondral bone. Recognition of some of these features in basal sauropterygians, and their application to the study of limb elements in derived sauropterygians such as Cryptoclidus, alters traditional identifications of several bones. The conventional intermedium is re-identified as a centrale. The ‘true’ intermedium is found to be a small bone that is variably free, ossifies to the base of the radius forming a dist...

HISTOLOGY OF TOOTH ATTACHMENT TISSUES IN THE LATE CRETACEOUS MOSASAURID PLATECARPUS

Abstract We present new data on the tooth attachment histology of the Late Cretaceous marine lizard Platecarpus (Mosasauridae). Examination of thin sections of a right dentary reveals the presence of a woven-fiber bone matrix that forms the margins and floor of the tooth alveolus; this bony matrix is traditionally identified as bone of attachment. We identify it as alveolar bone based on its histologic and topologic similarities to archosaurian and mammalian alveolar bone. We also identify a cribiform plate, a structure usually associated with the periodontal ligament. Parallel fibers present in multiple, non-resorbed generations of alveolar bone are tentatively identified as remnants of mineralized portions of collagen fiber bundles, or Sharpey’s fibers. Along the sides of the dentine root we identify a thin layer of acellular cementum. The acellular cementum is surrounded by an enormous mass of cellular cementum tissue that fills the alveolus. This cementum mass is composed of two histologically distinct forms: (1) a loosely organized cellular cementum ground matrix; (2) a laminar form surrounding the vascularization (cementeons) that we term osteocementum. Mosasaurs possess the attachment tissues that are used to diagnose thecodont ankylosis. Mosasaur thecodonty is derived within the Mosasauroidea (aigialosaurs + mosasaurs).