US ISSN 0006-9698 CAMBRIDGE,MASS.19OCTOBER 2009 NUMBER 518 AN ARCHOSAUR-LIKE LATEROSPHENOID IN EARLY TURTLES (REPTILIA: PANTESTUDINES) BHART-ANJAN S. BHULLAR1 AND GABE S. BEVER2 ABSTRACT. Turtles are placed with increasing consistency by molecular phylogenetic studies within Diapsida as sister to Archosauria, but published gross morphology–based phylogenetic analyses do not recover this position. Here, we present a previously unrecognized unique morphological character offering support for this hypothesis: the presence in stem turtles of a laterosphenoid ossification identical to that in Archosauriformes. The laterosphenoid is a tripartite chondrocranial ossification, consisting of an ossified pila antotica, pila metoptica, and taenia medialis + planum supraseptale. It forms the anterior border of the exit for the trigeminal nerve (V) and partially encloses the exits for cranial nerves III, IV, and II. This ossification is unique to turtles and Archosauriformes within Vertebrata. It has been mistakenly dismissed as anatomically dissimilar in these two groups in the past, so we provide a complete description and detailed analysis of correspondence between turtles and Archosauriformes in each of its embryologically distinct components. A preliminary phylogenetic analysis suggests other potential synapomorphies of turtles and archosaurs, including a row or rows of mid-dorsal dermal ossifications. KEY WORDS: Archosauria; Archosauriformes; Diapsida; turtle origins; chondrocranium; Proganochelys; Kayentachelys; fossil; braincase; interorbital ossification; Testudines Turtles (Pantestudines; Joyce et al., 2004) that is ancestral for diapsid reptiles, includ- have traditionally been classified as ‘‘ana- ing tuatara, lizards, crocodiles, and birds psid’’ reptiles owing to their lack of the (Gauthier et al., 1988, and references there- lateral and dorsal fenestration of the skull in). Early gross morphology–based phyloge- netic analyses suggested that turtles are the 1 Department of Organismic and Evolutionary Biology, sister taxon to Diapsida and thus one of the Harvard University, Biolabs room 4110, 16 Divinity two branches of the initial reptilian diver- Avenue, Cambridge, Massachusetts 02138, U.S.A.; e- gence (Gauthier et al., 1988). Most subse- mail: [email protected] quent morphological analyses have either 2 Division of Paleontology, American Museum of Natural History, Central Park West at 79th Street, supported this position (Brochu, 2001; New York, New York 10024, U.S.A. Laurin and Reisz, 1995; Lee, 1997) or have E The President and Fellows of Harvard College 2009. 2 BREVIORA No. 518 placed turtles close to the marine Euryapsida er, the general consensus at the time, along the stem of the lizard/tuatara clade including the hypothesis presented by Gaff- Lepidosauria (Li et al., 2008; Rieppel and ney (1990), was that turtles were sister to all Reisz, 1999), thus suggesting that they are other extant reptiles. These elements were highly modified diapsids. One analysis thus termed ‘‘pleurosphenoids,’’ with the (Merck, 1997) similarly indicated affinities quotation marks indicating probable non- to the Euryapsida but recovered a novel homology with those of Archosauriformes. result because the included characters of We posit, in contrast, that they are in fact non-turtle euryapsids placed the entire turtle homologous to the laterosphenoids of Arch- + euryapsid clade as sister to the archosaur osauriformes. lineage (Brochu, 2001). In contrast, a growing body of molecular MATERIALS AND METHODS phylogenetic work strongly supports a posi- All specimens examined are from the tion of turtles within Diapsida as sister to the collections of the Museum of Comparative crocodile/bird clade Archosauria (Cao et al., Zoology, Harvard University. The following 2000; Iwabe et al., 2005; Kumazawa and specimens from the Herpetology collection Nishida, 1999; Organ et al., 2008). Until were examined: Alligator mississippiensis now, no unique gross morphological support MCZ 17711, 34323; Caiman crocodilus has been reported for archosaur affinities of MCZ 5031; Crocodylus cataphractus MCZ turtles (Rieppel, 2000), and in particular, no 13985, 175004; C. niloticus MCZ 4372; C. morphological evidence has been forthcom- porosus MCZ 72937; Gavialis gangeticus ing that would help place turtles along the MCZ 33950; Osteolaemus tetraspis MCZ archosaur stem. However, such evidence has 22913; Paleosuchus palpebrosus MCZ existed, largely overlooked, since the further 84030; Tomistoma schlegeli MCZ 12459. preparation and monographic description by From the Ornithology collection: Tinamus Gaffney of the best-preserved stem turtle, major MCZ 342723, 342774. From the Proganochelys quenstedti, from the Late Vertebrate Paleontology collection: Eothyris Triassic (Norian) of Germany (Gaffney, parkeyi MCZ 1161. 1990). Phylogenetic analyses, as described below, A single specimen of P. quenstedti (SMNS used a modified version of the matrix from 15759) preserves the region anterior to the Dilkes (1998). Both used parsimony searches braincase. In this region, which would in life in PAUP* v4.0b10 (Swofford, 2001) with the have been occupied by the membranous branch-and-bound search option (1,000 rep- anterior braincase, a pair of dorsoventrally licates), specifying Petrolacosaurus as the tall, flat ossifications articulate with the outgroup as in Dilkes (1998). The con- prootic and basisphenoid on each side strained search used the monophyly con- (Fig. 1A). The initial description of this straint option to unite Proganochelys with region by Gaffney (1990) documented the the archosauriform clade, including Eupar- form of these bones but did not treat the keria and Proterosuchus. detailed morphology of each of their pro- cesses. It was noted that they are similar to a DESCRIPTION OF THE LATEROSPHE- pair of ossifications synapomorphic for the NOID IN PROGANOCHELYS clade Archosauriformes, the pleurosphe- noids (Fig. 1B), which are now usually called Following is a more complete description laterosphenoids (Clark et al., 1993). Howev- of the left laterosphenoid in Proganochelys 2009 ARCHOSAUR-LIKE LATEROSPHENOID IN EARLY TURTLES 3 Figure 1. (A) Left laterosphenoid of Proganochelys quenstedti SMNS 15759 in lateral view, after Gaffney (1990). (B) Right laterosphenoid of Proterosuchus fergusi NMQR 1484 in lateral view, reflected, after Clark et al. (1993). (C) Chondrocranium of Crocodylus porosus after ref 1 with region ossified as laterosphenoid filled in. BS, basisphenoid; FR, frontal; EP, epipterygoid; LS, laterosphenoid; OP, opisthotic; PA, parietal; PF, postfrontal; PO, postorbital; PR, prootic; Q, quadrate. 4 BREVIORA No. 518 than was offered in the original monograph. would have formed around cranial nerve II Our goal is to elucidate the developmental (optic nerve) and its associated neurovascu- origins of the turtle laterosphenoid and thus lar structures. Thus, topologically and mor- demonstrate its exact correspondence to the phologically, this strut corresponds to the archosauriform morphology. pila metoptica of the embryonic amniote Mediolaterally, the laterosphenoid is thin, chondrocranium (Fig. 1C), an observation especially near its periphery, and it is inclined not made in the description by Gaffney ventromedially, reflecting the angulation of (1990). the wall of the membranous braincase within The third major component of the latero- which it ossified (Fig. 1A). It has three major sphenoid is an anterodorsally directed, ter- components. The first is a strut that extends minally expanded lobe (Fig. 1A) connected anterodorsally from the clinoid process of basally to both of the other two components the basisphenoid, but whose posterodorsal whose broadly curved anteroventral margin portion forms a small contact with the forms the majority of the emargination for anterodorsal portion of the prootic. The cranial nerve II and whose posterodorsal posterior margin of the strut forms the margin borders an aperture that might anterior half of the border of the trigeminal represent the fenestra epioptica of the (prootic) foramen transmitting cranial nerve diapsid embryo (Bellairs and Kamal, 1981). V, which is fully encircled by virtue of its As noted in the description by Gaffney dual contacts—the ventral, broad contact (1990), the dorsal and anterior margins of with the clinoid process of the basisphenoid the lobe appear unfinished. This morphology and the dorsal, attenuate contact with the could represent breakage, but considering prootic. The anterior margin of the strut the general completeness of the surrounding forms the posterior border of a ventrally elements, we think it more plausible that it is incomplete aperture that in life would have instead the border between the ossified and been formed around cranial nerves III and cartilaginous portions of the structure. The IV. Topologically and morphologically, this rough but not jagged texture of the surfaces strut corresponds exactly to the pila antotica supports this interpretation. The original of the embryonic amniote chondrocranium description emphasizes that there are no (Fig. 1C; Bellairs and Kamal, 1981), as signs on the parietal of a bony suture with suggested but not fully explicated in the the laterosphenoid. Topologically and mor- description by Gaffney (1990). The meeting phologically, the lobe corresponds to the with the prootic and thus closure of the taenia medialis and perhaps a portion of the trigeminal foramen, however, is a unique planum supraseptale of the chondrocranium feature of laterosphenoids.