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CO 2 ^^5' ^v >: TUTION *^N0liniIlSNI_NVIN0SHlllMS*^S3 I yV8 a I l^L I B R AR I ES*^SMITHSONlAN INSTITUTION '^NOIini ^ CO ^ z \ ■ ^'^ ^ 5 c'J 5 ^ QL 66fi L25U4 1987X Rept. iiversity of California Publications ZOOLOGY Volume 118 Phylogenetic Systematics of Iguanine Lizards A Comparative Osteological Study by Kevin de Queiroz PHYLOGENETIC SYSTEMATICS OF IGUANINE LIZARDS A COMPARATIVE OSTEOLOGICAL STUDY KEPT. Phylogenetic Systematics of Iguanine Lizards/ A Comparative Osteological Study by Kevin de Queiroz A Contribution from the Museum of Vertebrate Zoology of the University of California at Berkeley yti»%K«^*^ UNIVERSITY OF CALIFORNIA PRESS Berkeley • Los Angeles • London UNIVERSITY OF CALIFORNIA PUBLICATIONS IN ZOOLOGY Editorial Board: Peter B. Moyle, James L. Patton, Donald C. Potts, David S. Woodruff Volume 118 Issue Date: December 1987 UNIVERSITY OF CALIFORNIA PRESS BERKELEY AND LOS ANGELES, CALIFORNIA UNIVERSITY OF CALIFORNIA PRESS, LTD. LONDON, ENGLAND ISBN 0-520-09730-0 LIBRARY OF CONGRESS CATALOG CARD NUMBER: 87-24594 © 1987 BY THE REGENTS OF THE UNIVERSITY OF CALIFORNIA PRINTED IN THE UNITED STATES OF AMERICA Library of Congress Cataloging-in-Publication Data De Queiroz, Kevin. Phylogenetic systematics of iguanine lizards: a comparative osteological study / by Kevin de Queiroz. p. cm. — (University of California publications in zoology: v. 118) Bibliography: p. ISBN 0-520-09730-0 (alk. paper) 1. Iguanidae — Classification. 2. Iguanidae — Evolution. 3. Iguanidae — ^Anatomy. 4. Anatomy, Comparative. 5. Reptiles — Qassification. 6. Reptiles — Evolution. 7. Reptiles — Anatomy. I. Title. II. Series. QL666.L25D4 1987 597.95— dc 19 87-24594 CIP Contents Li^f of Illustrations, vii List of Tables, x Acknowledgments, xi Abstract, xii INTRODUCTION 1 Historical Review, 1 Goals of This Study, 10 MATERIALS AND METHODS 1 3 Specimens, 13 Phylogenetic Analysis, 13 Basic Taxa, 14 The Problem of Variation, 14 Construction of Branching Diagrams, 16 IGUANINE MONOPHYLY 18 COMPARATIVE SKELETAL MORPHOLOGY 2 1 Skull Roof, 21 Palate, 39 Braincase, 44 Mandible, 49 Miscellaneous Head Skeleton, 59 Axial Skeleton, 69 Pectoral Girdle and Sternal Elements, 81 Pelvic Gridle, 86 Limbs, 89 Osteoderms, 89 NONSKELETAL MORPHOLOGY 92 Arterial Circulation, 92 Colic Anatomy, 93 External Morphology, 94 vi Contents SYSTEMATIC CHARACTERS 100 Skeletal Characters, 100 Nonskeletal Characters, 104 CHARACTER POLARITIES AND THE PHYLOGENETIC INFORMATION CONTENT OF CHARACTERS 1 06 ANALYSIS OF PHYLOGENETIC RELATIONSHIPS 1 17 PreHminary Analysis, 1 17 Lower Level Analysis, 122 PHYLOGENETIC CONCLUSIONS 130 Preferred Hypothesis of Relationships, 130 Character Evolution within Iguaninae, 130 COMPARISONS WITH PREVIOUS HYPOTHESES 132 DIAGNOSES OF MONOPHYLETIC GROUPS OF IGUANINES 135 Iguaninae Bell 1825, 135 Dipsosaurus Hallowell 1854, 141 Brachylophus Wagler 1830, 143 Iguanini Bell 1825, 145 Ctenosaura Wxtgmonn 1828, 146 Sauromalus T)\xvi\€n\ 1856, 157 Amblyrhynchina, new taxon, 160 Amblyrhynchus Bell 1825, 163 Conolophus Fitzinger 1843, 165 IguaninaBell 1825, 167 Iguana Laurenti 1768, 168 Odwra Harlan 1824,170 Appendix I: Specimens Examined, 175 Appendix II: Polarity Determination Under Uncertain Outgroup Relationships, 179 Appendix III: Polarity Determination for Lower Level Analysis, 185 Appendix IV: Polarity Reevaluation for Lower Level Analysis, 187 Literature Cited, 191 List of Illustrations FIGURES 1 . "The phylogeny and relationships of North American iguanid genera," after Mittleman (1942), 6 2. "Grouping and possible phylogeny of the genera of iguanids occurring in the United States," after H. M. Smith (1946), 7 3. "Phylogenetic relationships of the Madagascar Iguanidae and the genera of iguanine Hzards," after Avery and Tanner (1971), 9 4. Etheridge's phylogeny of the Iguanidae, 1 1 5. Skull of Brae hy lop hus vitiensis, 22 6. Skull and mandible of Brae hy lop hus vitiensis, 23 7. Posteroventral views of iguanine premaxillae, 24 8. Dorsal views of the preorbital portions of iguanine skulls, 25 9. Dorsal views of the skulls of Cyclura cornuta and Sauromaliis obesus, 11 10. Posterodorsal views of the anterior orbital regions oi Brachylophus fasciatm and Conolophus pallidus, 28 11. Dorsal view of the skull of Amblyrhynchus cristatus, 29 12. Ventral views of iguanine frontals, 31 13. Dorsal views of the parietals in an ontogenetic series of Iguana iguana, 34 14. Lateral view of the skull of Ctenosaura similis, 36 15. Lateral views of the posterolateral comers of iguanine skulls, 38 16. Posterodorsal views of disarticulated right palatines of Iguana delicatissima and Conolophus subcristatus, 40 17. Posterodorsal views of the right orbits of five iguanines and Morunasaurus annularis, 41 18. Ventral view of the skull of Iguana delicatissima, 43 19. Anterolateral views of the left orbitosphenoids in an ontogenetic series of Iguana iguana, 45 20. Ventral views of the posterior portion of the palate and anterior portion of the braincase of Sauromalus varius and Amblyrhynchus cristatus, 46 21. Ventral views of iguanine neurocrania, 47 22. Lateral views of the right mandibles of Iguana delicatissima and Amblyrhynchus cristatus, 50 23. Lingual views of the left mandibles of three iguanines, 51 24. Lateral views of the right mandibles of Conolophus pallidus and Cyclura cornuta, 52 vu viii List of Illustrations 25. Lateral views of the right mandibles of Iguana delicatissima, Sauromalus obesus, and Amblyrhynchus cristatus, 53 26. Lateral views of the right mandibles of Dipsosaurus dorsalis, Brachylophus vitiensis, and Iguana iguana, 55 27. Medial views of the left mandibles of Iguana delicatissima and Conolophus subcristatus, 56 28. Dorsal views of the posterior ends of the right mandibles in ontogenetic series of Ctenosaura hemilopha and Amblyrhynchus cristatus, 57 29. Dorsal views of the posterior ends of the right mandibles in an ontogenetic series of Dipsosaurus dorsalis, 58 30. Lingual views of left maxillary teeth of four iguanines and Basiliscus plumifrons, 62 31. Hypothetical character phylogeny for the iguanine pterygoid tooth patch, 65 32. Corneal view of the left scleral ring of Ctenosaura similis, 67 33. Ventral views of the iguanine hyoid apparati, 68 34. Twentieth presacral vertebra of Brachylophus vitiensis, 70 35. Lateral views of the twentieth presacral vertebrae of Sauromalus obesus and Ctenosaura pectinata, 11 36. Dorsolateral views of the twentieth presacral vertebrae of Dipsosaurus dorsalis and Sauromalus obesus, 73 37. Dorsal views of caudal vertebrae of Dipsosaurus dorsalis from different regions of the tail, 76 38. Lateral views of the ninth caudal vertebrae of Dipsosaurus dorsalis and Iguana iguana, 79 39. Presacral and sacral vertebrae and ribs of Dipsosaurus dorsalis in ventral view, 80 40. Pectoral girdles of three iguanines, 82 41. Dorsal views of the pelvic girdles of Sauromalus obesus and Ctenosaura pectinata, 86 42. Bones of the anterior limb of Brachylophus fasciatus, 87 43. Right hind limb skeleton of Brachylophus fasciatus, 88 44. Right tarsal region of Brachylophus fasciatus, 90 45. Anterodorsal views of pedal digit II of three iguanines, 97 46. Minimum-step cladograms for eight basic taxa of iguanines resulting from a preliminary analysis of 29 characters, 119 47. Alternative interpretations of character transformation for homoplastic characters on a minimum-step cladogram, 121 48. Alternative interpretations of character transformation for homoplastic characters on a minimum-step cladogram, 122 49. Minimum-step cladograms resulting from an analysis of 26 characters in a subset of iguanines, 127 50. Consensus cladogram for the three cladograms illustrated in Figure 49, 128 51. Phylogenetic relationships within Iguaninae, according to the present study, 131 52. Geographic distribution of Di/?^o^aMrM5, 141 53. Geographic distribution of firacA}'/<9/p/zM5', 144 List of Illustrations ix 54. Geographic distribution of CreAio5flMra, 147 55. Cladogram illustrating phylogenetic relationships within Ctenosaura, 154 56. Geographic distribution of Sawroma/t^, 158 57. Geographic distribution of Amblyrhynchina {Amblyrhynchus and Conolophus), 161 58. Geographic distribution of /^Mana, 169 59. Geographic distribution of C}'c/Mra, 171 60. All nine possible fully resolved cladogram topologies for four unspecified outgroups and an ingroup, 179 61. Dendrograms corresponding with the nine cladograms in Figure 60 after each is rerooted at the outgroup node, 180 62. Examples of polarity inferences for different arrangements of outgroup character state distributions, 182 63. All possible cladogram topologies for two unspecified outgroups and an ingroup before and after rerooting at the outgroup node, 185 64. All possible cladogram topol9gies for two unspecified near outgroups, one more remote outgroup, and an ingroup before and after rerooting at the outgroup node, 186 PLATE 1. Lateral and dorsal views of the skull oi Amblyrhynchus cristatus, 91 List of Tables 1 . The iguanine genera, 2 2. Position of the parietal foramen, 32 3. Numbers of premaxillary teeth, 60 4. Numbers of presacral vertebrae, 7 1 5. Distributions of character states of 95 characters among four outgroups to iguanines and the polarities that can be inferred from them, 108 6. Distributions of character states of 95 characters among eight iguanine taxa, 112 7. Distributions of character states of 29 characters used in the preliminary analysis, 118 8. Polarity inferences for lower-level analysis, using Brachylophus and Dipsosaurus as outgroups, 124 9. Distributions of character states of 26 characters among six taxa within Iguanini, 125 10. Distributions of character states of 19 characters among basic taxa within Ctenosaura (in the broad sense) and three close and two more distant outgroups, 153 11. Summary of polarity inferences for seven cases of character-state distribution among four outgroups of uncertain relationships to the ingroup, 181 12. Summary of polarity inferences for four cases of character-state distribution among two outgroups of uncertain relationships to the ingroup, 1 85 13. Summary of polarity inferences for six cases of character-state distribution among two near outgroups whose precise relationships to the ingroup are unresolved, and one more remote outgroup exhibiting a fixed character state, 1 87 Acknowledgments Many people have helped me toward the completion of this study in ways big and small. Over the years I have undoubtedly forgotten the contributions of some of them, and I apologize for this. Of those I have not forgotten, I want to thank the following people for lending me specimens under their care: Pere Alberch, Walter Auffenberg, James Berrian, Robert Bezy, Steven Busack, Joseph Collins, Ronald Crombie, Mark Dodero, Robert Drewes, William Duellman, Anne Fetzer, George Foley, Harry Greene, L. Lee Grismer, W. Ronald Heyer, J. Howard Hutchinson, Charles Meyers, Peter Meylan, Mark Norell, Gregory Pregill, Jose Rosado, Albert Schwartz, Jens Vindum, Van Wallach, John Wright, George Zug, Richard Zweifel, and especially Jay Savage and Richard Etheridge whose collections provided the majority of the specimens examined in this study. I am also grateful to various teachers, friends, and colleagues who helped my ideas on systematics and iguanine biology unfold through countless discussions: Troy Baird, Aaron Bauer, Theodore Cohn, Michael Donoghue, Richard Estes, Richard Etheridge, Jacques Gauthier, Eric Gold, David Good, George Gorman, Scott Lacour, Eric Lichtwardt, James Melli, Sheldon Newberger, Mark Norell, Michael Novacek, David Wake, and Andre Wyss. Linda Condon-Howe, Charles Crumly, Sanae and John Moorehead, Douglas Preston, Doris Taylor, and the late Kenneth Miyata generously provided lodging while I was visiting museums. Richard Estes, Richard Etheridge, Darrel Frost, Gregory Pregill, David Wake, and Edward Warren, provided valuable comments on earlier versions of the manuscript. David Cannatella and Rose Anne White gready assisted in the preparation of camera-ready-copy. Finally, I want to give special thanks to Karen Sitton for providing emotional support in her unique and charming way and to Richard Etheridge and Richard Estes for their influence on both my academic and personal development. This study partially fulfilled the requirements of a Master's degree in Zoology at San Diego State University, but was completed at the University of California, Berkeley. The research and preparation of the manuscript were supported in part by a grants from the Society of Sigma Xi, the San Diego State University Department of Zoology, the Theodore Roosevelt Memorial Fund of the American Museum of Natural History, and the Graduate Student Research Allocation Fund of the Department of Zoology, University of California at Berkeley. XI Abstract Iguaninae is a monophyletic taxon of tetrapodous squamates (lizards) that can be distinguished from other iguanians by at least five synapomorphies. Skeletal variation within Iguaninae is described and forms the basis of systematic characters used to determine phylogenetic relationships among eight basic taxa, the currendy recognized iguanine genera. Evolutionary character polarities are determined by comparison with four closely related taxa, basiliscines, crotaphytines, morunasaurs, and oplurines. The distributions of derived characters among iguanine taxa suggest that: (1) Either Brachylophus or Dipsosaurus is the sister group of the remaining iguanines (Iguanini). (2) Dipsosaurus is a monophyletic taxon diagnosed by at least six synapomorphies. (3) Brachylophus is a monophyletic taxon diagnosed by at least eight synapomorphies. (4) Iguanini, containing Amblyrhynchus, Conolophus, Ctenosaura, Cyclura, Iguana, and Sauromalus, is a new monophyletic taxon diagnosed by at least three synapomorphies. (5) vWithin Iguanini, the relationships among four t2Lxa.-Ctenosaura, Sauromalus, Amblyrhynchina, and Iguanina-are unresolved. (6) Ctenosaura is a monophyletic taxon 'diagnosed by at least three synapomorphies. (7) Enyaliosaurus is monophyletic, but it is a subgroup of Ctenosaura rather than a separate taxon. If Enyaliosaurus is separated from Ctenosaura, then Ctenosaura is not monophyletic. (8) Sauromalus is a monophyletic taxon diagnosed by at least 24 synapomorphies, many of which are convergent in Amblyrhynchus. (9) Amblyrhynchina is a new monophyletic taxon containing the Galapagos iguanas Amblyrhynchus and Conolophus, and is diagnosed by at least 1 1 synapomorphies. (10) Amblyrhynchus is a monophyletic taxon diagnosed by at least 28 synapomorphies and is perhaps the most divergent iguanine from the most recent common ancestor of all of them. Many of the unique features of Amblyrhynchus appear to be related to its unique natural history. (11) Conolophus is a monophyletic taxon diagnosed by at least eight synapomorphies and cannot, therefore, be considered ancestral to Amblyrhynchus. (12) Iguanina is a new monophyletic taxon composed oi Iguana and Cyclura and is diagnosed by at least three synapomorphies. (13) Iguana is a monophyletic taxon diagnosed by at least seven synapomorphies. (14) Monophyly of Cyclura is a problem in need of further study. Although three ostensible synapomorphies support monophyly of Cyclura, other derived characters suggest that some Cyclura shared a more recent common ancestor with Iguana than with other Cyclura. Summaries of Iguaninae and its monophyletic subgroups down to the level of the eight basic taxa are provided; each summary includes the type of the taxon, etymology of the taxon name, a phylogenetic definition, geographic distribution, a list of diagnostic synapomorphies, the fossil record, and various comments. xu INTRODUCTION Containing approximately 55 genera and more than 600 species, Iguanidae is one of the largest families of lizards. Its members occur primarily in the New World, from southern Canada to austral South America including the Galapagos Archipelago and much of the West Indies. Iguanids also occur on the island of Madagascar and in the Comores Archipelago in the western Indian Ocean, and on the Fiji and Tonga island groups in the southwestem Pacific. For over 100 years, systematists have attempted to discover the pattern of interrelationships among the genera in the family Iguanidae, but, because of the bewildering morphological diversity within this family, the task is far from complete. Nevertheless, many systematists have recognized suprageneric groups of iguanids (e.g., Wagler, 1830; Dumeril and Bibron, 1837; Fitzinger, 1843; Gray, 1845; Cope, 1886, 1900; Boulenger, 1890; H. M. Smith, 1946; Savage, 1958; Etheridge, 1959, 1964a). One of the earliest of these suprageneric groups to be recognized consists of the genera currently known informally as iguanines. This assemblage is also one of the most readily diagnosed on the basis of uniquely derived features. As currently conceived, there are eight genera and 31 species of iguanines (Etheridge, 1982). The iguanine genera are listed in Table 1, which also gives the number of included species, their habits, and the geographic distribution for each genus. HISTORICAL REVIEW The concept of an iguanine group is remarkably old, predating the publication of Darwin's Origin of Species (1859). This accomplishment is even more surprising when one realizes that all iguanines are native to regions far from western Europe, where systematists were developing the concept of an iguanine group. These systematists undoubtedly had few specimens at hand, and must have relied heavily on each others' character descriptions. Although I have been unable to see all of the potentially relevant literature, I attempt to trace and summarize the history of iguanine higher systematics. The Eighteenth Century. Although the eighteenth century was an important one for biological systematics as a whole, it was not so important for iguanine systematics. A convenient date to begin a historical discussion of iguanine systematics is 1758, when Linnaeus published the tenth edition of his Systema Naturae, the starting point of zoological nomenclature. Linnaeus himself was neither interested in nor fond of the "lower" tetrapods. He placed all tetrapodous squamates in two genera, one of which 1 University of California Publications in Zoology TABLE 1. The Iguanine Genera Genus (common name) Number of Species Habits Geograpiiic Distribution Amblyrhynchus Bell 1825 (Marine Iguanas) BrachylophusWagler 1830 (Banded Iguanas) Conolophus Fi\zingcT 1843 (Galapagos Land Iguanas) Clenosaura Wiegmann 1828 (Spiny-tailed Iguanas) 1 Terrestrial, saxicolous, semimarine Rocky coasts of various islands of the Galapagos Archipelago, Ecuador. 2 Arboreal Various South Pacific islands of the Fiji and Tonga groups. 2 Terrestrial Islands of the Galapagos Archipelago, Ecuador. 9 Terrestrial, arboreal Lowlands of Mexico and Central America, including various offshore islands, as far south as Panama. Cyclura Harlan 1824 (West Indian Ground Iguanas) Terrestrial Dipsosaurus Hallowell 1854 (Desert Iguanas) Iguana Laurenti 1768 (Green Iguanas) SauromalusYyumtnl 1856 (Chuckwallas) Terrestrial Arboreal Terrestrial, saxicolous The Bahama Islands; Cayman Islands; Navassa, Mona, and Anegada islands; and Cuba, Hispaniola, and Jamaica, and their nearby islets. Deserts of the southwestern United States, northwestern mainland Mexico, Baja California, and various islands in the Gulf of California. Lowlands of Mexico, Central America, and South America to southern Brazil and Paraguay; in the Caribbean northward through the Lesser Antilles to the Virgin Islands. Deserts of the southwestern United States, northwestern mainland Mexico, Baja California, and various islands in the Gulf of California. Sources: Etheridge (1982) and Gibbons (1981). Phylogenetic Systematics oflguanine Lizards contained Lacerta iguana (=Iguana iguana), the single known iguanine, and animals now placed in at least 12 different families, including crocodilians and amphibians. He considered them to be "foul and loathsome animals" (Linnaeus, 1758, translated in Goin et al., 1978). At the close of the eighteenth century only three of the currently recognized iguanine species (now placed in two genera) had been described, giving the systematists of that century, such as Laurenti (1768) and Lacepede (1788), Uttle of a group to recognize. The Nineteenth Century. Major advances in iguanine systematics came during the nineteenth century. Many important natural histories and systems or classifications of squamates appeared during these years, and by 1856 all of the currently recognized iguanine genera had been described. The concept of a natural iguanine taxon emerged during the first half of the nineteenth century. Most of the authors of classifications published during this period recognized a close relationship among at least some of the iguanine genera. Those that did not recognize a complete and exclusive group for the iguanines known at the time failed to do so for one or both of two reasons. Brongniart (1805), Latreille (1825), Fitzinger (1826, 1843), Wagler (1830), and Dumeril and Bibron (1837) grouped all the known iguanines together, but included some noniguanines with them. Although all the iguanines were sometimes placed together as part of a continuous list, it is not evident that they were considered to form their own subgroup within some larger group. Other authors such as Daudin (1805), Merrem (1820), Cuvier (1829, 1831), and Wagler (1830) failed to place all iguanines in a single group. Daudin, Cuvier, and Wagler included Brachylophus with the agamids, while Merrem did the same for Ctenosaura. At least three authors can truly be said to have recognized an iguanine group before 1850. I have two criteria for determining the true recognition of an iguanine group. First, all of the iguanine taxa known to the author (or at least all those listed in the classification) were included in the group; and second, no other taxa were included. Cuvier's (1817) "Les Iguanes proprement dits" consisted of what are now Iguana iguana, I. delicatissima, Cyclura cornuta, and Brachylophus fasciatus, although he later removed Brachylophus and placed it among the agamids (Cuvier, 1829, 1831). Wiegmann (1834) placed only the genera Cyclura, Ctenosaura, Iguana, Brachylophus, and Amblyrhynchus in his family Dendrobatae, Tribus II, b, ***, B. Like many of his contemporaries, Wiegmann constructed his classification as a hierarchy of sets and subsets that would also function as a key. The most fully developed early concept of an iguanine group appears to have been that of Gray (1831a, 1845). In 1831, Gray placed all known iguanines (equivalent to what are now 10 species in five genera) by themselves in a single genus, Iguana. Fourteen years later, he recognized nine different iguanine genera. Because these nine genera (again equivalent to five modem genera) formed one entire set in his hierarchical classification, it is evident that Gray still recognized the unity of the iguanine group. Progress in iguanine systematics, though less rapid than in the previous fifty years, continued through the second half of the nineteenth century. The last two iguanine genera that are still recognized, Dipsosaurus and Sauromalus, were described, but at first they University of California Publications in Zoology were not explicitly included with the rest of the iguanines in an exclusive group. The concept of an iguanine group, exclusive of Dipsosaurus and Sauromalus, was refined with more detailed anatomical descriptions. Beginning with Boulenger's (1885) monumental Catalogue of the Lizards in the British Museum, I undertake here a more detailed chronological treatment of the history of iguanine higher systematics. Boulenger (1885) listed all of the genera that are now called iguanines in a nearly continuous sequence in his catalogue, reflecting their position in his key as those iguanids having femoral pores and the fourth toe longer than the third but lacking spines on the head and an enlarged occipital scale. Nevertheless, the distantly related Hoplocercus (Etheridge in Paull et al., 1976) breaks the continuity of the iguanines in the list, and, in terms of Boulenger's characters, some iguanines are closer to certain non-iguanine iguanids than to other iguanines. Boulenger did not explicitly delimit subgroups within Iguanidae or any other family, and we can only guess about his precise ideas concerning such relationships. Cope (1886) appears to have been the first to use the name Iguaninae as a formal taxon for iguanine lizards. He further provided characters, both external and skeletal, by which members of this group could be distinguished from other iguanids. Cope's Iguaninae included Cyclura, Ctenosaura, Cachryx, Brachylophus, Iguana, Conolophus, and Amblyrhynchus, but failed to include Dipsosaurus and Sauromalus. The genera Aloponotus and Metopoceros were synonymized with Cyclura. In response to Cope, Boulenger (1890) provided what he considered to be osteological evidence for the separation of Metopoceros and Cyclura, and briefly described the skulls of "the iguanoid lizards allied to Iguana." Except for the recognition of Metopoceros and the omission of Cachryx, the genera included in this discussion were the same as Cope's (1886) Iguaninae. Dipsosaurus and Sauromalus were again left out of the group. Cope later (1900) greatly expanded his Iguaninae, and named two additional iguanid subfamilies, Anolinae and Basiliscinae. This new Iguaninae was a catch-all group for those iguanids that lacked midventrally continuous postxiphistemal inscriptional ribs, had simple clavicles, and lacked a left hepatopulmonary mesentery— in other words, those iguanids that lacked the distinctive features of anolines and basiliscines. Although this new Iguaninae was almost certainly an unnatural group, Cope recognized a slightly expanded version of his earlier (1886) Iguaninae as a discrete subset of his new and more inclusive group of the same name. This unnamed subset was characterized by the presence of femoral pores and of vertebrae with zygosphenal articulations. It contained Dipsosaurus and Sauromalus along with the genera included in his earlier Iguaninae; and it is therefore identical in generic content to the iguanine group as currently conceived. The Twentieth Century. During the first three-fourths of the twentieth century, the concept of an iguanine group underwent considerable change. The efforts of nineteenth- century authors such as Cope and Boulenger seem to have been largely ignored, and at least two authors envisioned the ancestry of most other North American iguanids within iguanines. This idea seems to have resulted from the misconception that iguanines were "primitive" iguanids and were, therefore, potential ancestors of other iguanid taxa; the integrity of the group was deemphasized or completely overlooked. Nevertheless, by the Phylogenetic Systematics oflguanine Lizards mid-1960's the iguanines had been resurrected as a natural group, the same group that Cope (1900) had recognized at the turn of the century. In his landmark paper on squamate systematics. Classification of the Lizards, Camp (1923) dealt primarily with the interrelationships of the lizard families. Nevertheless, his treatise contains scattered but intriguing comments on relationships at lower taxonomic levels. About the throat musculature of iguanines, he said: In the "Cyclura group" comprising the genera Iguana, Amblyrhynchus, Ctenosaura, Brachylophus, Sauromalus, and Cyclura, the superficial bundle [of the M. mylohyoideus anterior] is very specialized and consists of definitely directed fibers not connected with the skin. Detailed resemblances are present in this group which I have outlined in manuscript and which will not be repeated here. Suffice it to say that the group appears to be a natural one, on the basis of the musculature with close resemblances prevalent between Sauromalus and Cyclura, and Ctenosaura and Brachylophus. (Camp, 1923:371) Unfortunately, the whereabouts of the manuscript mentioned in this passage are unknown tome. Mittleman (1942) reviewed the genus Urosaurus and commented briefly on the relationships among the genera of North American iguanids, except Anolis. He implied that the North American iguanids formed a monophyletic group descended from Ctenosaura (Fig. 1) and that the similarities among Ctenosaura, Dipsosaurus, and Sauromalus were retained primitive features: Dipsosaurus is probably the most primitive of the North American Iguanidae (excepting Ctenosaura, which is properly a Central and South American form), and possesses several points in common with Ctenosaura, most easily observed of which is the dorsal crest; the genera further show their relationship in the similarity of the cephalic scutellation which is essentially simple, and shows no particular degree of differentiation. Sauromalus is considered a specialized offshoot of the Crotaphytus, or more properly, prQ-Crotaphytus stock, by reason of its solid sternum, as well as the five-lobed teeth; the simple type of cephalic scalation indicates its affinity with the more primitive Dipsosaurus-Ctenosaura stock. (Mittleman, 1942:112-113) H. M. Smith (1946:92) seemed to adopt a modified version of Mittleman's views on the phylogeny of North American iguanids (Fig. 2). His herbivore section {Ctenosaura, Dipsosaurus, and Sauromalus) was considered to be ancestral to the other North American Iguanidae, save Anolis, with Sauromalus hypothesized to share a more recent common ancestry with these other iguanids than with either Ctenosaura or Dipsosaurus. Smith's subsequent comments (1946:101), however, indicate that he recognized affinities of Ctenosaura, Dipsosaurus, and Sauromalus to iguanids occurring outside of the United University of California Publications in Zoology Streptosaurus Petrosaurus -^ Crotaphytus Callisaurus Uma Holbrookia Uta ,, y Urosaurus \ /" Sceloporus \ Sator Phrynosoma Dipsosaurus Ctenosaura Primitive Iguanid Type FIG. 1. "The phylogeny and relationships of North American iguanid genera," after Mittleman (1942:113). States. In addition to the three genera found in or near the United States, Smith's herbivore section contained other "large, primitive iguanids," namely Amblyrhynchus, Conolophus, Cyclura, and Iguana. Smith's Handbook dealt with the lizards of the United States and Canada; those iguanines whose ranges did not enter this area were apparently omitted from his phylogram for convenience. In any case. Smith could not have considered his herbivore section to be monophyletic in the more restricted modem sense, since the group was considered to be ancestral to other North American iguanids. Savage (1958) explicitly challenged Mittleman's (1942) implication that the North American iguanids formed a natural group: Insofar as can be determined at this time, the so-called Nearctic iguanids form two diverse groups that can only be distantly related. These two sections are Phylogenetic Systematics oflguanine Lizards FIG. 2. "Grouping and possible phylogeny of the genera of iguanids occurring in the United States," after H. M. Smith (1946:92). Roman numerals apparently refer to the following: (I) leaf-toed section, (II) herbivore section, (III) sand-lizard section, (IV) rock-lizard section, (V) pored utiform section, (V) horned- lizard section, and (VII) poreless utiform section. distinguished by marked differences in vertebral and nasal structures and include several genera not usually recognized as being allied to Nearctic forms. (Savage, 1958:48) Savage's "iguanine line" contained Amblyrhynchus, Brachylophus, Conolophus, Crotaphytus, Ctenosaura, Cyclura, Dipsosaurus, Enyaliosaurus {=Ctenosaiira, part), Iguana, and Sauromalus. This group was distinguished from the "sceloporine line" by two primary characters: the presence of accessory vertebral articulations, the zygosphenes and zygantra, and the possession of a relatively simple, S-shaped nasal passage with a concha present (Dipsosaurus-lypt of Stebbins, 1948). Other osteological and integumentary features characteristic of the majority of the genera in each line were also given. 8 University of California Publications in Zoology The currently recognized iguanine group is based on the work of Etheridge. In his paper on the systematic relationships of sceloporine lizards, Etheridge (1964a) showed that the two primary characters used by Savage (1958) to diagnose the iguanines were actually more widespread within the Iguanidae, and were thus insufficient to diagnose the group. He listed four fundamental differences between Crotaphytus and Savage's other iguanines, and asserted that if Crotaphytus was considered to be an iguanine, no character or combination of characters could be used to diagnose that group. Once he removed Crotaphytus from the group, the iguanines were readily diagnosed by their unique caudal vertebrae. Except for his recognition of Enyaliosaurus as a genus separate from Ctenosaura, Etheridge's (1964a) concept of the iguanines is identical to that held today (Etheridge, 1982). Despite the long history of iguanines as a recognized group and the great interest in many aspects of iguanine biology (e.g., Burghardt and Rand, 1982; Troyer, 1983), the interrelationships among the iguanine genera and the relationships of iguanines to other iguanians remain largely unknown. Commonly held beliefs are that Ctenosaura and Cyclura are closely related (Barbour and Noble, 1916; Bailey, 1928; Schwartz and Carey, 1977), and that the same is true of the Galapagos iguanas Amblyrhynchus and Conolophus (Heller, 1903; Eibl-Eibesfeldt, 1961; Thornton, 1971; Higgins, 1978). As mentioned above, Mittleman (1942) and H. M. Smith (1946) have offered dendrograms depicting their views on the relationships of the North American iguanines. Recent studies have examined diverse data for clues about the interrelationships among the iguanine genera, but have met with limited success. Zug (1971) studied the arterial system of iguanids. He published shortest-connection networks for more than 40 iguanid genera, some based on his arterial characters and others based on characters obtained from the literature, most of which were osteological. Other shortest-connection networks constructed from data on arterial variation within various suprageneric assemblages of iguanids, including iguanines, were also presented. Nevertheless, Zug doubted the usefulness of his arterial characters in iguanid systematics, stating: "The arterial characters employed herein appear to be of minimal value in iguanid classification. At the intrafamilial level, they are disruptive and form groups of questionable zoogeographic unity" (Zug, 1971:21). There has been but a single study in which the relationships among all known iguanine genera were sought, that of Avery and Tanner (1971). These authors provided descriptions of the iguanine skeleton, head and neck musculature, tongue, and hemipenes, and gave a number of osteological measurements. They based their hypothesis of relationships on mean length-width ratios of bones, assuming that "a difference of forty or less points between means of the same bone indicates a close relationship" (Avery and Tanner, 1971:67). Large numbers of such similarities were taken to indicate close phylogenetic relationship among taxa and were used in some unspecified way to construct a phylogenetic diagram (Fig. 3). Avery and Tanner examined small series (never more than five individuals of a single species), giving no consideration to allometric changes in the ratios that they used. I suspect that many of these ratios are correlated with a single Phylogenetic Systematics oflguanine Lizards Sauromalus Ctenosaura Cyclura Iguana Conolophus Amblyrhynchus Pre-Ctenosaura-lguana Stock Opiurus Dipsosaurus Brachylophus Chalarodon Iguanid Ancestor FIG. 3. "Phylogenetic relationships of the Madagascar Iguanidae and the genera of iguanine lizards," after Avery and Tanner (1971:71). variable, size, and should not therefore be used as independent evidence for relationship. Furthermore, these authors made no attempt to assess the evolutionary polarity of their characters by comparison with other iguanids. Karyological data on iguanines have been practically useless for systematic purposes. At the crude level of karyotypic analysis commonly applied to lizards, in which only numbers and sizes of chromosomes and their centromeric positions are determined, iguanines are conservative. All species of Conolophus, Cyclura, Ctenosaura, Dipsosaurus, and Sauromalus that have been studied possess a karyotype known to be 10 University of California Publications in Zoology widespread within Iguanidae and found in several other lizard families as well (Paull et al, 1976). Only Iguana iguana has been reported to differ from this seemingly primitive condition in that this species supposedly lacks one pair of microchromosomes (Cohen et al., 1967), but even this finding was contradicted in another study (Gorman et al., 1967; Gorman, 1973). Iguanine relationships have only been studied superficially with relatively new and increasingly popular biochemical techniques. Gorman et al. (1971) presented evidence for close relationship among iguanines based on immunological studies of lactic dehydrogenases and serum albumins in turtles and various diapsids. Higgins and Rand (1974, 1975) showed that the serum proteins and hemoglobins of Amblyrhynchus and Conolophus were more similar to each other than to those of Iguana. Unfortunately, other iguanines were not examined. Wyles and Sarich (1983) performed immunological comparisons of the serum albumins of 10 species of iguanines including representatives of all eight genera. However, antisera were prepared to the albumins of only four of the species, and comparisons with all others are given only for the antisera to the albumins of Amblyrhynchus and Conolophus. Because of the incompleteness of the data, only very general phylogenetic inferences can be drawn from them. The unique colon of iguanines was studied by Iverson (1980, 1982), who reported that the iguanine colon differed from that of all other iguanids and most other lizards in the possession of transverse valves or folds. However, Iverson (1980) felt that the variation in these structures within iguanines was of httle value for inferring phylogenetic relationships. Peterson (1984) has recently surveyed the scale surface microstructure of iguanids. Although some intergeneric variation in the morphology of the scale surface is known to occur in iguanines, representatives of only three iguanine genera {Iguana, Dipsosaurus, and Sauromalus) have been studied at this time. One final hypothesis about iguanine relationships deserves mention. At the prompting of a colleague (Ernest Williams) some twenty-five years ago, Richard Etheridge drew up a phylogenetic diagram depicting his views on the interrelationships among the iguanid genera. The character basis for this diagram was not specified, and Etheridge (pers. comm., 1981) informs me that the relationships shown among the iguanine genera were strongly influenced by his knowledge about the geographic distributions of these animals. Although he never intended the diagram to be published, it has been published in modified form (Paull et al., 1976; Peterson, 1984), and has also appeared in several graduate theses. I reproduce the original diagram here (Fig. 4), noting that its creator does not grant the hypothesis the conviction seemingly implied by a branching diagram. GOALS OF THIS STUDY A detailed study aimed at revealing the pattern of phylogenetic relationships among the various iguanine lizards is sorely needed. It would provide invaluable information for the many people studying other aspects of iguanine biology, particularly in an evolutionary context. I have attempted such a study here with the following as my goals: (1) to provide Phylogenetic Systematics oflguanine Lizards 11 Uracentron Ophrv^oessoides Plica 1 5tfob.\oru5 StenocercU5 Phrtjoosaora CVcnoV)\cpV\Qris \_\o\acrt\us Urarwscocion Le\ocet)V)a\os Sce\oporys H"?.'*- , ' Urosaoros , PWrij|noSoma 5auroma\us ^PetrosQurys Phenacosaurus CV\atT\ae\eoVis Po^cVtTus CorijlViopVioines Laetnanc^us Op\uro5 Cha\aro