Caldwell, 1996

Ontogeny and phylogeny of the mesopodialskeleton in mosasauroid reptiles

MICHAEL W. CALDWELL

Redpath Museum and Department of Biology, McGill University, 859 Sherbrooke St. West,Montreal, Quebec, Canada, H3A 2K6

Received January 1995, accepted for publication April 1995

Current phylogenies of mosasauroid reptiles are reviewed and a new phylogeny examining aigialosaurinterrelationships presented. Patterns of mesopodial ossification and overall limb morphology aredescribed for adult mosasauroids. Ossification sequences are mapped onto a phylogeny in order to assessthe distribution of ontogenetic characters. Consistent and ordered distributions are found. Based on thephylogenetic distribution of ossification patterns, an overall mesopodial ossification sequence formosasaurs is proposed. Carpal sequence: ulnare – distal carpal four (dc4) – intermedium – dc3 – radialeor dc2 – dc1 or pisiform and dc5. Tarsal sequence: astragalus – distal tarsal four or calcaneum. Skeletalpaedomorphosis is recognized as a dominant pattern in the evolution of mosasauroid limbs. Apomorphiccharacters of skeletal paedomorphosis, apparent in most taxa, reach extremes in tylosaurs. Argumentsfor the presence of a single proximal cartilage in the tarsus of mosasaurs are made. This cartilage ispresumed to include ossification centres from which both the astragalus and calcaneum will ossify.

©1996 The Linnean Society of London

ADDITIONAL KEY WORDS: — paedomorphosis – squamates – mosasaurs – aigialosaurs.

CONTENTS

Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . 408Material and methods . . . . . . . . . . . . . . . . . . . . . . . 409

Phylogenetic analysis . . . . . . . . . . . . . . . . . . . . . . 409Ontogenetic analysis . . . . . . . . . . . . . . . . . . . . . . 410

Mosasauroid phylogeny . . . . . . . . . . . . . . . . . . . . . . 410Review: recent phylogenies . . . . . . . . . . . . . . . . . . . . 410Results: phylogenetic analysis . . . . . . . . . . . . . . . . . . . 411

Osteology and ossification patterns . . . . . . . . . . . . . . . . . . . 413Aigialosaurs . . . . . . . . . . . . . . . . . . . . . . . . . 413Halisaurines . . . . . . . . . . . . . . . . . . . . . . . . 415‘Russellosaurines’ (Tylosaurines and Plioplatecarpines) . . . . . . . . . . . 416Mosasaurines . . . . . . . . . . . . . . . . . . . . . . . . 419

Discussion and conclusions . . . . . . . . . . . . . . . . . . . . . 422Ossification sequences and phylogeny . . . . . . . . . . . . . . . . 422Skeletal paedomorphosis . . . . . . . . . . . . . . . . . . . . 429Mosasaur astragalus . . . . . . . . . . . . . . . . . . . . . . 430

Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . 431

Present address: Department of Biological Sciences, Biological Sciences Center, University of Alberta, Edmonton,Alberta, Canada, T6G 2E9

Zoological Journal of the Linnean Society (1996), 116: 407–436. With 15 figures

4070024–4082/96/040407 + 30 $18.00/0 ©1996 The Linnean Society of London

References . . . . . . . . . . . . . . . . . . . . . . . . . . . 432Appendix I: data matrix and character descriptions from Bell (1993) . . . . . . . . 433

INTRODUCTION

Mosasauroid reptiles (aigialosaurs and mosasaurs) are a large group of extinctsquamates, united by a number of cranial synapomorphies, that achieved theirgreatest adaptive and taxonomic diversity in the Upper Cretaceous (Russell, 1967;Bell, 1993; deBraga & Carroll, 1993). Aigialosaurs are thought to have beenfacultatively aquatic while mosasaurs are believed to have been obligatory aquatic.These interpretations are based on characters of the appendicular and axial skeletonconsidered indicative of specialized aquatic adaptations (deBraga & Carroll, 1993).

The appendicular skeleton of aigialosaurs closely resembles that of a terrestrialsquamate, and shows no modifications that might be considered aquatic adaptations.Aigialosaurs do show some reduction of limb size relative to trunk length, but thiscondition has been shown to be equivocal as a diagnosis of aquatic lifestyles becausesimilar limb to body ratios are also found in fossorial squamates (Caldwell, Carroll,& Kaiser, 1995). However, modification of intervertebral articulations, generalshortening and loss of some transverse processes, and lateral compression of caudalcentra are interpreted as aquatic adaptations.

In contrast, the limbs of mosasaurs are paddle-like and differ significantly from thelimbs of aigialosaurs and other limbed squamates. Mosasaur limbs are characterizedby incomplete ossification of elements in the carpus and tarsus. Limb to body ratiosare significantly different from those of fossorial, terrestrial, or facultatively aquaticsquamates such as aigialosaurs (Caldwell et al., 1995). Aquatic adaptations are alsoobserved in the axial skeleton. The cauda central are laterally compressed and theneural spines and haemal arches are elongate. Further modifications include thereduction of zygosphene-zygantral articulations in a caudal to rostral direction, andan increase in the horizontal inflection, throughout the vertebral column, of theplane of articulation for the pre- and postzygapophyses.

This paper presents data on patterns of limb skeleton formation in mosasaurs. Theimmediate difficulty of such a study is that few juveniles of any mosasaur taxon areknown (Russell, 1967). Fortunately, for mosasaurs, as for other limbed squamates,ossification of carpal and tarsal bones (mesopodials) is significantly delayed relative toossification in the remainder of the appendicular skeleton (Rieppel, 1992 a,b,c;Caldwell, 1994). This phenomenon allows analysis of mesopodial ontogeneticpatterns in surprisingly late ontogenetic stages of large, adult mosasaurs. Despite therarity of juveniles, articulated adult mosasaurs are fairly common. Carpal and tarsal(mesopodial) ossification patterns described for extant squamates (Rieppel 1992a,b,c) and fossil stemgroup lepidosauromorphs (Caldwell, 1994) can therefore becompared to ontogenetic patterns in mosasaurs.

To understand the relationship of limb ontogeny to limb phylogeny, a priorunderstanding of mosasauroid phylogeny, free of assumptions regarding theontogenetic patterns under investigation, is a prerequisite. Previously proposedmosasauroid phylogenies are reviewed and discussed (Bell, 1993; deBraga & Carroll,1993; Caldwell et al., 1995) to establish a basis of comparison for ossificationpatterns.

No current phylogeny provides satisfactory resolution regarding the relationshipsof aigialosaurs. In an attempt to address this problem, the results of a phylogenetic

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analysis, focusing on basal mosasauroid relationships, and based on characters fromthe data sets of Bell (1993) and Caldwell et al. (1995), are presented. This phylogeny,and those of Bell (1993), deBraga & Carroll (1993), and Caldwell et al. (1995), werederived without the use of the ontogenetic data presented below. The intention is totest for the most congruent distribution of mesopodial ossification patterns amongmosasauroid reptiles by comparison with phylogenetic hypotheses presentedbelow.

The discovery of character congruence, based on hierarchies of synapomorphies,produces a pattern from which phylogeny may be deduced (Patterson, 1982). Acladogram provides a starting point for analysing and interpreting phylogeny. It iswithin this context that developmental and evolutionary patterns of skeletalpaedomorphosis can be recognized through evolution of a clade such as mosasauroidreptiles.

Particular attention is given to the nature of the mosasaur astragalus andcalcaneum. The general problem is whether or not these two bones ossifiedendochrondrally within a single cartilaginous precursor (the typical lizard condition)or within separate cartilaginous precursors (the primitive diapsid condition[Caldwell, 1994]). Much debate has centered on the phylogeny and ontogeny of theamniote astragalus with the focus being the number of elements in the proximaltarsal row (Rieppel, 1993). Understanding the mosasaur astragalus assists inunderstanding the phylogeny of this bone in diapsids generally and in squamatesspecifically.

MATERIALS AND METHODS

Phylogenetic analysis

Phylogenetic analysis of mosasauroids was conducted using PAUP Version 3.1.1for the Macintosh (Swofford, 1993). Characters and taxa from Bell’s (1993) analysiswere reduced in number (37 taxa to 15; 151 characters to 91) and a new matrixconstructed (Appendix I); some new taxa were added based on the analysis ofaigialosaurs by Caldwell et al. (1995). All multistate character transformations wereunordered and characters were optimized using assumptions of acceleratedtransformation (ACCTRAN). Polarity for all characters is according to Bell’s (1993)assessment of outgroup character states.

Mosasaur taxa included are the basal-most taxa of clades identified by Bell (1993).All aigialosaurs and halisaurs of Bell (1993) were included in this analysis. A numberof characters (Bell’s Characters 1, 13, 16, 40, 59, 70, 100, and 125) were recoded forAigialosaurus ( = Opetiosaurus) buccichi, Aigialosaurus dalmaticus, and the Trieste aigialo-saur, referred to here as Carsosaurus marchesetti based on Caldwell et al. (1995). Theserecodings are based on study of latex peels of the holotypes (see Appendix I forspecific changes). Sixty characters from Bell’s (1993) matrix were found to beautapomorphic or invariant within the reduced matrix and were therefore excluded(Appendix I). Characters 74 and 96 of Bell (1993) were recoded to accommodatechanges in the distribution of states due to the reduced number of terminal taxa.

409MOSASAUR MESOPODIALS

Ontogenetic analysis

Ossification patterns for most mosasaur taxa were obtained from originalspecimens. Data for several European mosasaur taxa were obtained from theprimary literature. For aigialosaurs, and a number of mosasaur taxa, limb ontogeniesare not available. Articulated limbs from forty-one individual mosasaurs and twoaigialosaurs are illustrated. Many specimens were either still in the matrix or wereaccompanied by field photos or drawings showing the original position of the bones.For ease of comparison some illustrations are reversed so that for a particular limbseries all figures are oriented in the same direction.

Materials examined or referred to in this study are housed in institutions bearingthe following abbreviations: American Museum of Natural History, New York(AMNH); Bayerische Staatssammlung fur Palaontologie und historische Geologie,Munchen (BSP); California Institute of Technology (CIT); Canterbury Museum,New Zealand (CM); Dominion Museum, Wellington, New Zealand (DM); FickMuseum, Oakley, Kansas (FM); Fort Hays Museum — Vertebrate Paleontology,Fort Hays State University, Fort Hays, Kansas (FHM — VP); Institut Royal desSciences Naturelles de Belgique, Brussels (IRSNB); Museum of Natural History,University of Kansas, Lawrence (KU); Los Angeles County Museum of NaturalHistory, Los Angeles, California (LACM); Museo Civico di Storia Naturale, Trieste,Italy (MCSNT); Museum of Comparative Zoology, Harvard University, Cambridge,Massachusetts (MCZ); Morden Museum, Morden, Manitoba (MDM); NationalMuseum of Canada, Ottawa, Ontario (NMC); Naturhistorisches Museum, Wien,Austria (NMW); Princeton University, Yale Peabody Museum, New Haven,Connecticut (PU); Saskatchewan Museum of Natural History, Regina (SMNH);South Dakota School of Mines and Technology, Rapid City (SDSM); Museum ofPaleontology, University of California, Berkeley (UCBMP); Yale Peabody Museum,New Haven, Connecticut (YPM).

MOSASAUROID PHYLOGENY

Review: recent phylogenies (Fig. 1A–C)

Bell (1993), deBraga & Carroll (1993), and Caldwell et al. (1995) examined thephylogenetic relationships of mosasauroid reptiles, drawing heavily from McDowell& Bogert (1954) and Russell (1967). Bell’s (1993) analysis is a taxonomic andphylogenetic revision of mosasauroid reptiles at the level of individual species.DeBraga & Carroll (1993) examined family or genus level relationships and weremore interested in macroevolutionary trends. Caldwell et al. (1995) focused onaigialosaur and mosasaur characters in the context of putative varanoidsistergroups.

The key problem in these phylogenies, critical to this study as it affects the polarityof morphological transformations, is the relationship of mosasauroids to varanoidlizards. DeBraga & Carroll (1993) assumed mosasauroids to be the sistergroup of theVaranidae (Fig. 1A). Caldwell et al. (1995) found no support for a varanid-mosasauroid clade, nor could mosasauroids be placed within the Varanoidea (Fig.1B). Bell (1993) was unable to falsify or support mosasauroid relationships either with

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or within the Varanidae (Fig. 1C). Neither Bell (1993) nor Caldwell et al. (1995) wereable to clarify a Varanoid-Mosasauroid sistergroup relationship.

A further important difference between the phylogenies of deBraga & Carroll(1993) (Fig. 1A) and Bell (1993) (Fig. 1C) concerns the ingroup relationships of themosasaurs Prognathodon and Plesiotylosaurus. DeBraga & Carroll (1993) followed Russell(1967) and reconstruct Prognathodon and Plesiotylosaurus within the Plioplatecarpinae(Fig. 1A) forming the basal plioplatecarpine clade. Tylosaurines are placed below thePlioplatecarpinae, separating plioplatecarpines from the Mosasaurinae. In contrast,Bell (1993) hypothesized the two genera as the sister-taxa to Globidens; together, thesethree taxa compromise the clade Globidensini within Mosasaurinae.

Results: Phylogenetic analysis

Analysis of the matrix given in Appendix I produced 70 most parsimonious trees,each of 189 steps, with a CI of 0.582. A Strict Consensus Tree of all trees (Fig. 2A)supports the monophyly of halisaurines, and all other more derived mosasaurs(‘russellosaurines’ and mosasaurines of Bell [1993]). The position of Ectenosaurusclidastoides is unstable, resulting in a polychotomy within derived mosasaurs. Thisappears to be a result of the reduced data set and the absence of conclusivesynapomorphies for ectenosaurs with either ‘russellosaurines’ or mosasaurines; this isreinforced by the consensus tree presented below. Bell’s (1993) ‘Taxon Novum’, anundescribed mosasaur, is unequivocally the most basal ‘mosasauroid’ taxon, otherthan Aigialosaurus buccichi. Aigialosaur monophyly, disputed by Bell (1993), is neithersupported nor falsified in this analysis as all aigialosaur terminal taxa are within theconventional Mosasauridae, and all aigialosaur branches collapse to a singlepolychotomous node. It is important to note that this polychotomy includes neitherhalisaurines nor Bell’s (1993) ‘Taxon Novum’. Halisaurines are resolved as a distinctclade within Bell’s (1993) Mosasauridae but his ‘Taxon Novum’ is not.

A Majority-Rule Consensus Tree (Fig. 2B), for all compatible groupings includingthose below 50%, provides some structure within the Strict Consensus aigialosaurpolychotomy. In 43% of the trees, the Dallas aigialosaur was the sister-taxon of theMosasauridae. The remaining aigialosaurs are reconstructed as successive branchesalong the main stem in the respective frequencies as illustrated. It appears that theabsence of data on many characters for the Dallas aigialosaur, and aigialosaurs ingeneral, may be responsible, in part, for the polychotomies present in this analysisand in Bell (1993).

Among derived mosasaurs (‘russellosaurines” and mosasaurines) the position ofEctenosaurus clidastoides is resolved in 50% of the trees as the siston-taxon of tylosaursand platecarpines.

To address the instability of Ectenosaurus clidastoides, a second analysis wasconducted in which the ingroup data set was enlarged by one taxon. The additionof Tylosaurus proriger to the character matrix increased the stability of the matrix andin all trees E. clidastoides was reconstructed as the sister taxon of both tylosaur speciesand Platecarpus planifrons.


B

A

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GENERAL OSTEOLOGY AND OSSIFICATION PATTERNS

Aigialosaurs

Carsosaurus marchesetti (Fig. 3A)Forelimb. The carpus contains ten ossified elements identified as the radiale, lateralcentrale, intermedium, ulnare, pisiform, medial centrale, and distal carpals twothrough five. The radiale is an irregularly shaped element, compressed proximodis-tally, and expanded into small lobes on its medial and lateral margins. The medialexpansion of the elements contributes to the distal margin of the antebrachial space.The lateral centrale is an irregular hexagon and articulates proximally with theintermedium, medially with the radiale and medial centrale, laterally with the ulnare,and distally with distal carpals two to four. The ulnare is the largest element in thecarpus, articulating with the lateral centrale and intermedium, as well as with distalcarpals four and five. The ulnare likely articulated with the pisiform but the pisiformappears to have rotated proximally out of articulation, making its exact morphologyand position difficult to determine. Distal carpal four is the largest element in thedistal carpal row. In order of largest to smallest in size, the remaining distal carpalsare respectively three, two, and five.

Figure 1. Mosasauroid phylogeny. A, redrawn from deBraga & Carroll (1993). B, strict consensus treederived from nine most-parsimonious trees of 107 steps; redrawn from Caldwell et al. (1995). C, Bell’s(1993) preferred hypothesis, an Adam’s Consensus Tree derived from seven most-parsimonious tree of375 steps; redrawn from Bell (1993).

C


Figure 2. Consensus trees of mosasauroid phylogeny derived from seventy most-parsimonious trees (treelength 189, CI 0.582), derived from data modified from Bell (1993) and Caldwell et al. (1995). A, strictconsensus tree. B, majority-rule consensus tree with option requests for all compatible groupingsincluding those below 50% (numbers refer to percentage of clade consistency of arrangement in seventytrees).

A

B

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Aigialosaurus buccichi ( = Opetiosaurus) (Fig. 3B)Forelimb. The carpus contains nine ossified elements identified as the radiale, lateralcentrale, ulnare, pisiform, medial centrale, and distal carpals two through five.Unlike Carsosaurus, there is no intermedium preserved in proximal articulation withthe lateral centrale and the pisiform is in contact with the ulnare. All other elementsand their articulations are similar to Carsosaurus.

Halisaurines

Halisaurus sternbergi (Fig. 3C)Forelimb. H. sternbergi (unnumbered specimen, Palaeontological Museum, Uppsala,Sweden) has four ossified carpal elements identified as the ulnare, intermedium, anddistal carpals four and three. The first metacarpal is the largest in the series and isa unique characteristic of mosasaurid metacarpal rows.

Figure 3. Forelimbs of two aigialosaurs and the mosasaur Halisaurus sternbergi. A, Carsosaurus marchesettiMCSNT unnumbered specimen. B, Aigialosaurus buccichi ( = Opetiosaurus) NMW unnumbered specimen. C,Halisaurus sternbergi (unnumbered specimen, Palaeontological Museum, Uppsala, Sweden; redrawn fromWiman [1920] and Bell [1993]). Abbreviations: a, astragalus; c, calcaneum; Co, coracoid; cS,cartilaginous sternum; F, femur; f, fibula; H, humerus; in, intermedium; lc, lateral centrale; mc, medialcentrale; p, pisiform; r1-5, sternal cartilages of presacral ribs 1-5; r, radius; rd, radiale; Sc, scapula; t,tibia; u, ulna; ul, ulnare; 2-5, distal carpals/tarsals; i-v, metacarpals/metatarsals.


‘Russellosaurines’ (Tylosaurines and Plioplatecarpines)

Tylosaurus and HainosaurusForelimb (Fig. 4). The smallest specimens (Fig. 4A–C) have only a single ossifiedelement identified as the ulnare. Larger individuals (Fig. 4D,E) have two ossifiedelements identified as the ulnare and distal carpal four. In the largest individualsknown, the tylosaurine carpus never exceeds two ossified carpal elements.Mesopodial elements are all poorly finished, sub-rounded bones. When found inarticulation, the spatial relationships and poor ossification of these elements suggeststhe presence of large cartilaginous margins; only a small portion of the elementossifies. The first metacarpal is the largest element in the metacarpal series.Rearlimb (Fig. 5). The least ossified tarsi (Fig. 5A–C) have only a single ossifiedelement identified as the astragalus. More highly ossified tarsi (Fig. 5D–F) have twoossified elements identified as the astragalus and distal tarsal four. The ossified stateof tarsal elements is similar to that described for carpals. The divergent fifthmetatarsal is short and proximally enlarged in both Tylosaurus and Hainosaurus. Thefifth metatarsal is divergent, short, proximally enlarged, but not hooked.

PlatecarpusForelimb (Fig. 6). Three stages of ossification are observed among the availablespecimens of Platecarpus. The smallest individual (Fig. 6A) has three ossified elementsidentified as the ulnare, intermedium, and distal carpal four. Intermediate sizedindividuals (Fig. 6B–D) have four ossified elements: ulnare, intermedium, and distalcarpals four and three. Larger individuals (Fig. 6E–H) have five ossified elements, butshow considerable variation regarding the identity of the fifth. The conventional fourare the ulnare, intermedium, and distal carpals four and three. The individual shownin Figure 6E bears a small element fused to the lateral margin of the fourth distalcarpal identified as the fifth distal carpal. This feature was consistent in both the rightand left carpus. In two specimens (Fig. 6F,G) the fifth ossification centre is identifiedas the radiale. This element is never very large and seldom bears finished periostealbone. A fifth ossification centre (Fig. 6H) is identified as distal carpal two. Unliketylosaurines, the early ossifying mesopodials are all moderately finished, sub-angularbones. Cartilaginous margins appear to be much smaller and a large portion of theelement surface bears finished bone. However, the fifth element to ossify, regardlessof its identity, is usually small and poorly ossified. As in other mosasaurs, the firstmetacarpal is the largest element in the metacarpal series.Rearlimb (Fig. 7). Only a single stage of ossification is observed among the availablespecimens of Platecarpus. The smallest to largest individuals (Fig. 7A–C) always havethree ossified elements: astragalus, calcaneum, and distal tarsal four. There is a largeopen space distal to the tibia and anterior to the astragalus. The fifth metatarsal isdivergent, short, proximally enlarged, and is not hooked; this is similar to Tylosaurusand Hainosaurus (Fig. 5). The fifth metatarsal presumably articulates with both thefourth distal tarsal and the calcaneum.

PlioplatecarpusForelimb. (Fig. 8A). One specimen of Plioplatecarpus has five ossified carpals identifiedas the ulnare, intermedium, and distal carpals four, three, and two. The firstmetacarpal is the largest in the series and the fifth metacarpal is small and articulatesat an acute angle with distal carpal four. A second specimen (Fig. 8B) has seven

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Figure 4. Forelimbs of tylosaurines. A, Tylosaurus sp. PU, unnumbered specimen. B, Tylosaurus proriger KUspecimen, (redrawn from Williston, 1897). C, Hainosaurus bernardi IRSNB R23 (redrawn from Nicholls,1988). D, AMNH specimen (redrawn from Osborn, 1899). E, Tylosaurus proriger. YPM 4002. Forabbreviations see Figure 3.


ossified carpals identified as the ulnare, intermedium, radiale, and distal carpals four,three, and two. The two small elements, adjacent to the base of the radius, aretentatively identified as the radiale and first distal carpal based on the topologicalrelations of these elements in other squamates. The first metacarpal is equal in sizeto the second and third. The fifth metacarpal is divergent, small, and articulates withdistal carpal four.

Ectenosaurus clidastoidesForelimb (Fig. 9). Estenosaurus clidastoides (FHM-VP 401) has six ossified elements in theright limb identified as the ulnare, intermedium, radiale, and distal carpals four,three, and two. The first metacarpal is the largest in the series; the fifth metacarpal

Figure 5. Rearlimbs of tylosaurines. (A–E) Tylosaurus. A, FHM-VP 393. B, AMNH 126. C, YPM 24919.D, AMNH specimen (redrawn from Osborn, 1899). E, FHM-VP 3. F, Hainosaurus pembinensis, MDMM74.06.06 (redrawn from Nicholls, 1988). For abbreviations see Figure 3.

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is small and bears no ossified phalanges (this limb appears to be in naturalarticulation). Seven elements are present in the left limb, but this pattern is suspectdue to obvious reconstruction. The relationships and identity of these elementscannot be relied upon.

Mosasaurines

ClidastesForelimb (Fig. 10A–C). Two stages of ossification are observed among the availablespecimens of Clidastes. There are usually seven ossified elements in the carpus (Fig.10C). These are identified as the ulnare, intermedium, radiale, distal carpals four,three, two, and the pisiform. A small, but obvious space is always present distal to theradius, proximal to metacarpal one, and anterior to the radiale. In the second stageavailable, bearing eight elements (Fig. 10A), a small, rounded, bony element is foundin this space, possibly distal carpal one.Rearlimb (Fig. 10D,E). Only a single stage of ossification is observed among theavailable specimens of Clidastes. There are three ossified elements: astragalus,calcaneum, and distal tarsal four. Unlike the condition in ‘russellosaurine’ mosasaurs

Figure 6. Forelimbs of Platecarpus. A, YPM 1254. B, NMC 40911. C, YPM 1426. D, YPM 1269. E,(reversed) FHM-VP 322. F, (reversed) YPM 1430. G, (reversed) YPM 40691. H, (reversed) KU 1001. Forabbreviations see Figure 3.


(Figs 4, 9) there is no open space distal to the tibia and anterior to the astragalus. Thefirst and second metatarsals appear to articulate directly with the tibia and astragalusrespectively; this is similar to the condition observed in extant squamates. The fifthmetatarsal is divergent, short, proximally enlarged, articulates with the calcaneumand distal tarsal four, and is not hooked; this is similar to ‘russellosaurines’.

MosasaurusForelimb (Fig. 11A,B). Only the adult stage of seven ossified elements is known forMosasaurus and these are identified as the ulnare, intermedium, radiale, distal carpalsfour, three, two, and the pisiform. Unlike Clidastes, there is no obvious space betweenthe radius, metacarpal one, and radiale. The latter element is exceptionally large.Rearlimb (Fig. 11C–E). As in Clidastes, there is only a single stage of ossificationpreserved for Mosasaurus. The smallest to largest individuals always have threeossified elements: astragalus, calcaneum, and distal tarsal four. The structure andarticular relationships of the meso- and metapodials are similar to those described forClidastes regarding the articulation of the first and second metatarsals.

Prognathodon and PlesiotylosaurusForelimb (Fig. 12A–C). Only the adult stage of ossification is known for Prognathodonand Plesiotylosaurus and is based on a small number of articulated limbs (Yang, 1983).

Figure 7. Rearlimbs of Platecarpus. A, YPM 1430. B, FHM-VP 322. C, KU 1004. For abbreviations seeFigure 3.

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From these specimens it is observed that there are at least six ossified elements in thecarpus and possibly seven depending on the presence or absence of a pisiform. Thesix commonly present are identified as the ulnare, intermedium, radiale, and distalcarpals four, three, and two.

PlotosaurusForelimb (Fig. 12D). Only the adult stage is known for Plotosaurus. Six ossified elementsare preserved in the carpus and are identified as the ulnare, intermedium, radiale,and distal carpals four, three, and two. However, Bell (1993) found a pisiform to bepresent in the left manus of LACM (CIT) 2750. As in Mosasaurus, there is no obviousspace between the radius, metacarpal one, and radiale. With the reconstruction of apisiform this limb becomes very similar in structure to that of Mosasaurus. The mostapparent differences are the morphology of the intermedium (there does not appearto be an antebrachial embayment) and the increased number of phalangeal elements(cf. Fig. 11). There is no evidence of a fifth digit.Rearlimb (Fig. 12E). There is very little preserved of the rear limb of Plotosaurus. Theonly specimen is represented by the first digit, the tibia, femur and astragalus. Whileposterior structures and relationships are unknown, the articulation and fit of thetibia, astragalus, and first metatarsal are similar to those described for Clidastes (Fig.10D,E) and Mosasaurus (Fig. 11C–F).

Figure 8. Forelimbs of Plioplatecarpus sp. A, NMC 21853. B, AMNH 14470. For abbreviations see Figure3.


DISCUSSION AND CONCLUSIONS

Ossification sequences and phylogeny

A complete ontogenetic sequence of mesopodial ossification cannot be ascertainedfor any one of the mosasaur species examined. However, it is possible to hypothesizea ‘mosasaur’ ossification sequence for the both the carpus and tarsus from the adultmorphologies and partial ontogenies described above. This is accomplished byconsidering the phylogeny of mesopodial patterns in reverse, i.e. patterns ofphylogenetic reduction as an ontogenetic sequence of mesopodial ossification (Fig.13A,B), in association with the actual ontogenetic sequences.

‘Russellosaurines’ and the Mosasaurinae show differences in the number ofterminally deleted elements that are both orderly and predictable; this allowsassessment of ontogenetic states within and between taxa. Sequences are also basedon the character states possessed by terminal taxa, by the available sequences withinseveral taxa (specifically Platecarpus and Tylosaurus), from reconstructed states forinternal nodes, and by the symplesiomorphy of these stages and sequences withstages of ossification and ossification sequences observed in three Permian diapsids(Caldwell, 1994) and in some extant squamates (Rieppel, 1992a,b,c).

The carpal ossification sequence for the Permian diapsids Thadeosaurus, Hovasaurus,

Figure 9. Forelimbs and pectoral girdle of Ectenosaurus clidastoides FHM-VP 401. For abbreviations seeFigure 3.

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and Claudiosaurus, is ulnare – distal carpal four – intermedium – lateral centrale – anddistal carpal three or one (ossification sequence of the remaining carpals is highlyvariable); the tarsal ossification sequence is astragalus/calcaneum – distal tarsal four

Figure 10. Fore- and rearlimbs of Clidastes sp. A, forelimb FM 1972.119.5F. B, forelimb YPM 1333. C,forelimb KU 1022. D, rearlimb KU 1022. F, rearlimb KU 1026. For abbreviations see Figure 3.


– distal tarsal three – centrale – and distal tarsals two, one, or five (see Caldwell,1994). The sequences reported by Rieppel (1992a,b,c) for extant squamates areconsistent with those given above for the Permian diapsids with the exception thatterminal elements in the sequence are absent in many lizards.

The inferred sequence of mosasaur carpal ossification is: ulnare – distal carpal four(dc4) – intermedium – dc3 – radiale or dc2 – dc1 or pisiform and dc5. For the

Figure 11. A, forelimb of Mosasaurus conodon. SDSM 452. B, forelimb of Mosasaurus mokoroa, DM R1535(from Welles & Gregg, 1971). C, rearlimb of ?Mosasaurus sp. UCBMP 137246 (from Yang, 1983). D,rearlimb of Mosasaurus lemmonieri IRSNB 3098 (from Dollo, 1892). E, rearlimb of Mosasaurus conodon.SDSM 452. For abbreviations see Figure 3.

424 M. W. CALDWELL

mosasaur tarsus the inferred sequence is: astragalus – distal tarsal four and/orcalcaneum.

Tylosaurines show one and two element stages for both the carpus and tarsus.Platecarpines show three, four and five element stages for the carpus and a threeelement stage in the tarsus. Five and seven element stages are known for the carpusof plioplatecarpines, and Ectenosaurus shows a six element stage of carpal ossification.

Figure 12. A, forelimb of Prognathodon sp. UCBMP 126715 (from Yang, 1983). B, forelimb of Prognathodonwaipariensis CM Zfr 108 (from Welles & Gregg, 1971). C, forelimb of Plesiotylosaurus sp. UCBMP 126716(from Yang, 1983). D, forelimb of Plotosaurus bennisoni CIT 2750 (from Camp, 1942). E, rearlimb ofPlotosaurus bennisoni CIT 2750 (from Camp, 1942). For abbreviations see Figure 3.


Figure 13. Hypothetical carpal and tarsal ossification sequences of Mosasaurs. A, carpal ossificationsequences derived from partial sequences available for Tylosaurus (first and second figures) and Platecarpus(third, fourth and fifth figures), followed by Ectenosaurus and Plioplatecarpus, and finally the seventh andeighth element stages of Clidastes. Most of the direct sequence data are available for ‘russellosaurines’;mosasaurine sequences are almost completely hypothetical. B, tarsal ossification sequences are derivedfrom Tylosaurus (first and second figures) and Mosasaurus (third figure); in this case any other mosasaur withan articulated rearlimb shows the three element stage, presumed here to be the final stage of tarsalossification. For abbreviations see Figure 3.

426 M. W. CALDWELL

Seven to eight elements in the carpus and three in the tarus characterize allmosasaurines (Clidastes, Mosasaurus etc.).

If tylosaurines have the least ossified mesopodia, and platecarpines, plioplate-carpines, ectenosaurs and mosasaurines have mesopodia where ossified elementsincrease by consistent, sequential addition from a tylosaurine-like pattern, then thelogical conclusion is that mesopodial ossification in mosasaurs proceeded from one toseven carpals and one to three tarsals (Fig. 14) in manner consistent with thesequences observed in other diapsids (Rieppel, 1992a,b,c; Caldwell, 1994). There isno reason to assume that ontogeny proceeded in any other direction than absence topresence of ossified elements; in other words, three ossified elements in the adult werenot preceded by four ossified elements in earlier ontogenetic stages where the fourthelement is lost by a process other than late stage fusion.

The distribution of adult ossification patterns, optimized on MacClade (Maddison& Maddison, 1992) and mapped onto a tree topology (Fig. 14) constructed from theconsensus trees presented above (Fig. 2A,B), and from Bell (1993; Fig. 1C), showsthat skeletal paedomorphosis was a dominant heterochronic pattern in mosasauridlimb evolution. Continued reduction of mesopodial ossification resulted in the

Figure 14. Ossified carpals and tarsals of adult mosasauroid reptiles optimized against a phylogenyconstructed from consensus trees given in Figure 2A,B, and from Bell’s (1993) preferred phylogeny (Fig.1C). ‘Russellosaurines’ and halisaurines show extreme paedomorphosis of mesopodial ossification.Mosasaurines show very limited paedomorphosis. Characters were optimized using MacClade 3.04(Maddison & Maddison, 1991) and ancestral states for internal nodes reconstructed. Numbers indicatethe number of ossified carpals and tarsals, respectively; values in parentheses indicate reconstructed statesfor internal nodes. Missing data are indicated by question marks. Values in parentheses, such as (10/7/4,5/3), indicate equivocal state reconstructions for those internal nodes; this is due to missing data.


deletion of ossified elements from the ossification sequence; this pattern characterizesmore exclusive groups within the Mosasauroidea (Fig. 14).

The exception is the eight and three combination seen in the manus and pes of themost highly ossified specimen of Clidastes (Fig. 10A, Fig. 14). The optimized adultcharacter state distributions support this condition as a reversal; heterochronically,this would be a peramorphic pattern via terminal addition. It is important to notethat the eight and three states are seen in only one individual; in all other Clidastesspecimens examined, the eighth carpal element (distal carpal one) was never foundto be ossified. It should also be noted that this specimen (Fig. 10A) is assigned toClidastes liodontus, a smaller, stratigraphically lower occurring taxon than Clidastespropython, a taxon for which only the seven and three combination is known.Therefore, the eight and three combination may be plesiomorphic for clidastinemosasaurines and is again a reversal from the natantid condition. It is also possiblethat all natantids are derived from either an eight and three combination at the nodeMosasauridae (Fig. 14), or from an unknown condition found within the equivocalreconstructed states ten/seven and five/three at the node below Mosasauridae.

Even though ontogenetic sequences are not known for aigialosaurs, themorphology of the adult carpus is found to be symplesiomorphic with that of otheranguimorphs (Caldwell et al., 1995) and more primitive diapsids (Caldwell, 1994).The existence of symplesiomorphic morphologies suggests the retention ofplesiomorphic diapsid ossification sequences (Caldwell, 1994), and, though phyloge-netically uninformative, the retention of plesiomorphic sequences is also observed inhighly derived mosasauroids such as Platecarpus (Figs 6 and 7) and Tylosaurus (Figs 4and 5). Based on the symplesiomorphies of conserved lepidosauromorph sequences(Caldwell, 1994), mosasaur apomorphies include variations on the degree ofossification, the number of ossified elements, and the number of terminal deletionsin the digital arch sequences.

The derived limbs of halisaurines, as described for the only known specimen withan articulated forelimb (Fig. 3), can only be considered relative to the Natantia, (Fig.14), not aigialosaurs. The reduction of ossified elements in the carpus of Halisaurussternbergi, from ten to four (the tarsus is unknown), defines the halisaurine conditionat the node Mosasauridae. This reduction is supported as a synapomorphy ofhalisaurines in the same way that the reduction from ten to seven carpals and five tothree tarsals is supported as a synapomorphy of the Natantia. The halisaurinecondition should not be interpreted as a rapid loss of carpal ossifications in a stem-group mosasaur. This character (four ossified carpals), despite missing informationfor other OTUs, can only be considered a synapomorphy of halisaurines until furtherevidence is collected. The halisaurine carpus of four elements is found to correspondto the four element stage of Platecarpus and the four element stage of the hypotheticalsequence (Fig. 13A). The difficulty in interpreting the condition of the halisaurinecarpus is that there is no comparative basis for knowing the relative stage ofossification this individual has achieved. It is a large specimen and is doubtless anadult, as are all other mosasaurs described in this study. However, there is nocomparison possible with other halisaurines, nor even with the hindlimb, todetermine whether four ossified mesopodials was the terminal stage or a midpoint asseen in platecarpines (Fig. 6).

Reduction of ossified mesopodials, producing apparent terminal deletions alongthe digital arch sequence, are apomorphic for various clades within the Mosasaur-idae (Fig. 14). The character states differ between halisaurines and natantids

428 M. W. CALDWELL

(mosasaurines and ‘russellosaurines’) in the degree of reduced ossification. Moreexclusive clades within ‘russelosaurines’, specifically the tylosaurines, are charac-terized by highly reduced sequences. It is interesting to note that mosasaurines showlittle change from the hypothesized mosasaurid or mosasauroid plesiomorphic state(ten to eight or seven carpals, and five to three tarsals).

The mesopodial ossification patterns described above are equally ‘congruent’ withboth the phylogenetic hypothesis of Bell (1993) and that of deBraga & Carroll (1993).However, character analysis of individual elements (see above descriptions and Fig.12A,B) require homoloplasious distributions for all limb characters of Prognathodonand Plesiotylosaurus if the reconstruction of this clade within plioplatecarpines isaccepted, as has been proposed by deBraga & Carroll (1993).

The ingroup relationships of aigialosaurs are still poorly resolved (Figs 1C, 2A,B)but this does not affect the distribution of ontogenetic limb characters with currentmosasauroid phylogeny. Aigialosaurs retain the plesiomorphic squamate sequence,while mosasaur clades show derived states regarding the degree of ossification andtermination of ossification sequences.

Skeletal paedomorphosis

The distribution of mesopodial ossification patterns among the Mosasauridae, ascompared to the sistergroup condition of aigialosaurs, supports the conclusion thatthe evolution of mosasaur limbs was significantly influenced by skeletal paedomor-phosis. Paedomorphic reductions of limb ossification take several forms in mosasaurs:reduction in the number of elements (spatial); reduction in degree of ossification(temporal); retention of the paedomorphic state of perichondral ossification vs.endochondral ossifications; retention of juvenile chondrocyte to osteocyte ratios(Sheldon, 1994; Sheldon et al., 1994).

Compared to aigialosaurs or varanoid anguimorphs, mosasaurs have fewerossified carpal and tarsal elements. Unfortunately, it is not possible to determinewhether cartilage precursors of the ‘missing’ bones have been lost or simply did notossify. Comparisons between ‘russelosaurines’ and mosasaurines, or betweentylosaurs and platecarpines-plioplatecarpines (Fig. 14), show that in those taxapossessing a larger complement of ossified elements, the cartilage precursors for 7 to8 elements are present; this would suggest that in those clades with fewer elements,the cartilaginous precursors for at least the 7 to 8 elements were present. However,arguments in favour of the retention of the cartilage precursors can only be made asarguments based on the phylogenetic distribution of ossified elements.

For some elements, such as those never represented as ossified structures inmosasaurs, i.e. the centrale series, plesiomorphically present in basal diapsids(Caldwell, 1994), it is possible that evolutionary loss of the cartilage element hasoccurred. Such loss would be a synapomorphy of the Mosasauridae. Ossifiedcentrale elements present in aigialosaurs and other lizards indicates plesiomorphicretention of the cartilage precursors to at least these branching points in mosasauroidphylogeny. Assuming that mosasaurs had similar patterns of chondrogenesis as havebeen reported for many tetrapods (Shubin & Alberch, 1986), at the chondrogenicstage of development, the centrale element(s) either did not form, were resorbed insome manner, or else were fused to proximal or distal mesopodials prior toossification.


Sheldon (1994) and Sheldon et al. (1994), provide histological data indicative oflarge scale heterochronic changes in the mode and degree of ossification of ribs andsome long bones in mosasaurs. These histological features include both an increasedpercentage of cartilaginous matrix, as well as differences in the type of perichondraland endochondral bone, present in adult bone. These modifications are mostpronounced in ‘russellosaurines’, and more specifically tylosaurs, and wereinterpreted as skeletal paedomorphosis. Endochondral osteogenesis involves complextemporal and spatial controls over the replacement and differentiation ofperichondral and endochondral tissues (Wolpert & Tickle, 1993; Wozney, Cappar-ella, & Rosen, 1993). Paedomorphosis, in the form of neoteny, might involve thetruncation of endochondral osteogenesis resulting in the retention of chondrocytes inendochondral bone matrix; the proportion of chondrocytes would be similar to adevelopmental stage of osteogenesis in juveniles of a sistergroup.

Mosasaur astragalus

In younginiforms and claudiosaurids the astragalus and calcaneum are distinctstructures in both juveniles and adults; fusion into a single proximal tarsal bone, asseen in extant lizards, never occurs (Caldwell, 1994). The absence of fusion of theseelements, at any of the known stages in ontogeny, in association with the presence ofa large foramen between them that permits passage of the perforating artery,suggests that the astragalus and calcaneum of early diapsids developed fromindependent cartilaginous elements.

In extant lizards, a single ossified element, referred to as the astragalocalcaneum,occupies the proximal tarsal row (Rieppel, 1993). This single element results from thefusion of two centres of ossification, referred to the astragalar and calcaneal centres,that form within a single proximal tarsal cartilage. The astragalus ossifiesendochondrally from a single centre located in the intermedium position of thisproximal tarsal cartilage (Sewertzoff, 1908; Rieppel, 1992a,b,c), while the calcaneumbegins endochondral ossification within the cartilage distal to the fibula and lateralto the astragalus. As these independent ossification centres increase in size theyeventually come into contact. Later in ontogeny these elements fuse so that onlyminor traces of the fusion line can be determined (pers. observ.). The perforatingartery does not pass through either the single proximal cartilage or theastragalocalcaneum, but rather follows a groove over the proximal portion of theastragalus and through the antebrachial space.

There are two elements in the proximal tarsal row of mosasaurs: the astragalusand calcaneum (Figs 7, 10 and 12). In only a few platecarpines was it apparent thatvery limited fusion of these two tarsals had occurred and sutures were verypronounced in the few showing fusion (Fig. 15). The degree of completion ofendochondral and perichondral ossification in the astragalus and calcaneum wasvery poor with surface bone often present as a small disc restricted to the middle ofthe element, and with poorly finished endochondral margins. These poorly finishedmargins suggest contact with a large cartilage border.

Comparison of the mosasaur astragalus and calcaneum with the ossified elementsfound in the single proximal cartilage of extant squamates at various ontogeneticstages (Rieppel, 1992a,b), shows remarkable similarities in the shape of the elementand the position of ossification (Fig. 15). Articulated mosasaur hindlimbs show very

430 M. W. CALDWELL

clearly that the astragalus ossified from a single centre in the intermedium positionof the proximal tarsus, while the calcaneum also ossified from a single centre beneaththe fibula. In even the most poorly ossified astragali there is a groove on the proximaledge, where the element forms the distal margin of the antebrachium, for passage ofthe perforating artery. This feature is present in all mosasaur taxa (Fig. 15) and in allextant lizards.

Though cartilage elements are not preserved, it is reasonable to conclude, bycongruence of characters, that a single proximal cartilage was present in mosasaursand that the astragalus and calcaneum ossified from single centres within thatcartilage. The existence of fused proximal tarsal bones, though limited, and the factthat the perforating artery passes through the antebrachium, not between theastragalus and calcaneum as seen in more primitive diapsids (Caldwell, 1994), lendssupport to this conclusion.

Skeletal paedomorphosis in mosasaurs does not appear to have altered the earlierontogenetic condition of the single proximal tarsal cartilage. There is no‘recapitulation’ of the independent cartilaginous centres found in more primitivediapsids. The heterochronic effects observed in mosasaurs appear to have altered thetiming and duration of ossification in the mesopodium. There is no evidence, at leastin terms of the astragalus, for assuming that there were alterations of earlier patternformation involving cartilaginous elements.

ACKNOWLEDGEMENTS

For assistance while gathering of data on mosasauroids reptiles I want to thank C.Holton, D. Brinkman, S. Chapman, J. Chorn, A. Currant, F. Crompton, J. Martin,

Figure 15. Morphology of the astragalus in mosasaurs, and the calcaneum of Platecarpus, A&B, Platecarpussp., YPM 55712; A, flexor view, right astragalo-calcaneum; B, proximal view, right astragalus. C&D,Tylosaurus sp., YPM 24908; C, extensor view; D, flexor view. E, Clidastes unnumbered KU specimen. F,Mosasaurus conodon SDSM 452. Arrows indicate the position of the groove for the perforating artery (grpa). Scale bar (1 cm) applies A–E; 5 cm scale bar applies to F. For abbreviations see Figure 3.


L. Martin, A. Neuman, B. Nicholls, V. Sowiak, J. Storer, T. Tokaryk, M. Turner,and R. Zachevsky. I thank R. Carroll, and M. Wilson for extremely useful criticismsof various drafts of this paper. I thank O. Rieppel, G. Bell, and an anonymousreviewer for valuable criticisms. In particular I wish to thank M.V.H. Wilson for theuse of his laboratory space while I finished the writing of this paper and of my thesis.The research presented here was supported by a Natural Sciences and EngineeringResearch Council of Canada (NSERC) Post Graduate Scholarship to M.W.Caldwell, and by NSERC operating grants to R. Carroll.

REFERENCES

Bell GL. 1993. A phylogenetic revision of Mosasauroidea (Squamata). Ph.D. dissertation, University of Texas,Austin, Texas, 293 pp.

Caldwell MW. 1994. Developmental constraints and limb evolution in Permian and modern lepidosauromorphdiapsids. Journal of Vertebrate Paleontology 14: 459–471.

Caldwell MW, Carroll RL, Kaiser H, 1995. The pectoral girdle and forelimb of Carsosaurus marchesetti(Aigialosauridae), with a preliminary phylogenetic analysis of mosasauroids and varanoids. Journal of VertebratePaleontology 15: 516–531.

Camp CL. 1942. California Mosasaurs. Memoirs of the University of California 13: 1–68.Carroll RL, deBraga M. 1992. Aigialosaurs: Mid-Cretaceous varanoid lizards. Journal of Vertebrate Paleontology 12:

66–86.DeBraga M, Carroll RL. 1993. The origin of mosasaurs as a model of macroevolutionary patterns and processes.

Evolutionary Biology 27: 245–322.Dollo L. 1892. Nouvelle note sur L’Osteologie des Mosasauriens. Bulletin de la Societe Belge de Geologie de Paleontologie

et d’Hydrologie (Bruxelles) 7: 219–259.Kornhuber AG. 1893. Carsosaurus marchesetti, ein neuer fossiler Lacertilier aus den Kreideschichten des Karstes bei

Komen. Abhandlungen der geologischen Reichsanstalt Wien 17: 1–15.Kornhuber AG. 1901. Opetiosaurus bucchichi, eine neue fossile Eidechse aus der unteren Kreide von Lesina in

Dalamtien. Abhandlungen der geologischen Reichsanstalt Wien 17: 1–24.Kramberger KG. 1892. Aigialosaurus, eine neue Eidechse aus den Kreideschiefern der Insel Lesina mit Rucksicht

auf die bereits beschriebenen Lacertiden von Comen und Lesina. Glasnik Hrvatskoga Naravoslovnoga Drustva (SocietasHistorico-Naturalis Croatica) u Zagrebu 7: 74–106.

Maddison WP, Maddison DR. 1992. MacClade: Analysis of phylogeny and character evolution. Version 3. Sunderland,Massachusetts: Sinauer Associates.

McDowell SB, Bogert CM. 1954. The systematic position of Lanthanotus and the affinities of the anguimorphlizards. Bulletin of the American Museum of Natural History 105: 1–142.

Nicholls EL. 1988. The first record of the mosasaur Hainosaurus (Reptilia: Lacertilia) from North America. CanadianJournal of Earth Sciences 25: 1564–1570.

Osborn HF. 1899. A complete Mosasaur skeleton, osseous and cartilaginous. Memoirs of the American Museum ofNatural History 1: 167–188.

Patterson C. 1982. Morphological characters and homology. In: Joysey KA, Friday AE, eds. Problems of phylogeneticreconstruction Vol. 21. New York: Academic Press, 21–74.

Rieppel O. 1992a. Studies on skeleton formation in reptiles. I. The postembryonic development of the skeletonin Cyrtodactylus pubisulcus (Reptilia, Gekkonidae). Journal of Zoology, London 227: 87–100.

Rieppel O. 1992b. Studies on skeleton formation in reptiles. III. Patterns of ossification in the skeleton of Lacertavivipara Jacquin (Reptilia, Squamata). Fieldiana Zoology, New Series 68: 1–25.

Rieppel O. 1992c. The skeleton of a juvenile Lanthanotus (Varanoidea). Amphibia-Reptilia 13: 27–34.Rieppel O. 1993. Studies on skeleton formation in reptiles. IV. The homology of the reptilian (amniote) astragulus

revisited. Journal of Vertebrate Paleontology 13: 31–47.Russell DA. 1967. Systematics and morphology of North American Mosasaurs. Bulletin of the Peabody Museum of

Natural History, Yale University 23: 1–241.Sewertzoff AN. 1908. Studien uber die Entwicklung der Muskeln, Nerven und des Skeletts der Extremitaten der

niederen Tetrapoda. Bulletin de la Societe Imperiale des Naturalistes de Moscou, Annee 1907. 21: 1–430.Sheldon AS. 1994. Ecological implications of mosasaur bone microstructure. Abstracts of Papers, 54th Annual

Meeting of the Society of Vertebrate Paleontology, Journal of Vertebrate Paleontology 14: 45A.Sheldon AS, Williams M, Bell GL, Donachy J. 1994. Microstructural and biochemical analysis of mosasaur

bone. Abstracts of Papers, 52nd Annual Meeting of the Society of Vertebrate Paleontology, Journal of VertebratePaleontology 14: 45A.

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Shubin NS, Alberch P. 1986. A morphogenetic approach to the origin and basic organization of the tetrapodlimb. In: Hecht MK, Wallace B, Prance GT, eds. Evolutionary Biology, Volume 20. New York and London:Plenum Press, 319–387.

Swofford DL. 1993. PAUP: Phylogenetic Analysis Using Parsimony, Version 3.1.1. Computer program distributed by theIllinois Natural History Survey, Champaign, Illinois.

Welles SP, Gregg DR. 1971. Late Cretaceous marine reptiles of New Zealand. Records of the Canterbury Museum 9:1–111.

Williston SW. 1897. On the extremities of Tylosaurus. Kansas University Quarterly 6: 99–102.Wiman C. 1920. Some reptiles from the Niobrara Group of Kansas. Bulletin of the Geological Institute of Uppsala 18:

11–18.Wolpert L, Tickle C. 1993. 14. Pattern formation and limb morphogenesis. In: Bernfield M, ed. Molecular Basis

of Morphogenesis. New York: Wiley-Liss, Inc., 207–219.Wozney JM, Capparella J, Rosen V. 1993. 15. The bone morphogenetic proteins in cartilage and bone

development. In: Bernfield M, ed. Molecular Basis of Morphogenesis. New York: Wiley-Liss, Inc., 221–230.Yang D. 1983. A study of the pectoral and pelvic appendages of California Mosasaurs. Unpublished Masters

Thesis, California State University, Fresno, 65 pp.

APPENDIX I

Data matrix and character descriptions for Mosasauroidea as revised from Bell (1993).Sixty of Bell’s 151 characters were deleted from this analysis as they were either invariant or uninformative

(Characters 3, 6, 10, 12, 18–20, 22, 29, 32, 35, 36, 45, 48, 51, 53, 55, 56, 60, 61, 64, 65, 68, 72, 73, 76, 78–80, 84,87–89, 92, 95, 97, 102–105, 107, 112–114, 117, 119, 120, 127, 128, 131, 134, 135, 143–149, and 151). Thecharacter states for characters 74 and 96 were recoded from Bell (1993) as some states did not apply to the reducedterminal taxa. Specific characters and character states were recoded based on examination of latex peels andphotographs of the type specimens of Aigialosaurus buccichi (NMW specimen and Kornhuber [1901]), Aigialosaurusdalmaticus (BSP 1902II501 and Kramberger [1892]), and Carsosaurus marchesetti (MCSNT unnumbered specimen andMCSNT 11430, 11431, 11432 [in three parts], and Kornhuber [1893]). The character number in brackets refer tothe character number as listed in Bell (1993). Altered states are as follows:


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Character descriptions1(1). Bony predental rostrum on premaxilla: absent (0); present (1).2(2). Size of bony predental rostrum on premaxilla: short and obtuse (0); distinctly protruding (1).3(4). Premaxillary rostral foramen size: small (0); large (1).4(5). Width of premaxillary internarial bar: narrow (0); wide (1).5(7). Dorsal keel of premaxillary internarial bar: absent (0); present (1).6(8). Entrance of Vth cranial nerve on internarial bar of premaxilla: close to rostrum (0); far removed from

rostrum (1).7(9). Premaxillary tooth count: more than four (0); only four (1).

8(11). Nasal bones: present (0); absent (1).9(13). Width of internarial process of frontal: not constricted (0); very constricted (1).

10(14). Frontal width: broad and short (0); long and narrow (1).11(15). Narial emargination of frontal: not invaded by posterior nares (0); embayment of frontal present (1).12(16). Sagittal dorsal keel on frontal: absent (0); low and inconspicuous (1); high, thin and well developed

(2).13(17). Shape of frontal ala: sharply accuminate (0); broadly pointed and rounded (1).14(21). Fronto-parietal suture: low interlocking ridges from each (0); overlapping flanges (1).15(23). Frontal invasion of parietal: posteriorly extended lateral sutural flange (0); posteriorly extended median

frontal sutural flange (1); both present (2).16(24). Frontal medial invasion of parietal: posteriorly extended median sutural ridge short (0); same but long

(1).17(25). Length of parietal: dorsal surface short (0); dorsal surface elongate (1).18(26). Shape of parietal table: rectangular to trapezoidal with convergent sides (0); triangular with straight sides

contacting anterior to suspensorial rami (1).19(27). Parietal foramen size: small (0); large (1).20(28). Position of parietal foramen: near to center of parietal table (0); close to suture (1); touching suture (2);

straddles suture invading frontal (3).21(30). Parietal posterior shelf: distinct shelf projecting posteriorly between suspensorial rami (0); shelf absent

(1).22(31). Parietal suspensorial ramus greatest width: vertical or oblique (0); horizontal (1).23(33). Prefrontal suborbital process:process absent or a small knob (0); large overhanging wing (1).24(34). Prefrontal contact with postorbital frontal: no contact at edge of frontal (0); elements in contact at edge

of frontal (1).25(37). Postorbitofrontal: without low, rounded, transverse dorsal ridge (0); with dorsal ridge (1).26(38). Postorbitofrontal squamosal ramus: does not reach end of supratemporal fenestra (0); does reach end of

ramus (1).27(39). Maxillary tooth count: 20 to 24 (00; 17–19 (1); 15–16 (2); 14 (3); 13 (4); 12 (5).28(40). Posterior terminus of maxillo-premax suture: anterior or even with midline of fourth maxillary tooth (0);

between fourth and ninth tooth (1); even with or posterior to ninth tooth (2).29(41). Posterodorsal process of maxilla: recurved wing of maxilla dorsolaterally overlaps a portion of the

anterior end of prefrontal (0); no recurved posterodorsal process present (1).30(42). Posterodorsal extent of maxilla: recurved wing of maxilla prevents prefrontal emargination on lateral

edge of narial opening (0); does not prevent emargination (1).31(43). Angle of posteroventral margin of jugal: very obtuse or curvilinear (0); near 120 degrees (1);

approximately 90 degrees (2).32(44). Posteroventral process of jugal: absent (0); present (1).33(46). Pterygoid tooth row: teeth arise from main shaft of pterygoid (0); teeth arise from thin pronounced ridge

(1).34(47). Pterygoid tooth number: 12 or less (0); more than 12 (1).35(49). Length of quadrate stapedial process: short (0); moderate length (1); long (2).36(50). Constriction of quadrate stapedial process: distinct (0); none (1).37(52). Fusion of quadrate stapedial process to ventral process: absent (0); present (1).38(54). Quadrate stapedial pit shape: oval to circular (0); narrow oval (1); elongate with constricted middle

(2).39(57). Thickness of quadrate ala: thin (0); thick (1).40(58). Quadrate conch: ala and main shaft describe a deep bowl (0); alar concavity shallow (1).41(59). Quadrate ala shape: anterodorsal segment of tympanic rim more tightly curved than rest of rim (0); or

rim curve uniformly circular (1).42(62). Quadrate ala groove: no groove in anterolateral edge of ala (0); long distinct groove (1).43(63). Quadrate tympanic rim size: large, almost as high as quadrate (0); smaller, 50–65% of quadrate height

(1).44(66). Quadrate ventral median ridge: single thin ridge (0); thin ridge diverging ventrally (1).45(67). Quadrate ventral condyle: condyle saddle-shaped, concave anteroposterior view (0); condyle gently

domed, convex in any view (1).


46(69). Quadrate anteroventral condyle modification: no upward deflection of anterior edge of condyle (0);distinct deflection (1).

47(70). Basisphenoid pterygoid process shape: process relatively narrow with articular surface facing mostlyanterolaterally (0); process thinner, more fan-shaped with posterior extension of articular surface (1).

48(71). Basioccipital tubera size: short (0); long (1).49(74). Dentary tooth number: 20 to 24 or more (0); 15 to 16 (1); 14 (2); 13 (3).50(75). Anterior projection of dentary: projection of bone anterior to first tooth present (0); absent (1).51(77). Medial parapet of dentary: median subdental shelf low (0); shelf elevated and straplike (1); equal in

height to lateral wall (2).52(81). Coronoid shape: with slight dorsal curvature, posterior wing not wide fan-shape (0); very concave above,

posterior wing expanded (1).53(82). Coronoid posteromedial process: present (0); absent (1).54(83). Coronoid medial wing: does not reach angular (0); contacts angular (1).55(85). Surangular-coronoid buttress: low, thick, and parallel to lower edge of mandible (0); high, thin, rapidly

rising anteriorly (1).56(86). Surangular-articular suture position: behind condyle in lateral view (0); at middle of glenoid on lateral

edge (1).57(90). Foramina on lateral aspect of retroarticular process: none (0); one to three (1).58(91). Tooth surfaces: teeth finely striate medially (0); not striated medially (1).59(93). Tooth facets: no facets (0); with facets (1).60(94). Tooth fluting: no fluting (0); numerous broad flutes (1).61(96). Tooth carinae: present but weak (0); strong and elevated (1).62(98). Tooth replacement mode: in shallow excavations (0); in subdental crypts (1).63(99). Atlas neural arch: notch in anterior border (0); no notch (1).

64(100). Atlas synapophysis: extremely reduced (0); large and elongate (1).65(101). Zyosphenes and zygantra: absent (0); present (1).66(106). Cervical synapophysis ventral extension: extend slightly or not all below ventral margin of centrum (0);

far below ventral margin (1).67(108). Trunk vertebrae condyle inclination: inclined (0); vertical (1).68(109). Condyle shape: extremely dorsoventrally depressed (0); slightly depressed (1); rounded (2).69(110). Posterior trunk condyle shape: not higher than wide (0); slightly compressed (1).70(111). Dorsal ridge of posterior vertebral synapophysis connecting with zygapophysis: no sharp ridge making

connection (0); sharp ridge makes connection (1).71(115). Number of sacral vertebrae: two (0); one (1).72(116). Neural spines of caudal vertebrae: uniformly shortened posteriorly (0); several spines dorsally elongated

in mid-tail region (1).73(118). Haemal arch articulation: articulate (0); fused (1).74(121). Scapula-Coracoid size: bone approximately equal in proximo-distal length (0); scapula about half length

of coracoid (1).75(122). Scapula width: no anteroposterior widening (0); distinct fan-shaped expansion (1); extreme widening

(2).76(123). Scapula dorsal margin convexity, if widened: very convex (0); or broadly convex (1).77(124). Scapula posterior emargination: gently concave (0); deeply concave (1).78(125). Scapula-coracoid fusion: bones fused (0); not fused (1).79(126). Scapula-coracoid suture in unfused state: interdigitate suture (0); flat, no interdigitation (1).80(129). Humerus length relative to distal width: elongate, 3 to 4 (0); shortened, 1.5 to 2 (1); length and width

equal (2); distal width greater (3).81(130). Humerus postglenoid process: absent or very small (0); distinctly enlarged (1).82(132). Humerus deltopectoral crest: single ridge (0); two separate insertion areas (1).83(133). Humerus pectoral crest: located anteriorly (0); located medially (1).84(136). Humerus entepicondyle: absent (0); present as a prominence (1).85(137). Radius shape: radius not expanded (0); slightly expanded (1); broadly expanded (2).86(138). Ulna contact with centrale: excluded by broad ulnare (0); contacts centrale (1).87(139). Radiale size: large and broad (0); reduced or absent (1).88(140). Carpal reduction: size or more (0); five or less (1).89(141). Pisiform: present (0); absent (1).90(142). Metacarpal I expansion: spindle shaped, elongate (0); broadly expanded (1).91(150). Appendicular epiphyses: formed from ossified cartilages (0); from thick unossified cartilage (1); missing

or extremely thin (2).

436 M. W. CALDWELL

Documents

Caldwell, 1996