Assembling the Squamate Tree of Life: Perspectives from the Phenotype and the Fossil Record Jacques A. Gauthier,1 Maureen Kearney,2 Jessica Anderson Maisano,3 Olivier Rieppel4 and Adam D.B. Behlke5 1 Corresponding author: Department of Geology and Geophysics, Yale University, P.O. Box 208109, New Haven CT 06520-8109 USA and Divisions of Vertebrate Paleontology and Vertebrate Zoology, Peabody Museum of Natural History, Yale University, P.O. Box 208118, New Haven CT 06520-8118 USA —email: [email protected] 2 Division of Environmental Biology, National Science Foundation, Arlington VA 22230 USA 3 Jackson School of Geosciences, The University of Texas at Austin, Austin TX 78712 USA 4 Department of Geology, Field Museum of Natural History, 1400 S. Lake Shore Drive, Chicago, IL 60605-2496 USA 5 Department of Geology and Geophysics, Yale University, P.O. Box 208109, New Haven CT 06520-8109 USA Abstract We assembled a dataset of 192 carefully selected species—51 extinct and 141 extant—and 976 apo- morphies distributed among 610 phenotypic characters to investigate the phylogeny of Squamata (“lizards,” including snakes and amphisbaenians). These data enabled us to infer a tree much like those derived from previous morphological analyses, but with better support for some key clades. There are also several novel elements, some of which pose striking departures from traditional ideas about lizard evolution (e.g., that mosasaurs and polyglyphanodontians are on the scleroglos- san stem, rather than parts of the crown, and related to varanoids and teiids, respectively). Long- bodied, limb-reduced, “snake-like” fossorial lizards—most notably dibamids, amphisbaenians and snakes—have been and continue to be the chief source of character conflict in squamate morpho- logical phylogenetics. Carnivorous lizards (especially snakes, mosasaurs and varanoids) have proven a close second. Genetic data, presumably less burdened by the potential for adaptive con- vergence related to fossoriality, were expected to resolve these conflicts. Although recent gene phy- logenies seem to do so, they also differ radically from any phylogeny based on the phenotype, especially for the most ancient crown squamate divergences that occured during the latter half of the Mesozoic. Our study relied on traditionally prepared specimens as well as high-resolution computed tomography scans that afforded unprecendented access to the cranial anatomy of Squa- mata. This, along with the inclusion of stem fossils, provided an unparalleled sample of the phe- notype enabling us to more fully explore the extreme incongruences between molecular and morphological topologies for the squamate tree of life. Despite this extensive new database, we were unable to find morphological support for the major rearrangement of the deep divergences in Squamata proposed by recent molecular studies. Instead, our data strongly support the same fun- damental topology suggested by most previous morphological studies—an Iguania–Scleroglossa basal split, a sister-group relationship between Gekkota and Autarchoglossa, and the divergence between Anguimorpha and Scincomorpha—and documents the extreme degree of morphological homoplasy required by those molecular topologies. Keywords Rhynchocephalia, Squamata, Iguania, Polyglyphanodontia, Scleroglossa, Gekkota, Autar- choglossa, Scincomorpha, Anguimorpha, Mosasauria, Serpentes, phylogeny, morphology, fos- sils, biogeography, divergence times, homoplasy, evolution, taxon sampling, morphology vs. molecules. Bulletin of the Peabody Museum of Natural History 53(1):3–308, April 2012. © 2012 Peabody Museum of Natural History, Yale University. All rights reserved. • http://peabody.yale.edu 4 Bulletin of the Peabody Museum of Natural History 53(1) • April 2012 Introduction Although the Cuvierian scheme of classifica- tion portrayed “affinities” in terms of a dichoto- With his “Essai d’une Classification Naturelle des mous hierarchy, the image of an underlying Reptiles,” Alexandre Brongniart (1800a, 1800b), a “series” of forms still dominated comparative collaborator of Georges Cuvier, set the stage for biology well into the 19th century (Daudin 1926), all later discussions of “reptile” classification. as can be seen from Oppel’s (1811) concerns Applying Cuvier’s method of dichotomized clas- about the continuity of the “lizard” with the snake sification (called méthode naturelle by Cuvier “series.” Louis Agassiz, in his famous Essay on [1817:10]) to extant tetrapods (except birds and Classification (1857), emphasized continuity of mammals), he recognized four “orders” later limb reduction in squamates, citing the graded adopted by Duméril (1806) in his classic Zoologie series of intermediates between “lizards” and Analytique: Chéloniens, Sauriens, Ophidiens and snakes as evidence for the completeness (pleni- Batraciens. Because of an error in the dissection of tude) of the scheme of nature, which for him was the caecilian, “lizard” and snake hearts jointly ultimately rooted in Divine thought. Such views, undertaken by Cuvier, Brongniart, and F.M. of course, were famously opposed by Charles Daudin, snakes were separated from “lizards,” but Darwin. Noting the presence of rudimentary the long-bodied, limbless caecilian amphibians hindlimbs in some basal snakes, Darwin was sat- were included within snakes (Daudin 1926; Riep- isfied that “on my view of descent with modifica- pel 1987b). tion, the origin of rudimentary organs is simple” The “order Squamata” was introduced by (Darwin 1859:206). The gradual transition from Oppel (1811:14) to encompass “Saurii” (with dis- limb-reduced “lizards” to snakes pointed to tinct limbs and nondilatable maxillary bones) and descent with modification. This pattern of “Ophidii” (lacking external limbs and character- thought was interrupted, though, by Cope ized by dilatable maxillary bones). Oppel’s (1869:253), who referred monitor-like, marine (1811:19) “Saurii” included the crocodilians lizards from the Cretaceous to his Pythonomor- (which will not be further commented on here). pha based on the fact that mosasaurs have an More important is his grouping of “lizards” and intramandibular joint in the lower jaw, as well as snakes within one order, which he based on the a loose mandibular symphysis, as do some snakes insight that hardly any single character unam- such as pythons. Later, Cope (1872) used similar- biguously differentiates “lizards” from snakes. For ities of inferred jaw mechanics in support of Ophisaurus (considered an intermediate between the phylogenetic derivation of snakes from snakes [Ophi-] and “lizards” [-saurus] by F.M. mosasaurs. Cope (1878, 1895a, 1895b, 1896) con- Daudin [O. ventralis, Daudin 1803:346]), and tinued to defend his gradualistic scenario linking Anguis fragilis (both of which Duméril [1806] had the feeding mechanics of mosasaurs with those of grouped with other “lizards”), Oppel (1811:17) macrostomatan snakes like boas and pythons confessed difficulty in deciding whether these against criticisms such as those of Owen (1877, should be arranged “at the end of the lizard 1878) and Baur (1895, 1896). [series], or at the beginning of the snake The subsequent discovery of basal mosasaurs [series]...nature herself seems not to have placed such as “aigialosaurs” and dolichosaurs—the lat- great weight on the character of [the presence or ter approaching snakes more closely in general absence] of limbs.” But whereas he continued to body proportions than the highly derived group Ophisaurus and Anguis with “lizards,” he Mosasauridae, and exhibiting various stages of included the (mostly) limbless amphisbaenians limb size reduction and body elongation (Korn- with snakes (Oppel 1811:53), as Brongniart huber 1873, 1901; Gorjanovic-Kramberger 1901; (1800a) had done before him. Oppel’s early Nopcsa 1903, 1908; Janensch 1906)—from early (1811) efforts in his “arrangement of reptiles” mid-Cretaceous marine sediments of southern introduced themes that still resonate in contem- Europe, seemed to lend further support to Cope’s porary discussions of squamate phylogeny, in earlier theory of snake origins. With the discovery particular the potential relationships of snakes to of Pachyophis woodwardi from the early Upper other limb-reduced and long-bodied taxa within Cretaceous of Bosnia-Herzogevina, Nopcsa Squamata. (1923) believed he had finally found the critical Assembling the Squamate Tree of Life • Gauthier et al. 5 transitional species between basal mosasaurs and by McDowell and Bogert (1954). This mono- snakes, which in his view also necessarily implied graph not only made important improvements to a marine origin of snakes (Nopcsa 1925). Camp’s (1923) original lizard phylogeny with Meanwhile, Camp’s (1923) monograph on respect to the composition and interrelationships the classification of lizards was an important mile- of Anguimorpha, but also proposed the earless stone, the first modern attempt at a broad-scale “monitor” Lanthanotus borneensis as the extant analysis of squamate relationships (Underwood quadrupedal “lizard” most closely related to 1971). Much of the later work on lizard classifi- snakes. Interpreted by McDowell and Bogert cation based on morphology can be seen as refin- (1954:54) as a “living aigialosaurian,” the particu- ing Camp’s (1923) results. What Camp’s (1923) lar habits of Lanthanotus, a secretive creature monograph established for “lizard” classification, found on the banks of the Sarawak River in Bor- Underwood’s (1967) seminal contribution pro- neo, would nicely bridge the gap