The Skull of the Rare Malaysian Snake Anomochilus Leonardi Smith, Based

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Blackwell Publishing LtdOxford, UKZOJZoological Journal of the Linnean Society0024-4082The Lin- nean Society of London, 2007? 2007 1494 671685 Original Articles

SKULL OF THE MALAYSIAN SNAKE ANOMOCHILUS LEONARDIO. RIEPPEL and J. A. MAISANO

Zoological Journal of the Linnean Society, 2007, 149, 671–685. With 5 figures

The skull of the rare Malaysian snake Anomochilus leonardi Smith, based on high-resolution X-ray computed tomography Downloaded from https://academic.oup.com/zoolinnean/article/149/4/671/2630933 by guest on 30 September 2021 O. RIEPPEL1* and J. A. MAISANO2

1Department of Geology, The Field Museum, 1400 S Lake Shore Drive, Chicago, Illinois 60605-2496, USA 2Jackson School of Geosciences, The University of Texas at Austin, Austin, Texas 78712, USA

Received January 2006; accepted for publication June 2006

The skull of the rare Malaysian snake Anomochilus leonardi is described in detail on the basis of a high-resolution X-ray computed tomographic scan of a mature specimen. Its skull anatomy is compared with that of Anomochilus weberi, as well as with that of scolecophidians and basal alethinophidians such as Anilius, Cylindrophis, uropeltines and selected Booidea. Anomochilus leonardi is found to be more paedomorphic than Anomochilus weberi. The genus Anomochilus most closely resembles uropeltines in skull anatomy. Both Anomochilus and uropeltines develop a ‘central rod design’ of skull morphology, which requires the presence of medial frontal pillars, in adaptation to burrowing habits. These pillars are an alethinophidian characteristic, absent in the skull of scolecophidians, which develop an ‘outer shell design’ in adaptation to burrowing. These results are discussed in the light of the hypothesis that scolecophidians and basal (i.e. non-macrostomatan) alethinophidians are ‘regressed macrostomatans’. © 2007 The Linnean Society of London, Zoological Journal of the Linnean Society, 2007, 149, 671–685.

ADDITIONAL KEYWORDS: anatomy – paedomorphosis – phylogeny.

INTRODUCTION East have ignited a vigorous debate on snake interrelationships (e.g. Coates & Ruta, 2000; Rieppel & The snake genus Anomochilus comprises two species. Kearney, 2001; for a full discussion of the debate and Anomochilus weberi (Lidth de Jeude, 1890) is known references see Rieppel et al., 2003). Some analyses from three specimens collected in Sumatra and (e.g. Lee & Caldwell, 1998; Scanlon & Lee, 2000; Lee, Borneo (Lidth de Jeude, 1890, 1922; Brongersma & 2005; Scanlon, 2005) challenge the traditional view Helle, 1951), and A. leonardi Smith (1940) is known that the burrowing or fossorial (secretive) scolecophid- from ﬁve specimens collected in Malaysia (Lim & ians (blindsnakes and threadsnakes) and ‘anilioids’ Mohd. Sharef, 1975; Stuebing & Goh, 1993; Yaakob, (pipesnakes and shieldtails) are basal to macrostoma- 2003). Due to the scarcity of these Indonesian snakes, tan snakes (boas, pythons and colubroids). They do so little is known about their anatomy and biology. How- by placing the fossil snakes with well-developed hind ever, in light of the genus’ putative relationship to limbs at the bottom of the snake tree. But because other basal snakes such as scolecophidians or ‘anili- these fossils combine well-developed hind limbs with a oids’ (Lidth de Jeude, 1890; Boulenger, 1893; Under- macrostomatan skull structure (e.g. Zaher, 1998; Rage wood, 1967; McDowell, 1975, 1987; Rieppel, 1977, & Escuillié, 2000, 2003; Polcyn, Jacobs & Haber, 1979a; Groombridge, 1979a), Anomochilus has long 2005), their placement basal to all extant snakes been an important taxon in the analysis of snake renders scolecophidians and ‘anilioids’ ‘regressed mac- phylogeny. rostomatans’ (Rage & Escuillié, 2000, 2003; G. Under- More recently, fossil snakes with well-developed wood, pers. comm.). These recent controversies hind limbs from the mid-Cretaceous of the Middle highlight the importance of an improved understanding of the phylogenetic interrelationships of basal *Corresponding author. E-mail: orieppel@ﬁeldmuseum.org snakes, including Anomochilus.

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In two landmark papers, Cundall and collaborators The specimen was scanned using the following (Cundall & Rossman, 1993; Cundall, Wallach & parameters. A FeinFocus microfocal X-ray source oper- Rossman, 1993) presented a detailed description of ating at 180 kV and 0.088 mA with no X-ray prefilter the cranial anatomy of Anomochilus weberi, which was employed. An empty container wedge was used. formed the basis of a cladistic analysis of the phyloge- Slice thickness corresponded to two lines in a CCD netic relationships of the species. Anomochilus was image intensifier imaging system, with a source-to- found not to be a scolecophidian, as indicated by vis- object distance of 21 mm. For each slice, 1600 views ceral and integumental features (V. Wallach, cited in were taken with four samples per view. The field of Cundall & Rossman, 1993: 236), but instead to be a image reconstruction was 5.5 mm, and an image non-macrostomatan alethinophidian snake. Its inclu- reconstruction offset of 10 000 was used with a recon- sion in that analysis resulted in rejection of the puta- struction scale of 1500. Downloaded from https://academic.oup.com/zoolinnean/article/149/4/671/2630933 by guest on 30 September 2021 tive monophyly of Anilioidea (Rieppel, 1977, 1979a), The data set consists of 553 HRXCT slices taken however, as Anomochilus was found to be the sister- along the transverse (= coronal) axis of the skull from taxon of all other alethinophidian snakes. This is an the tip of the snout to the occiput. The scan axis was important result, as it supports the hypothesis that offset from orthogonal approximately 9° on the trans- ‘Anomochilus might be an intermediate between verse axis and 10° on the frontal axis due to a fixed tilt living scolecophidian and alethinophidian snakes’ of the specimen's head relative to its body. Each slice (Cundall & Rossman, 1993: 236). If correct, this image was gathered at 1024 × 1024-pixel resolution, hypothesis has major implications either for under- resulting in an in-plane resolution of 5.4 µm per pixel. standing the interrelationships of basal snakes, or for Each slice represents a thickness of 14 µm, with understanding the ‘regression’ of the macrostomatan 14-µm interslice spacing. skull structure. The data set was rendered in three dimensions The interrelationships of Anomochilus can be fur- using VGStudio MAX 1.2 (Volume Graphics, Heidel- ther clarified by the inclusion of the second species, berg, Germany). The data volume was rotated to posi- A. leonardi. In order to prepare the ground for such tion the skull orthogonally, then three-dimensional future analysis we describe and illustrate the skull of (3D) cutaway views were generated along its true this species, and compare and contrast its anatomy orthogonal axes. Noise in the HRXCT data set, due to with that of A. weberi, scolecophidians, Anilius, the very small size of the specimen, causes the 3D ren- cylindrophines and uropeltines, as well as some basal derings to appear grainy. macrostomatans. The slices spanned by each element in the original This description of the skull of Anomochilus HRXCT data set are noted at the beginning of the leonardi is based on a high-resolution X-ray computed description of that element, and selected labelled tomographic (HRXCT) scan of a mature specimen HRXCT cutaway views (Figs 3–5) illustrate the inter- (FRIM 0026, Forest Research Institute Malaysia). nal anatomy of the skull in transverse (Tra), frontal HRXCT permits the non-destructive visualization of (Fro) and sagittal (Sag) planes. Original data set slice hard tissues in preserved specimens, and is particu- numbers are referenced throughout the description. larly useful when dealing with small, rare taxa such An interactive, web-deliverable version of the HRXCT as Anomochilus. data set, as well as animations of 3D reconstructions, can be viewed at http://www.digimorph.org/specimens/ Anomochilus_leonardi, and the original full resolution MATERIAL AND METHODS HRXCT data are available from the authors. The head of a whole preserved specimen (FRIM 0026) At certain points in the description below, the Ano- was scanned at the High-Resolution X-ray CT Facility mochilus leonardi data set is compared with HRXCT at The University of Texas at Austin. The specimen data sets for Typhlops jamaicensis (Typhlopidae; was collected on the campus of the Forest Research USNM 12378, National Museum of Natural History), Institute Malaysia, Kepong, Selangor State, Malaysia. Leptotyphlops dulcis (Leptotyphlopidae; TNHC 60638, The skull measures 6.8 mm in length and 2.9 mm Texas Natural History Collection, Texas Memorial across the otic capsules. The snout–vent length of the Museum), Anilius scytale (Aniliidae; USNM 204078), specimen is 251 mm and its total length is 257 mm Loxocemus bicolor (Loxocemidae; FMNH 104800, (Yaakob, 2003). The scanned specimen is thus compa- Field Museum of Natural History), Xenopeltis unicolor rable in size (length) with the other specimens from (Xenopeltidae; FMNH 148900), Python molurus Peninsular Malaysia with total lengths ranging from (Pythonidae; TNHC 62769), Aspidites melanocephalus 220 mm (Lim & Mohd. Sharef, 1975) to 228 mm and (Pythonidae; FMNH 97055), Casarea dussumieri 227 mm, respectively (Stuebing & Goh, 1993), but is (Bolyeriidae; UMMZ 190285, University of Michigan smaller than the Sabah specimen with a total length Museum of Zoology), Boa constrictor (Boidae; FMNH of 390 mm (Stuebing & Goh, 1993). 31182), Calabaria reinhardtii (Boidae; FMNH

SKULL OF THE MALAYSIAN SNAKE ANOMOCHILUS LEONARDI 673

117833), Lichanura trivirgata (Boidae; YPM 12869, canal anterior opening; Vcp, Vidian canal posterior Yale Peabody Museum), Epicrates striatus (Boidae; opening; vf, vagus foramen; vm, vomer medially USNM 59918) and Eryx colubrinus (Boidae; FMNH ascending flange; vnf, vomeronasal foramen; vp, 63117). vomer palatal shelf; V3r, recess for mandibular branch of trigeminal nerve. Key to figure abbreviations: a, angular; aar, anterior ampullary recess; adf, adductor fossa; aetc, anterior exit from trigeminofacialis chamber; af, apical fora- MORPHOLOGICAL DESCRIPTION men; am, anterior mylohyoid foramen; an, acoustic THE DERMATOCRANIUM nerve foramen; arf, articular fossa; avs, anterior vertical semicircular canal; bo, basioccipital; br, breakage; The skull of Anomochilus leonardi is characteristic of Downloaded from https://academic.oup.com/zoolinnean/article/149/4/671/2630933 by guest on 30 September 2021 cb, compound bone; cbc, compound bone coronoid pro- fossorial snakes, with a broad snout and a broad yet cess; cc, crista circumfenestralis; ccf, cerebral carotid streamlined braincase (Fig. 1). As noted by Cundall & foramen; co, coronoid; ctf, chorda tympani foramen; d, Rossman (1993: 268, fig. 25), the snout construction in dentary; dpd, dentary posterodorsal process; dpv, den- Anomochilus is intermediate between the ‘outer shell tary posteroventral process; dt, dentary tooth; ec, design’ of scolecophidians and the ‘central rod design’ ectopterygoid; ef, endolymphatic foramen; en, external of uropeltines. The skull lacks the lateral expansion naris; f, frontal; fd, fovea dentis; ff, facialis foramen; fl, across the otic region that is seen in Anilius, Cylin- frontal laterally descending flange; fm, foramen mag- drophis and †Dinilysia (Estes, Frazzetta & Williams, num; fmp, frontal medially descending pillar; fo, fora- 1970). men; fp, frontal preorbital ridge; fv, fenestra The premaxilla (Tra 005-048) is edentulous in both vomeronasalis; hf, hypoglossal foramen; hs, horizontal species of Anomochilus, a character which this genus semicircular canal; lf, labial foramen; ls, laterosphe- shares with Cylindrophis and uropeltines (Rieppel & noid; lsf, laterosphenoid foramen; m, maxilla; mam, Zaher, 2002). In A. leonardi, the anterior transverse maxilla anterior medial process; marst, medial aper- premaxillary process has an evenly convex anterior ture of recessus scalae tympani; Mc, Meckel's canal; margin (Fig. 1D). Its lateral end very narrowly mf, mental foramen; mp, maxilla palatine process; mt, approaches the anterior end of the maxilla (Tra 024) maxillary tooth; n, nasal; na, nasal anteroventral pro- (Fig. 3A), with which it may have formed a mobile syn- cess; nd, nasal dorsal lamina; nm, nasal medially desmotic contact, as has been described for A. weberi descending flange; oc, occipital condyle; of, optic fora- (Cundall & Rossman, 1993). The posterior vomerine men; ooc, otooccipital; op, opisthotic; p, parietal; pa, processes are small, short, and taper to a blunt tip palatine; paa, palatine anterolateral process; pac, (Fig. 1C). They underlap the dorsally curved anterior palatine choanal process; pap, palatine pterygoid pro- ends of the vomers (Tra 045) (Fig. 4B). A premaxillary cess; par, posterior ampullary recess; pbs, paraba- foramen (premaxillary channel sensu Frazzetta, 1959; sisphenoid; pf, prefrontal; pff, prefrontal facial lobe; Kluge, 1993) opens on either side of the dorsally pfo, prefrontal orbital lobe; pl, parietal laterally ascending process near its base (Tra 028) (Figs 1A, descending flange; plf, perilymphatic foramen; pm, 5B). These channels become confluent within the pre- premaxilla; pma, premaxillary ascending process; maxilla (Tra 019) before forming a single opening on pmf, premaxillary foramen; pmn, premaxillary nasal its ventral surface (Tra 021) (Fig. 1C). This is a feature process; pmt, premaxillary transverse process; pmv, that Anomochilus shares with uropeltines (Rieppel & premaxillary vomerine process; pr, prootic; ps, parietal Zaher, 2002) and Anilius, but not Cylindrophis supraorbital process; psr, parasphenoid rostrum; psri, (Rieppel, 1977). In superficial dorsal view (Fig. 1B), parasphenoid rostrum interchoanal process; pt, ptery- the ascending process inserts between the anterior goid; ptp, pterygoid palatine process; ptq, pterygoid ends of the paired nasals. HRXCT sections show medi- quadrate process; ptt, pterygoid transverse process; ally descending flanges of the nasals tightly embracing pvs, posterior vertical semicircular canal; q, quadrate; the dorsal tip of the premaxillary ascending process qmc, quadrate mandibular condyle; qs, quadrate (Tra 036) (Figs 3A, 4B, 5A), obscuring it from view. The suprastapedial process; rcc, recessus crus communis; nasal process of the premaxilla (sensu Cundall & Ross- rp, retroarticular process; rst, recessus scalae tym- mann, 1993; Fig. 3) is relatively weakly developed pani; s, stapes; san, superior alveolar nerve passage/ (Fig. 4B), similar to the condition observed in Anomo- foramen; sc, sagittal crest; sf, surangular foramen; sm, chilus weberi. Its moderately expanded posterior edge septomaxilla; sml, septomaxilla lateral lamina; smnb, is encased in a gutter-like recess defined by the anter- septomaxilla nasal buttress; so, supraoccipital; sp, omedial corner of both septomaxillae (Fig. 5B). splenial; tc, trabeculae cranii; trc, trigeminofacialis Both maxillae (Tra 022-141) carry three marginal chamber; trcm, trigeminofacialis chamber medial tooth positions anteriorly (Fig. 1A, C), and two rela- opening; v, vomer; vc, vomerine canal; Vca, Vidian tively large labial foramina on the lateral surface

674 O. RIEPPEL and J. A. MAISANO

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na en paa mt ptt ptq f nd qmc p p DEpff so pma af na sml ooc fm fd en lf hf pmt qs oc cb rp mt mf d bo

Figure 1. Three-dimensional reconstruction of the skull of Anomochilus leonardi (FRIM 0026) based on HRXCT data. A, lateral view; B, dorsal view; C, ventral view with lower jaw digitally removed; D, anterior view; and E, posterior view. Scale bar = 1 mm. See key for abbreviations.

SKULL OF THE MALAYSIAN SNAKE ANOMOCHILUS LEONARDI 675

(Figs 1A, D, 3A) that convey cutaneous branches of the carries a lateral lamina that curves upward to contact superior alveolar nerve (Tra 038, 052). The maxilla of the nasal dorsal lamina (Tra 037) (Figs 3A, 5A). The alethinophidian snakes is characterized by the devel- septomaxillary lateral lamina extends along the nasal opment of an anterior medial process (Rieppel, 1977; to a level deep to the overlapping prefrontal, finally Scanlon & Lee, 2000). This process is only weakly tapering out via a short, slender posterior process (Tra developed in Anomochilus leonardi (Tra 031), and 060). Medially, the septomaxilla arches dorsally to underlaps the upward curving anterolateral tip of the form the nasal buttress and the thin roof of the septomaxilla (Fig. 3A). The posterior third of the max- vomeronasal chamber (Tra 042) (Figs 3A, 4A). The illa is edentulous, shallows in height (Fig. 1A) and car- septomaxilla encloses a longitudinal canal anterome- ries a posteromedially trending palatine process (Tra dially (Tra 044) that opens anteriorly through the api- 086) that tapers to a blunt tip (Fig. 1C). The palatine cal foramen (Tra 029) (Figs 1D, 5A), which conveys Downloaded from https://academic.oup.com/zoolinnean/article/149/4/671/2630933 by guest on 30 September 2021 process is received by an anterolaterally facing con- premaxillary and ethmoid branches of the trigeminal cavity on the anterior portion of the palatine (Fig. 3B). nerve (Oelrich, 1956). The canal is pierced posterodor- The superior alveolar nerve passes across the palatine sally by the vomeronasal foramen (Figs 3B, 5B) (sensu process. It remains superficially exposed in a groove Cundall & Rossman, 1993, fig. 66), which affords com- on the dorsomedial surface of the maxilla for some dis- munication between the vomeronasal and nasal cham- tance (Tra 073-050) before becoming fully enclosed in bers (Tra 087). a canal at a level between the two labial foramina The paired frontals (Tra 075-181) are slightly (Fig. 5B). In this respect, A. leonardi is intermediate shorter than the nasals. They meet the parietal in an between Cylindrophis, where the superior alveolar anteriorly concave suture, resulting in the develop- nerve is superficially exposed only across the medial ment of well-defined supraorbital processes of the palatine process of the maxilla, and uropeltines, parietal (Figs 1B, 3C). A small lateral projection of the where the nerve remains superficially exposed along preorbital ridge of the frontal narrowly separates the the entire dorsomedial surface of the maxilla (Rieppel prefrontal from the supraorbital process of the pari- & Zaher, 2002; Fig. 4; in Anilius, the superior alveolar etal along the dorsal margin of the orbit (Fig. 1A). This nerve enters a foramen near the posterior margin of is different from Anomochilus weberi, in which the the palatine process of the maxilla). As in Anomochi- prefrontal meets the supraorbital process of the pari- lus weberi (Cundall & Rossman, 1993), the ectoptery- etal, thus excluding the frontal from the dorsal margin goid establishes no contact with the maxilla in of the orbit (Cundall & Rossman, 1993). The laterally A. leonardi (Fig. 1B). descending flanges of the frontals meet each other dor- The paired nasals (Tra 003-091) are distinctly wider sal to the parasphenoid (parasphenoid rostrum), anteriorly than posteriorly, each bearing a triangular thereby completely enclosing the braincase (Tra 107) anteroventral process that curves ventrally to roof the (Figs 3D, 5A). The optic foramen opens anteriorly external naris (Figs 1B, D). Behind the anteroventral between the frontal and parietal (Tra 145) (Fig. 3D). process, the dorsal lamina of the nasal is supported Anterior and ventral to the optic foramen, the later- laterally by the dorsally curving lateral lamina of the ally descending frontal flange forms a distinct, vent- septomaxilla (Tra 037) (Fig. 1D, 3A). Anteromedially, rolaterally projecting ridge that extends towards but the nasal dorsal lamina is supported by the nasal but- does not contact the choanal process of the palatine tress of the septomaxilla (sensu Cundall & Rossman, (Tra 141), and that remains separated from the para- 1993; Fig. 5) that arises from the latter's anterodorsal sphenoid along its entire length (Fig. 3D). Anteriorly, surface (Tra 028) (Figs 3A, 4A). The medial descend- the frontal forms a medially descending pillar that is a ing flange of the nasal is narrow anteriorly, broaden- synapomorphy of alethinophidian snakes absent in ing posteriorly (Fig. 4B). It is supported by the scolecophidians (Tra 100) (Figs 3C, 4B). This pillar dorsomedial surface of the septomaxilla (Figs 3A, 5A). abuts its counterpart medially and the posteroventral Posteriorly, the medial descending flange of the nasal process of the nasal medial descending flange anteri- forms a distinct posteroventral process that abuts the orly (Fig. 4B). The medial frontal pillar closely posteroventrally trending medial frontal pillar (Tra approaches the lateral frontal flange, but does not 096) (Fig. 3B). Together, the posteroventral process of establish contact (Tra 105). A ventrolaterally directed the nasal medial flange and the nasal dorsal lamina foramen pierces the laterally descending frontal define a deep cleft that clasps the anterodorsal margin flange just posterior to the medial frontal pillars (Tra of the frontal (Tra 087) (Fig. 4B; preorbital ridge of 110) (Figs 3B, 5A). Previously unreported in snakes, frontal sensu Frazzetta, 1966, fig. 15; supraolfactory this foramen might transmit one or more eye-muscle process of frontal sensu Cundall & Rossman, 1993, nerves. fig. 5). Each of the paired prefrontals (Tra 035-133) is com- The paired septomaxillae (Tra 027-101) are wholly posed of a convex facial lobe (sensu Frazzetta, 1966) of enclosed within the nasal chamber (Figs 1D, 3A). Each nearly rectangular outline that follows the lateral

676 O. RIEPPEL and J. A. MAISANO

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Figure 2. Three-dimensional reconstruction of the lower jaw of Anomochilus leonardi (FRIM 0026) based on HRXCT data. A, lateral view; B, medial view; C, dorsal view; and D, ventral view. Scale bar = 1 mm. See key for abbreviations. margin of the nasal as it connects the frontal to the A postorbital (postfrontal, supraorbital) is absent. maxilla (Fig. 1B), and a concave orbital lobe (sensu The anterior edge of the azygous parietal (Tra 115- Frazzetta, 1966) that forms the anteromedial wall of 404) slightly underlaps the posterior edges of the fron- the orbit (Fig. 1A). The ventral margin of the orbital tals (Tra 177) (Fig. 1B). Posteriorly, the parietal con- lobe forms an anteriorly located narrow lateral foot tacts the supraoccipital in a broad, straight, process (sensu Frazzetta, 1966), which contacts the transversely orientated suture. There is a very poorly dorsomedial surface of the maxilla close to the ante- developed sagittal crest. The laterally descending rior margin of the palatine process (Tra 062). More ﬂanges of the parietal establish a sutural contact with posteriorly, the ventral margin of the orbital lobe the lateral margins of the parabasisphenoid along forms a broader medial foot process (sensu Frazzetta, their entire length (Tra 167-318) (Figs 1C, 4A, 5A). 1966), which rests on the dorsal surface of the palatine This contact is interrupted only by the anterior open- anterior to its medial choanal process (Tra 089). The ing of the Vidian canal (Tra 219) (Fig. 5A). Posteriorly, two prefrontal foot processes are separated by a con- the laterally descending ﬂange of the parietal broadly cavity in the ventral margin of the orbital lobe result- underlaps the anterior part of the otic capsule, extend- ing in a gap between the prefrontal, maxilla and ing backwards and inwards deep to the prootic (e.g. palatine (Fro 158) that presumably transmits the lac- Tra 348) (Figs 3E, 5A). rimal duct (Cundall & Rossman, 1993). A fairly wide Cundall & Rossman (1993) described the presence triangular gap also remains in the anteromedial cor- of a well-developed supratemporal in Anomochilus ner of the orbit between the prefrontal orbital lobe, the weberi, incorporated into the braincase wall as is typ- frontal, and the palatine (Fro 136). ical for ‘anilioids’ and †Dinilysia (Estes et al., 1970).

The left side of the skull of this specimen of A. leonardi end of the palatine process of the pterygoid (Tra 162) exhibits slight damage to the quadrate and otic cap- (Figs 1C, 3D, 4A). There are no palatine teeth in Ano- sule (Fig. 1A). This results in a spur of bone projecting mochilus, nor is there a differentiated anterior denti- from the otic capsule dorsal to the posterior end of the gerous process of the palatine that is characteristic of suprastapedial process of the quadrate (Tra 372). alethinophidian snakes with the exception of uropel- However, no such structure occurs on the undamaged tines. Indeed, the palatine of Anomochilus most right side of the skull, which confirms the absence of a closely resembles that of uropeltines in its general supratemporal in A. leonardi. This feature is shared morphology (Cundall & Rossman, 1993; Rieppel & with scolecophidians and uropeltines. Zaher, 2002). The paired vomers (Tra 027-144), together with the The paired pterygoids (Tra 158-379) are rather del- septomaxillae, define the vomeronasal chambers, the icately built in Anomochilus leonardi. Each bifurcates Downloaded from https://academic.oup.com/zoolinnean/article/149/4/671/2630933 by guest on 30 September 2021 bony enclosures of Jacobson's organ. The narrow ante- anteriorly (Tra 192) into a larger palatine process and rior end of the vomer overlaps the short premaxillary a smaller transverse (ectopterygoid) process (Fig. 1C). vomerine process (Tra 042) (Figs 1C, 4B). The vomer The palatine process projects anteriorly, tapering to a forms the medial, posterior and posterolateral mar- blunt tip as it underlaps the pterygoid process of the gins of the fenestra vomeronasalis, restricting the sep- palatine (Tra 162) (Fig. 4A). The transverse process is tomaxilla to the anterolateral margin (Fig. 1C). The little more than an anterolaterally directed pointed margin of the fenestra vomeronasalis formed by the spur that fails to contact the ectopterygoid (Fig. 1C). vomer is deflected ventrally (e.g. Tra 051). Behind this The elongate quadrate process of the pterygoid forms fenestra, the vomer forms an elongate triangular pal- an obliquely positioned, blade-like structure that atal shelf that tapers to a pointed tip below the choa- extends posteriorly to the medial surface of the man- nal process of the palatine (Tra 119) (Figs 1C, 3C, 4B). dibular condyle of the quadrate (Tra 346). The ptery- Medially, the vomer forms an ascending flange which, goid is toothless. together with the ventrally descending medial flange The paired ectopterygoids (Tra 111-198) are simple, of the septomaxilla, forms the medial wall of the vom- slender and flat with somewhat expanded anterior eronasal chamber (Tra 070) (Fig. 4B). The vomerona- ends (Figs 1B.C). As in Anomochilus weberi (Cundall sal cupola remains fenestrated medially, however (Tra & Rossman, 1993), the ectopterygoid does not contact 065), as is also the case in Anomochilus weberi the maxilla anteriorly or the pterygoid posteriorly, but (Cundall & Rossman, 1993, fig. 6). In A. leonardi, the rather is entirely embedded in the pterygomaxillary ventromedial part of the vomerine medially ascending ligament. The ectopterygoid forms a partial floor for flange is pierced by a canal (Fig. 3B) transmitting the the orbit. palatine branch of the facial nerve (Bellairs, 1949: 135; Oelrich, 1956). It opens anteriorly through a medioventrally facing foramen (Tra 092). Posteriorly, THE BRAINCASE the vomeronasal nerve enters the vomer through a The parabasisphenoid of Anomochilus leonardi (Tra single vomeronasal foramen (Tra 100) (Figs 3B, 5B), 121-396) is broad and shallow, with a smooth external as is also the case in A. weberi (Cundall & Rossman, surface that is ventrally convex posteriorly, but ven- 1993, fig. 6), as well as in ‘anilioids’ generally (Groom- trally concave anteriorly (Figs 1C, 4B), as is also the bridge, 1979b). In A. leonardi, the posterior ends of the case in Cylindrophis and uropeltines (Cundall & vomerine palatal shelf and medially ascending flange Rossman, 1993). There is no indication of a longitudi- form a recess that receives the anteromedial tip of the nal crest or any ventrolateral projections (‘basiptery- choanal process of the palatine (Tra 112) (Figs 3C, 4B). goid processes’) that would guide the movements of Each of the paired palatines (Tra 079-199) exhibits the pterygoid. Anteriorly, the parabasisphenoid grad- a wide anterolateral process that is somewhat ually tapers to a narrow plate located dorsal to the deflected laterally (e.g. Tra 090) (Figs 1C, 5B). The palatine choanal processes (e.g. Tra 149) (Fig. 5B). The anterolateral process has a distinct facet on its ventral contact area on the anterolateral corners of the para- surface that receives the palatine process of the max- basisphenoid for the paired trabeculae cranii is illa in a loose overlapping contact (Fig. 1C). At the pos- located near the level of the ventrolateral contact of teromedial corner of that facet the palatine forms a frontal and parietal (Tra 164) (Fig. 1C). Such an ante- deep, laterally open groove for the passage of the supe- riorly placed contact of the trabeculae with the para- rior alveolar nerve (Tra 112) (Fig. 3C). More posteri- basisphenoid is shared by Anomochilus and some orly, the broad choanal process curves dorsomedially uropeltines, whereas in Anilius and Cylindrophis this as it arches over the choanal tubes (Tra 126) (Figs 1C, contact occurs well behind the ventrolateral contact of 3C, 5B). The posterolateral end of the palatine is frontal and parietal. Anteriorly, the parabasisphenoid drawn out into a pterygoid process with a ventrolat- of Anomochilus leonardi extends into a short and slen- erally facing facet that receives the pointed anterior der parasphenoid rostrum (‘cultriform process’), which

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Figure 3. Three-dimensional cutaway views along the transverse axis of Anomochilus leonardi (FRIM 0026) based on HRXCT data. A, approximately 0.36 mm depth; B, approximately 1.29 mm depth; C, approximately 1.58 mm depth; D, approximately 1.97 mm depth; E, approximately 5.19 mm depth; F, approximately 5.81 mm depth; and G, approximately 5.94 mm depth. Scale bar = 1 mm. See key for abbreviations.

© 2007 The Linnean Society of London, Zoological Journal of the Linnean Society, 2007, 149, 671–685 SKULL OF THE MALAYSIAN SNAKE ANOMOCHILUS LEONARDI 679 extends anteriorly between the palatine choanal pro- curved suture (Fig. 1C). The sella turcica is very shal- cesses (e.g. Tra 135) (Figs 3D, 5B). low and located towards the posterior end of the Cundall & Rossman (1993) described an intercho- basisphenoid (e.g. Tra 344). A dorsum sellae is not anal process on the parasphenoid rostrum of Anomo- developed across the medial portion of the basisphe- chilus weberi, a ventral keel projecting between the noid. Cundall & Rossman (1993) described the Vidian choanal processes of the palatines. They found this canal of A. weberi as having a posterior opening feature to be shared with Cylindrophis and uropel- located within the basisphenoid but connected to the tines, but not with other snakes. The interchoanal pro- posterior trigeminal foramen by a groove, and an ante- cess of the parasphenoid rostrum is also present in rior opening between the parabasisphenoid and the A. leonardi (Tra 131) (Figs 3D, 4B, 5B), as well as in parietal. In A. leonardi, the posterior opening of the Anilius scytale, but it is absent in scolecophidians. A Vidian canal is located on the basisphenoid–prootic Downloaded from https://academic.oup.com/zoolinnean/article/149/4/671/2630933 by guest on 30 September 2021 less pronounced interchoanal process is also present suture just below the posteroventral corner of the lat- in Loxocemus bicolor and in a somewhat modiﬁed form erosphenoid (Tra 357) (Figs 3E, 4A). The single fora- in Xenopeltis unicolor, and indeed in most basal mac- men for the facialis (VII) nerve pierces the prootic at rostomatans examined (Python molurus, Aspidites the level of the posterior opening of the Vidian canal melanocephalus, Casarea dussumieri, Boa constrictor, (Fig. 4B). From there, the hyomandibular branch of Calabaria reinhardtii and Lichanura trivirgata). The the facialis nerve passes through a posterolaterally interchoanal process is almost fully reduced in Epi- facing foramen located below the recess of the man- crates striatus, and absent in Eryx colubrinus. Thus, dibular branch (V3) foramen (Tra 357). This condition the presence of an interchoanal process on the para- is reminiscent of that observed in Cylindrophis mac- sphenoid rostrum is an alethinophidian character that ulatus and some uropeltines (Rieppel & Zaher, 2002). may be reduced or lost in macrostomatans. The palatine branch of the facialis nerve enters the Posteriorly, the parabasisphenoid of Anomochilus Vidian canal, which continues anteriorly in the leonardi meets the basioccipital in a sigmoidally prootic–basisphenoid suture (Tra 343). Shortly behind

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Figure 4. Three-dimensional cutaway views along the sagittal axis of Anomochilus leonardi (FRIM 0026) based on HRXCT data. A, approximately 0.69 mm depth; and B, approximately 1.45 mm depth. Scale bar = 1 mm. See key for abbreviations.

© 2007 The Linnean Society of London, Zoological Journal of the Linnean Society, 2007, 149, 671–685 680 O. RIEPPEL and J. A. MAISANO the passage of the cerebral carotid into the cranial cav- nerve branch to the constrictor internus dorsalis mus- ity (Tra 332), the Vidian canal becomes fully enclosed culature (Rieppel, 1979a). within the basisphenoid (Tra 336). The (intracranial) The otico-occipital complex comprises the basioccip- cerebral carotid foramen is located at the level of the ital (Tra 376-475), paired prootics (Tra 320-428), anterior margin of the laterosphenoid (Tra 352) paired otooccipitals (fused opisthotic-exoccipital) (Tra (Figs 4B, 5B). Just anterior to the cerebral carotid 379-476), and supraoccipital (Tra 353-432). Cundall & foramen, the Vidian canal forms a shallow groove on Rossman (1993) described a restricted dorsal exposure the margin of the basisphenoid (Tra 331), which of the prootic between the supraoccipital, supratem- quickly flattens out. The anterior opening of the Vid- poral and otooccipital in Anomochilus weberi, a char- ian canal lies between the parabasisphenoid and the acter shared with Anilius and Cylindrophis. This laterally descending flange of the parietal (Tra 219) feature is absent in Anomochilus leonardi, due to the Downloaded from https://academic.oup.com/zoolinnean/article/149/4/671/2630933 by guest on 30 September 2021 (Fig. 5A) at the level where the pterygoid broadens to absence of a supratemporal. The supraoccipital of form the palatine and transverse processes (Fig. 1C). A. leonardi is exposed in dorsal view as a wide yet As described in A. weberi by Cundall & Rossman short element, meeting the parietal anteriorly in an (1993, fig. 4), there is a groove across the posterolat- essentially straight transverse suture, and the exoc- eral corners of the basisphenoid in A. leonardi, cipitals posteriorly in a sigmoidally curved suture although it is unclear whether it connects to a minute (Fig. 1B). The exoccipitals meet each other behind the foramen of unknown function. supraoccipital, excluding the latter from the dorsal The basioccipital in Anomochilus leonardi (Tra 376- margin of the foramen magnum. The surface of the 475) is roughly triangular, with a posterior projection supraoccipital is smooth, devoid of even a weakly that contributes to the occipital condyle (Fig. 1C). The developed sagittal ridge. convex ventral surface of the basioccipital is smooth, The bony labyrinth is formed by the prootic, otooc- with no indication of a longitudinal crest or facets for cipital and supraoccipital. The crista circumfenestralis the insertion of the hypaxial neck muscles. The exoc- is poorly developed in Anomochilus leonardi, with a cipitals contact each other above the basioccipital prominent ventral rim but only a narrow dorsal rim (Tra 434), excluding the latter from the margin of the overhanging the columellar footplate (e.g. Tra 381) foramen magnum (Figs 1E, 5A). Between the exoccip- (Fig. 3F). The posterior closure of the juxtastapedial itals, the occipital condyle carries a distinct fovea den- recess is poorly defined, leaving the vagus (jugular) tis (Tra 465) (Fig. 1E). The exoccipitals also contact foramen exposed in lateral view (Tra 418) (Fig. 1A). each other above the basioccipital in Cylindrophis, The prootic forms the prominent anterior part of the but not in scolecophidians or Anilius. The occipital ventral rim of the crista circumfenestralis, gaining a condyle of uropeltines is uniquely modified (Williams, discrete exposure in the basicranium lateral to the 1959). basisphenoid–basioccipital suture (Fig. 1C). The pos- A relatively narrow laterosphenoid closes the terior part of the ventral rim of the crista circumfenes- ‘trigeminofacialis chamber’ (Rieppel, 1979a) laterally tralis is formed by the otooccipital (e.g. Tra 398). The (e.g. Tra 332). The medial entry into the trigeminofa- fenestra vestibuli faces ventrolaterally, accommodat- cialis chamber is relatively small in Anomochilus ing the large columellar footplate (Tra 390) (Fig. 3F). leonardi, restricted by the broad posteromedial expan- On the medial wall of the otic capsule, the endolym- sion of the laterally descending parietal flange deep to phatic foramen is located between the prootic and the otic capsule (Tra 349) (Fig. 4B). The posterior opisthotic (Tra 379), to the exclusion of the supraoc- opening for the mandibular branch of the trigeminal cipital (Fig. 4B). There is a single opening for the entry nerve (V3) forms a deep, well-defined recess (Fig. 3E). of the acoustic nerve (VIII) into the otic capsule Anteriorly, the laterosphenoid closely approaches the (Fig. 4B). As a result, there is no differentiation of an laterally descending flange of the parietal (e.g. Tra internal auditory meatus. This is a character that 325), thus restricting the anterior exit from the A. leonardi shares with Cylindrophis (Rieppel, 1979a), trigeminofacialis chamber. This anterior exit is in fact but not with scolecophidians (Rieppel, 1979b) or other subdivided into two anteriorly facing openings ‘anilioids’ or basal macrostomatans (Rieppel, 1979a). (Fig. 1A). The smaller dorsal opening (Tra 333) possi- The medial aperture of the recessus scalae tympani is bly transmits a branch of the cerebral vein (Rieppel, located on the suture between the basioccipital and 1979a), whereas the larger ventral opening (Tra 336) opisthotic (Figs 3F, 4B). It opens laterally into the ven- transmits the maxillary (V2) branch of the trigeminal tral part of the crista circumfenestralis, somewhat pos- nerve. Such a subdivision of the anterior exit from the terior to the anterior margin of the fenestra vestibuli trigeminofacialis chamber is variably observed in but anterior to the perilymphatic foramen (Tra 401). specimens of Anilius and Cylindrophis. In Anomochi- Rieppel (1979a) described a fenestra pseudorotunda lus leonardi, the laterosphenoid itself is pierced by the that is characteristic of ‘anilioids’ (Anilius, cylindro- laterosphenoid foramen (Fig. 1A), transmitting a cid- phines and uropeltines with the exception of Pseudo-

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Figure 5. Three-dimensional cutaway views along the frontal axis of Anomochilus leonardi (FRIM 0026) based on HRXCT data. A, approximately 0.97 mm depth; and B, approximately 1.34 mm depth. Scale bar = 1 mm. See key for abbreviations. typhlops; Rieppel & Zaher, 2002). This condition cylindrophines and most uropeltines (where the exit of results from the fact that the perilymphatic foramen the perilymphatic duct from the otic capsule is sepa- does not open ventrally into the recessus scalae tym- rate from the recessus scalae tympani). pani as in other alethinophidians. Instead, the peri- The vagus foramen in Anomochilus leonardi is sub- lymphatic duct passes through a channel that opens divided internally (Fig. 4A), as is also the case in uro- separately into the juxtastapedial recess behind the peltines (Rieppel & Zaher, 2002). Two foramina in the stapedial footplate (Tra 405) (Fig. 3G). In Anomochi- medial wall of the otooccipital become conﬂuent (Tra lus leonardi, the separation of the perilymphatic fora- 417) before they open posterolaterally near the level of men from the recessus scalae tympani is incomplete. the posterior tip of the quadrate (Tra 420) (Fig. 1A). Thus, this taxon exhibits a condition intermediate Without histological data it is impossible to ascertain between the general alethinophidian condition (where whether the two medial foramina transmit the glos- the perilymphatic foramen opens ventrally into the sopharyngeal (IX) nerve root (dorsal) and vagus (X) recessus scalae tympani) and the condition in Anilius, nerve root (ventral), or the vagus nerve root (dorsal)

© 2007 The Linnean Society of London, Zoological Journal of the Linnean Society, 2007, 149, 671–685 682 O. RIEPPEL and J. A. MAISANO and a root of the hypoglossal nerve (XII) (ventral). As splenial near its posterior end (Tra 171). Anteriorly, in uropeltines (Rieppel & Zaher, 2002), a single, sep- the splenial tapers out without gaining any lateral arate and relatively large hypoglossal foramen pierces exposure (Fig. 2A). the exoccipital in a location well behind the vagus The angular (Tra 177-253) lies along the anteroven- foramen, just anterior to the occipital condyle (Tra tral aspect of the medial surface of the compound bone 423) (Figs 1E, 3D, 4B). (Fig. 2B), with virtually no lateral exposure (Fig. 2A). In Anomochilus weberi, the anterior end of the angular is tall enough to establish contact with the coronoid THE SPLANCHNOCRANIUM (Cundall & Rossman, 1993). In A. leonardi, however, The shaft of the quadrate (Tra 339-451) of Anomochi- the angular is much shorter anteriorly and does not lus leonardi is short and terminates ventrally in a contact the coronoid (e.g. Tra 182) (Fig. 2B). Unlike in Downloaded from https://academic.oup.com/zoolinnean/article/149/4/671/2630933 by guest on 30 September 2021 moderately transversely expanded mandibular A. weberi, there is no posterior mylohyoid foramen in condyle (Fig. 1A, C). Posterodorsally, the quadrate the angular of A. leonardi. In having a well-developed extends into a suprastapedial process that is distinctly angular and splenial, Anomochilus approaches cylin- longer than the shaft. The quadrate articulates drophines and uropeltines more closely than Anilius directly on the otic capsule at a level well below the (Rieppel & Zaher, 2000). But whereas Cylindrophis latter's dorsal margin (Fig. 3D), a feature shared with retains a coronoid–angular contact, this contact is lost uropeltines. As noted by Cundall & Rossman (1993), in uropeltines (Rieppel & Zaher, 2000). the quadrate of Anomochilus most closely resembles The coronoid (Tra 174-235) is also smaller in Ano- that of uropeltines, and to some degree that of mochilus leonardi than in A. weberi. It forms an essen- Typhlops, although the shaft of the quadrate (bearing tially triangular plate of bone with weakly concave the mandibular condyle at its distal end) slants ante- anterior and posterior margins, and a weakly convex riorly in the latter taxon, whereas it is vertically ori- ventral margin (Fig. 2B). It closely approaches but entated in Anomochilus. does not contact or overlap the dentary, and it remains The stapes of Anomochilus leonardi (Tra 369-440) widely separated from the angular. The coronoid lies has a large footplate (Tra 387) and a short slender in apposition with the anteromedial surface of the shaft that meets the footplate at an acute angle (Tra coronoid process of the compound bone, anterior to the 403) (Fig. 3F). The shaft extends posterolaterally, ter- adductor fossa (e.g. Tra 190) (Fig. 2C). It gains only minating below the quadrate suprastapedial process limited lateral exposure (Fig. 2A), which is also the but not reaching the latter's posterior end (Figs 1A, case in A. weberi (Cundall & Rossman, 1993). 3G). Cundall & Rossman (1993: 249) described a car- The lateral (surangular) portion of the compound tilaginous rod ‘that lay along the entire dorsomedial bone (Tra 146-412) in Anomochilus leonardi forms a edge of the [suprastapedial process of the] quadrate.’ coronoid process before tapering to a tip in between the This points to the fact that the contact between stapes two posterior processes of the dentary (Fig. 2A). The and quadrate in Anomochilus corresponds to the pat- coronoid process of the compound bone is pierced by a tern observed in other ‘anilioids’ (Rieppel, 1980). large, anterolaterally facing anterior surangular foramen (Tra 198). The adductor fossa is relatively small (Fig. 2C), with a smooth and rounded medial margin THE LOWER JAW that lies lower than its lateral margin (Tra 238) The lower jaw of Anomochilus leonardi comprises the (Fig. 2B). In this respect, Anomochilus again resem- dentary, coronoid, splenial, angular and compound bles cylindrophines and uropeltines more closely than bone (Fig. 2). The dentary (Tra 028-218) carries six Anilius (Rieppel & Zaher, 2000). The articular fossa is teeth, with a large mental foramen near its anterior relatively shallow, and a large chorda tympani fora- end (Tra 060) (Figs 2D, 3A). Its posterior end is bifur- men pierces the medial surface of the short yet dis- cated, the posteroventral process being longer and tinct, spatulate retroarticular process (Tra 355) more massively built than the posterodorsal process (Fig. 2B). In Anomochilus weberi, the retroarticular (Fig. 2A). Meckel's canal remains wide open along the process forms a small dorsal projection directly behind ventromedial aspect of the dentary (Figs 2B, 3B–D). the articular fossa that wraps around the posterior The splenial (Tra 127-196) is a relatively small, aspect of the quadrate mandibular condyle (Cundall & slender element lying along the ventromedial margin Rossman, 1993, fig. 13). A similar projection is absent of the dentary (Figs 2B, 3D). Its posterior end abuts on the retroarticular process of A. leonardi. the anterior end of the angular in a poorly defined, roughly straight contact (Fig. 2B). Unlike in Anomo- DISCUSSION chilus weberi, the posterior end of the splenial of A. leonardi is not tall enough to bridge Meckel's canal Using their osteological data (38 characters), Cundall fully. A large anterior mylohyoid foramen pierces the et al. (1993, fig. 3) found Anomochilus to be the sister-

© 2007 The Linnean Society of London, Zoological Journal of the Linnean Society, 2007, 149, 671–685 SKULL OF THE MALAYSIAN SNAKE ANOMOCHILUS LEONARDI 683 group of uropeltines. Using total evidence (Cundall (Cundall & Rossman, 1993). Anomochilus shares the et al., 1993, fig. 2), however, Anomochilus was found to following with uropeltines: the elongate quadrate be the sister-taxon of all other alethinophidian snakes. suprastapedial process; the quadrate articulation low By virtue of the presence of medial frontal pillars, a on the otic capsule; the loss of a supratemporal (in laterosphenoid and an interchoanal process on the A. leonardi); the absence (loss) of an anterior dentiger- parasphenoid rostrum, Anomochilus qualifies as an ous process of the palatine; the anterior displacement alethinophidian snake. of the contact between the trabeculae cranii and the Increasing the number of cranial characters to 89, parabasisphenoid; the internal subdivision of the Tchernov et al. (2000) recovered a monophyletic Anil- vagus foramen; the single enlarged hypoglossal fora- ioidea, and found Anomochilus to be the sister-taxon of men in the exoccipital behind the vagus foramen; and uropeltines. The characters that diagnose Anilioidea the lack of contact between coronoid and angular (in Downloaded from https://academic.oup.com/zoolinnean/article/149/4/671/2630933 by guest on 30 September 2021 in that analysis (Tchernov et al., 2000, supplementary A. leonardi). The superior alveolar nerve is superfi- data) are: anteroventrally slanting prefrontal cially exposed on the dorsal surface of the maxillary (c.i. < 1); enlarged surface for pterygoid articulation palatine process in Cylindrophis. It continues to be formed by the otooccipital as it contributes to the pos- superficially exposed along the posterior part of the teroventral part of the crista circumfenestralis dentigerous portion of the maxilla in A. leonardi, and (c.i. = 1); and presence of a fenestra pseudorotunda it is superficially exposed along the entire length of the (incomplete in Anomochilus, absent in Pseudo- maxilla in uropeltines. typhlops). The support for a monophyletic Anilioidea is Whether Anomochilus is the sister-taxon to all other therefore rather weak and requires further testing (a alethinophidians (Cundall et al., 1993), to uropeltines monophyletic Anilioidea is also not supported by only (Tchernov et al., 2000) or to Cylindrophis macu- molecular data: Vidal & David, 2004; Vidal & Hedges, latus (Gower et al., 2005), the skull of A. leonardi 2004). The characters in the Tchernov et al. (2000) appears to be subject to some degree of paedomorpho- analysis that support the sister-group relationship of sis, even more so than the skull of A. weberi. This is Anomochilus with uropeltines are: contact of the based on the absence of a supratemporal, the rela- supraorbital process of the parietal with the prefron- tively smaller splenial, angular and coronoid, and the tal (c.i. = 1; but absent in A. leonardi); absence of an less complex retroarticular process in A. leonardi. anterior medial foramen on the maxilla (c.i. = 1); lack Paedomorphosis is involved in the reduction of the of expansion of the braincase at the level of the sus- ectopterygoid in Anomochilus, as well as the reduction pensorium (c.i. < 1); absence of an anterior dentiger- of other palatal bones and their dentition in Anomo- ous process on the palatine (c.i. < 1); edentulous chilus and uropeltines. The superficial exposure of the pterygoid (c.i. < 1); quadrate shaft much shorter than superior alveolar nerve along the maxilla is another the suprastapedial process (c.i. = 1); articulation of the paedomorphic feature of Anomochilus and uropeltines quadrate low on the otic capsule (c.i. < 1); and mor- (Rieppel & Zaher, 2002). Nevertheless, Anomochilus phology of the retroarticular process (in A. weberi; evolved a ‘central rod design’ of the skull in adaptation c.i. < 1). A recent molecular study (Gower et al., 2005) to a fossorial lifestyle (Cundall & Rossman, 1993: found Anomochilus to be the sister-taxon to Cylindro- 269). It is comparable with that of basal uropeltines phis maculatus, the two together forming the sister- with a loose premaxillary–maxillary contact (Mel- group to uropeltines. anophidium: Rieppel & Zaher, 2002), but different The present study of Anomochilus leonardi rein- from that of scolecophidians, which are characterized forces the signal for uropeltine affinities, although this by an ‘outer shell design’ of the skull (Cundall & hypothesis will require corroboration by a total Rossman, 1993). evidence analysis to be presented elsewhere. Never- The medial frontal pillars supporting the naso-fron- theless, many characteristics of the cranial anatomy of tal joint (Frazzetta, 1966; Rieppel, 1978) appear to be A. leonardi are, indeed, uniquely shared by cylindro- the principal element involved in the evolution of the phines and/or uropeltines amongst basal snakes. ‘central rod design’ (Cundall & Rossman, 1993) as an Anomochilus shares with Cylindrophis the contact of adaptation to burrowing, as it is seen in Anomochilus the exoccipitals above the basioccipital in the occipital and uropeltines. This contrasts with the ‘outer shell condyle, and the single opening for the entry of the design’ (Cundall & Rossman, 1993) that is typical of acoustic nerve into the otic capsule. The premaxilla is scolecophidians. In the context of the debate on the edentulous in Anomochilus, Cylindrophis and uropel- phylogenetic relationships of the mid-Cretaceous fos- tines, and the premaxillary channels are ventrally sil snakes with well-developed hind limbs (see Intro- confluent in Anomochilus and uropeltines (as well as duction), it has been argued that scolecophidians and in Anilius: Rieppel, 1977). The ventrally concave ante- ‘anilioids’ might be ‘regressed macrostomatans’ (Rage rior portion of the parabasisphenoid is another feature & Escuillié, 2000, 2003; G. Underwood, pers. comm.). shared by Anomochilus, Cylindrophis and uropeltines This position may derive additional support from

© 2007 The Linnean Society of London, Zoological Journal of the Linnean Society, 2007, 149, 671–685 684 O. RIEPPEL and J. A. MAISANO recent molecular studies suggesting a very basal posi- snakes. 1. Proceedings Koninklijke Nederlandse Akademie tion of Trachyboa and Tropidophis among alethi- van Wetenschappen 54C: 1–8. nophidian snakes (Vidal & David, 2004; Vidal & Coates M, Ruta M. 2000. Nice snakes, shame about the legs. Hedges, 2004), resulting in paraphyly of Macrosto- Trends in Ecology and Evolution 15: 503–507. mata as traditionally conceived (see also Gower et al., Cundall D, Rossman DA. 1993. Cephalic anatomy of the rare 2005). Most recently, Kley (2006) supported a ‘regres- Indonesian snake genus Anomochilus. Zoological Journal of sive evolution’ of scolecophidians as a consequence of the Linnean Society 109: 235–273. paedomorphosis. Scolecophidians long have been Cundall D, Wallach V, Rossman DA. 1993. The systematic known for a ‘vexing mixture of primitive and derived relationships of the snake genus Anomochilus. Zoological Journal of the Linnean Society 109: 275–299. characters’ (Kley, 2006: 510), where the modification Estes R, Frazzetta TH, Williams EE. 1970. Studies on the Downloaded from https://academic.oup.com/zoolinnean/article/149/4/671/2630933 by guest on 30 September 2021 (‘telescoping’: Haas, 1930) of the snout that results in fossil snake Dinilysia patagonica Woodward. Part I. Cranial the ‘outer shell design’ unquestionably represents an morphology. Bulletin of the Museum of Comparative Zoology autapomorphy of the clade. In contrast, the absence of 140: 25–74. the laterosphenoid as well as of medial frontal pillars Frazzetta TH. 1959. Studies on the morphology and function – two morphological characters that exclude scole- of the skull in the Boidae (Serpentes). Part 1. Cranial differ- cophidians from alethinophidians (Rieppel, 1988) – ences between Python sebae and Epicrates cenchris. Bulletin might well have resulted from paedomorphosis. of the Museum of Comparative Zoology 119: 453–472. Regression of the macrostomatan skull structure Frazzetta TH. 1966. Studies on the morphology and function involving paedomorphosis certainly might result in a of the skull in the Boidae (Serpentes). Part 2. Morphology skull structure similar to that of Anomochilus and and function of the jaw apparatus in Python sebae and uropeltines, where the medial frontal flanges are an Python molurus. Journal of Morphology 118: 217–296. integral component in the ‘central rod design’. Deriva- Gower DJ, Vidal N, Spinks JN, McCarthy CJ. 2005. The tion of the scolecophidian skull from an alethinophid- phylogenetic position of Anomochilidae (Reptilia: Serpentes): ian skull would require not only the loss of the medial first evidence from DNA sequences. Journal of Zoological frontal pillars through paedomorphosis, but also the Systematics and Evolutionary Research 43: 315–320. development of a much modified snout complex that Groombridge BC. 1979a. Variations in morphology of the resulted in the ‘outer shell design’. Ultimately, the superficial palate of henophidian snakes and some possible identification of paedomorphosis requires the prior systematic implications. Journal of Natural History 13: 661– establishment of sister-group relationships that pro- 680. vides a framework for the comparison of ontogenetic Groombridge BC. 1979b. On the vomer in Acrochordidae trajectories. Similarly, the derivation of scolecophidi- (Reptilia: Serpentes), and its cladistic significance. Journal of Zoology, London 189: 559–567. ans from macrostomatan (or alethinophidian) snakes Haas G. 1930. Über das Kopfskelett und die Kaumuskula- requires that scolecophidians be nested inside macro- tur der Typhlopiden und Glauconiiden. Zoologisches Jahr- stomatans (or alethinophidians), a phylogenetic signal buch, Abteilung für Anatomie und Ontogenie der Tiere 52: that has not been recovered. 1–94. Kley NJ. 2006. Morphology of the lower jaw and suspensorium in the Texas blindsnake, Leptotyphlops dulcis (Scole- ACKNOWLEDGEMENTS cophidia: Leptotyphlopidae). Journal of Morphology 267: We are grateful to Norsham Yaakob (Forest Research 494–515. Institute Malaysia) for making the specimen available Kluge AG. 1993. Aspidites and the phylogeny of pythonine for HRXCT scanning. Scanning was performed by snakes. Records of the Australian Museum Supplement 19: Matthew Colbert. Funding for scanning and image 1–77. processing was provided by an NSF grant (EF- Lee MSY. 2005. Squamate phylogeny, taxon sampling, and 0334961) to Maureen Kearney and Olivier Rieppel, data congruence. Organisms, Diversity and Evolution 5: 25– 45. The Field Museum. Lee MSY, Caldwell MW. 1998. 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