(Anguimorpha, Anguidae) from the early Miocene

Historical Biology An International Journal of Paleobiology

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The first record of anguine lizards (Anguimorpha, Anguidae) from the early Miocene locality Ulm – Westtangente in Germany Jozef Klembara, Miroslav Hain & Andrej Čerňanský To cite this article: Jozef Klembara, Miroslav Hain & Andrej Čerňanský (2017): The first record of anguine lizards (Anguimorpha, Anguidae) from the early Miocene locality Ulm – Westtangente in Germany, Historical Biology, DOI: 10.1080/08912963.2017.1416469 To link to this article: https://doi.org/10.1080/08912963.2017.1416469

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Date: 28 December 2017, At: 08:45

Historical Biology, 2017 https://doi.org/10.1080/08912963.2017.1416469

The first record of anguine lizards (Anguimorpha, Anguidae) from the early Miocene locality Ulm – Westtangente in Germany Jozef Klembaraa, Miroslav Hainb and Andrej Čerňanskýa a

Faculty of Natural Sciences, Department of Ecology, Comenius University in Bratislava, Bratislava, Slovakia; bSlovak Academy of Sciences, Institute of Measurement Science, Bratislava, Slovakia

Downloaded by [188.167.250.129] at 08:45 28 December 2017

ABSTRACT

The first fossil anguine material from the lower Miocene (MN 2) locality Ulm – Westtangente in Germany is described. The parietal and compound bone of the lower jaw can be attributed to Ophisaurus holeci, previously known only from younger age (MN 3–MN 7). Moreover, the parietal represents the largest parietal of this species. In other disarticulated material, such as frontal, maxilla, dentary and osteoderms, alpha taxonomy is not possible and these elements cannot be allocated at the species level. Despite a limited data source, a phylogenetic analysis was done (16 taxa, 36 characters) producing four equally parsimonious trees. The analysis shows a close relationship of O. holeci and the Eocene Ophisauriscus quadrupes. These two taxa form a monophyletic clade, a sister-clade to Ophisaurus + Anguis. However, more complete skeletal material of O. holeci is needed to support such a statement. We used our phylogenetic analysis to analyze trace character history for one frontal and three parietal characters. The palaeoenvironmental conditions of the locality Ulm – Westtangente bring further support of the previous hypothesis that O. holeci was adapted to environments with high ground water levels – environments around lakes or rivers.

Introduction The beginning of the Neogene is a very important time-period for the evolution of squamates, because the transition between the Oligocene and Miocene shows dramatic changes in European assemblages (for German Oligocene, see e.g. Böhme 2008; Čerňanský and Augé 2013; Čerňanský et al. 2016a). Following the comparatively cool and dry Oligocene, the return to a warm and humid climate by the earliest Miocene deeply influenced squamate fauna composition (Szyndlar and Rage 2003; Rage and Szyndlar 2005; Augé and Smith 2009). Such a prominent faunal turnover brought the modern squamate fauna to Europe (see Čerňanský et al. 2015). However, the anguines and other squamates from the early Miocene zone MN 2 have been only rarely reported from Europe. For squamates, a surprisingly rich assemblage, showing the first steps of modern squamates in Europe, has been reported from the locality Wiesbaden (Čerňanský et al. 2015). Among other anguimorphs, several anguines have been also described from this locality: Pseudopus cf. ahnikoviensis, Pseudopus sp. (these finds represent the oldest known record of Pseudopus), Ophisaurus spinari and Ophisaurus sp. Gerhardt (1903) described a new species of Ophisaurus as Ophisaurus ulmensis from the lower Miocene locality Ulm – Westtangente. The type material is represented by a mandible with amblyodont dentition. It is very likely that Gerhardt`s determination was based on the similar morphology of the dentition of his finds with that of the extant anguine taxon Pseudopus apodus.

KEYWORDS

Squamata; Ophisaurus; skeletal elements; anatomy; palaeobiodiversity

The original material was lost for a long time, but most of it has been found again recently, although its preservation is poor. First doubts about attribution of this material to the clade Anguinae have been suggested by Böhme and Ilg (2003). According to them, the Gerhardt`s material represented the remains of a cordylid (Scincoidea: Cordyliformes). Recently, based on new and more complete material, Čerňanský et al. (2016b) showed that the taxon is in fact sister to the Canary Island taxon Gallotia (Lacertidae) and a new generic name, Janosikia, was erected for this lacertid. Besides the remains of Janosikia (Čerňanský et al. 2016b), the new material described herein represents the first record of anguines at the locality Ulm – Westtangente. The aims of this paper are: (1) the detailed description of the new skeletal material of anguines from the German early Miocene locality Ulm – Westtangente, and (2) the evaluation of the frontal and parietal characters in the context of the evolution of anguines. Institutional Abbreviations: SMNS, Staatliches Museum für Naturkunde Stuttgart; AMNH, American Museum of Natural History, New York, U.S.A.; BSPG, Bayerische Staatssammlung für Paläontologie, Munich, Germany; CM, Carnegie Museum of Natural History, Pittsburg, U.S.A.; DE, Department of Ecology, Comenius University in Bratislava, Faculty of Natural Sciences Slovakia; MCZ, Museum of Comparative Zoology, Harvard University, Cambridge, Mass., U.S.A.; UF, University of Florida, Gainesville, U.S.A.; USNM, United States National Museum, Washington D.C., U.S.A..

CONTACT Andrej Čerňanský [email protected] Supplemental data for this article can be accessed https://doi.org/10.1080/08912963.2017.1416469 © 2017 Informa UK Limited, trading as Taylor & Francis Group

ARTICLE HISTORY

Received 4 October 2017 Accepted 9 December 2017

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Material and methods The individual bones described here are embedded in several blocks of matrix and there is no evidence that they belong to a single species (because of a different size, the elements certainly do not belong to one individual). Besides the parietal and compound bone of the lower jaw of Ophisaurus holeci, only a maxilla and dentary may be attributed to the same taxon on basis of a similar morphology of the dentition. The individual skeletal elements were photographed using a Leica M125 binocular microscope with axially mounted DFC500 camera; software: LAS (Leica Application Suite) version 4.1.0 (build 1264). The terminology of the anatomical structures is from Fejérváry-Lángh (1923), Klembara (1979), Klembara et al. (2010, 2014, 2017), Conrad (2004) and Evans (2008).


Comparative specimens used For comparisons, the skeletons of the following species of extant anguines were used: Anguis fragilis (DE 14–21, 24, 25, 45–48); Ophisaurus ventralis (DE 34, 35, 38; AMNH 73057; UF 52539; CM 1411), O. attenuatus (DE 32, 33, 43, 44; UF 57121), O. compressus (DE 50), O. mimicus (DE 49), O. koellikeri (DE 30, 41), O. harti (DE 36, 37, 56, 57, 86; AMNH 34956), O. gracilis (DE 42), Pseudopus apodus (DE 1, 3–13, 22, 23, 29, 52–54, 58, 59; BSPG 1982 X 2383). Comparisons are also based on descriptions and illustrations of extant anguimorphs Shinisaurus crocodilurus and Xenosaurus grandis (Conrad 2004; Bhullar 2011). The following specimens of extinct anguid taxa have been used: Odaxosaurus piger (USNM 10918, 10687; MCZ 3499, 3689, 3498); Peltosaurus granulosus (USNM 13870, AMNH 8138, 42913).

PAUP* 4b10 (Swofford 2002). We applied the heuristic search algorithm. Character evolution was analyzed in MESQUITE 2.75 (build 566; Maddison and Maddison 2011). We used Mesquite for optimizations and ancestral state determinations and visualization of all trees.

Geological setting The locality Ulm – Westtangente is located Nord-West of Ulm, 590 m above sea level (coordinates r 35 69 188, h 53 64 925). This locality has yielded 15 species of lower vertebrates and more than 45 mammalian species representing the richest vertebrate fauna from the early Miocene ever found in Germany. The age of the fauna is middle Agenian (MN 2a), lower Miocene (Heizmann et al. 1989). The fossils are preserved in the white-grey calcareous marls. For detailed information about sedimentology and a list of fossil taxa, see Heizmann et al. (1989). Systematic palaeontology Squamata Oppel 1811 Anguimorpha Fűrbringer 1900 Anguidae Gray 1825 Anguinae Gray 1825 Ophisaurus Daudin 1803 Ophisaurus holeci Klembara 2015 Figures 1, 2 Material -parietal SMNS 96576c; articulated surangular and articular + prearticular SMNS 96576b. Diagnosis -see Klembara (2015).

Description

Computed tomography

Parietal

All anguine elements from Ulm were scanned at Slovak Academy of Sciences in Bratislava (Slovakia). We used X-ray microCT tomography system Nanotom 180 (GE Phoenix) with the following settings: VxSize = 0.01142855; Current = 100; Voltage = 120; Inttime = 20,000; Average = 3; Steps = 1800; Steps360 = 1800. The images were recorded over 360°. The CT data-set was analyzed using VG STUDIO MAX 2.2 on a high-end computer workstation at the Slovak Academy of Sciences.

The parietal is completely preserved; its total anteroposterior length is 17.5 mm (Figure 1). The parietal table is anteroposteriorly elongated and of quadrangular shape (Figure 1(A), (B)). Its lateral margins converge gradually posteromedially. The anterolateral processes of the parietal table are well developed and have rounded margins. The parietal table is covered by an ornamented osteodermal surface divided into the four shields. The parietal table is slightly longer than wide. The ornamentation is distinctly developed and consists of densely arranged ridges, tubercles and deep grooves and pits. The radially arranged elongated grooves and ridges are present on the periphery of the ornamented surface. The lateral margins of the ornamented surface converge slightly medially. The parietal foramen lies slightly posterior to the mid-length of the ornamented surface. Both interparietal and occipital sulci are distinctly developed. The anterior end of the interparietal sulcus ends medially to the anterolateral corner of the ornamented surface. There is a short transversally oriented junction of the interparietal and occipital sulci. The lateral margin of the lateral ornamented shield does not extend to the lateral margin of the parietal table; a narrow, uncovered surface is present between them. The occipital ornamented shield is of oval shape. The smooth area lying immediately posterior to the ornamented surface is anteroposteriorly slightly longer than the anteroposterior length of the occipital ornamented surface

Phylogenetic and Mesquite analyses A morphological data matrix (see Supplemental data 1) was developed and modified using 36 characters (see Supplemental data 2) primarily from Klembara (1981), Conrad et al. (2011), Klembara et al. (2014) and Klembara and Rummel (2016). The matrix comprises 36 characters scored for five extant anguine in-group taxa (Anguis fragilis, Ophisaurus ventralis, O. harti, O. koellikeri, Pseudopus apodus) and one xenosaurid (Xenosaurus grandis) in addition to the nine extinct taxa (Pseudopus pannonicus, P. laurillardi, P. ahnikoviensis, P. confertus, Ophisaurus holeci, Ophisaurus roqueprunensis, Ophisauriscus quadrupes, Odaxosaurus piger and Peltosaurus granulosus). Shinisaurus crocodilurus was used as an out-group. We analyzed the data matrix using maximum parsimony as an optimality criterion in


HISTORICAL BIOLOGY

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Figure 1. Ophisaurus holeci SMNS 96576c. Photographs of parietal in dorsal (A) and ventral (C) views. Virtual 3D reconstructions of the same parietal in dorsal (B) and ventral (D) views.

(measured in the median plane). The arcuate edge forms the posterior margin of the parietal table and extends posterolaterally on the dorsal surface of the supratemporal process; it touches the lateral margin of the supratemporal process, although it fades out here. A shallow parietal notch is present. On the ventral surface, the most conspicuous structure is the parietal cranial crest (Figure 1(C), (D)). The parietal cranial crest is a sharp wall, slightly concave in its mid-length. Laterally to the crest, a distinct muscular surface is present; its width is about one-third of the distance between the pineal foramen and parietal cranial crest. A short postfoveal crest is present. The posteromedian margin of the parietal table reaches anteriorly the level of the juxtafoveal crests. The supratemporal process is straight. The ventrolateral ridge of the supratemporal process is well developed and its anterior end joins the parietal cranial crest at the level of the posteromedian margin of the floor of the parietal fossa. Between the anteriormost portion of the ventrolateral ridge and the anterolateral margin of the supratemporal process, a short ventrolateral surface is present. This surface lies posterior to the parietal cranial crest-supratemporal process junction and

is continuous anteriorly with the muscular surface of the parietal table. The anterior end of the supratemporal articulation lies posterior to the level of the posteromedian margin of the parietal table. The paroccipital process articulation is anteroposteriorly elongated and with a distinct ridge divided from the supratemporal articulation. Remarks The parietal described here can be attributed to Ophisaurus holeci on the basis of following combination of characters, some of which are diagnostic characters (Klembara 2015; Klembara and Rummel 2016): (1) the ornamentation of the parietal consists of short, pronounced anastomosing ridges and grooves and distinct pits; (2) the anterior end of the interparietal sulcus lies medial to the anterolateral corner of the ornamented surface; (3) the anterior end of the ventrolateral ridge of the supratemporal process joins the parietal cranial crest at the level of or slightly posterior to the posteromedian margin of the floor of the parietal fossa; (4) a long anterior section of the parietal cranial crest is more


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or less distinctly concave or straight; (5) the posterior section of the parietal cranial crest is very low, especially in place of its junction with the posterolateral ridge of the supratemporal process; (6) the supratemporal process is straight; (7) the base of the supratemporal process is mediolaterally narrow; and (8) presence of a short postfoveal crest (a similar crest is present also in O. fejfari, however, O. fejfari lacks the characters 1–5 above). Comments to ontogeny of parietal. The parietal of O. holeci described here represents the largest parietal of this species (Figure 1). The parietal of one small specimen of O. holeci was described from the locality Öhningen in Germany (Čerňanský and Klembara 2017) and it represents the smallest parietal of this species. Intermediate sized parietals of O. holeci were described from the early Miocene of the Czech Republic (Klembara 2015; Klembara and Rummel, 2016). The following ontogenetic changes of the parietal of O. holeci may be recognized:

process is absent. In the largest parietal, a short ventrolateral surface along the anterolateral margin of the supratemporal ridge and continuously passing anteriorly into the muscular surface is present. The same condition is present in large specimens of Pseudopus ahnikoviensis (Klembara 2012) and middle Eocene Ophisauriscus quadrupes (Sullivan et al. 1999; personal observation of J.K.). (5) In the smallest parietal, the length of the postfoveal crest is about one fifth of the length of the juxtafoveal crest. In the largest specimen, the length of the postfoveal crest is about one third of the length of the juxtafoveal crest (Figure 1(C), (D)). The elongation of the postfoveal crest in ontogeny is well documented also in Ophisaurus fejfari (Klembara and Rummel, 2016) and Pseudopus apodus (Klembara et al. 2017).

(1) In the smallest parietal, the lateral margins of the dorsal ornamented surface coincide with the lateral margins of the parietal table. In the largest parietal, there is a distinct unornamented surface between the lateral margin of the ornamented surface and the lateral margin of the parietal table (Figure 1(A), (B)). (2) In the smallest parietal, the anteroposterior length of the posterior smooth surface (area levis) is twice as long as the length of the occipital ornamented shield (measured in the median plane). In the middle-sized and the largest specimens, the length of the smooth surface and that of the occipital ornamented shield are about the same (Figure 1(A), (B)). Such a long smooth surface as present in the smallest specimen of Ophisaurus holeci is present in adults of middle Eocene anguines like Ophisauriscus quadrupes from Germany (Klembara 1981; Sullivan et al. 1999), late Eocene Headonhillia parva and Ophisaurus sp. from Great Britain (Klembara and Green 2010) and the Upper Cretaceous Odaxosaurus piger from North America (Meszoely 1970 and Figure 4(A)). (3) In the smallest parietal, the muscular surface (facies muscularis) is absent. In the middle-sized specimens, the muscular surface is only slightly indicated, but in the largest specimen it is well developed (Figure 1(C), (D)). The mediolateral width of the muscular surface increases during growth also in Pseudopus apodus (Klembara et al. 2017). The progressive widening of the muscular surface during growth was also recorded in the early Miocene P. ahnikoviensis (Klembara 2012). (4) In the smallest parietal, as well as in the middle-sized parietals, the ventrolateral surface of the supratemporal

The ontogeny and evolution of these and other anguine characters are discussed below. Surangular and articular + prearticular The surangular is posteriorly fused with the articular + prearticular forming a compound bone (Figure 2). The retroarticular process, although not completely preserved, is estimated to be of quadrangular shape. Its dorsal surface is concave. The glenoid fossa faces dorsally and slightly medially. Immediately posteriorly to it, a small foramen for the chorda tympani is present. On the medial surface of the compound bone, two small foramina lie immediately anteriorly to the glenoid fossa. The adductor fossa is anteroposteriorly elongated, deep and of elliptical shape. Posteriorly to it, a large posteromedial surangular foramen is present. Anteriorly to the adductor fossa, a large coronoid articulation is present. The lateral surface of the compound bone is smooth and bears two foramina (Figure 2(A)). The large posterior surangular foramen lies anteriorly to the glenoid fossa. The anterior surangular foramen lies immediately posteriorly to the articular surface of the surangular process of the dentary. Immediately anteriorly to the mid-length of the compound element, the ventrolateral surface bears an elongated roughened area indicating the angular articulation. Remarks The morphology of the compound element described here is very similar to that of Ophisaurus holeci described recently from the middle Miocene of Germany (Čerňanský and Klembara, 2017). The only difference between these two compound elements is

Figure 2. Ophisaurus holeci SMNS 96576b. Virtual 3D reconstruction of articulated right surangular and articular + prearticular in lateral (A) and medial (B) views.

HISTORICAL BIOLOGY

the smaller size of that middle Miocene one. Because there are no other structural differences between the specimens from both German localities, we consider the compound element described here as belonging to O. holeci. Ophisaurus morphotype 1 Figure 3(A)–(C) Material -frontal SMNS 85974a.

Description


Frontal One complete frontal is preserved (Figure 3(A)–(C)). It is an elongated and slender element, with a mediolateral constriction slightly posterior to its mid-length. The ornamentation section covers most of the dorsal surface of the frontal and forms three shields of different sizes. The ornamentation consists of small tubercles, short ridges and deep grooves and pits. At all margins of the frontal shield, the ridges radially diverge. The largest shield is the frontal shield. It covers most of the dorsal surface of the bone. Its lateral and medial margins are parallel. The

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posteromedial margin of the frontal shield is slightly shorter than the posterolateral margin. The posteromedial margin of the frontal shield courses in anteromedial-posterolateral direction, while the posterolateral margin courses in the posteromedial-anterolateral direction. Posteriorly to the frontal shield there is a slightly ornamented shield, but only a very indistinct anteroposteriorly coursing sulcus divides it into the interfrontal and frontoparietal shields. Anteriorly to the frontal shield, a slightly sculptured nasal articulation is present. Laterally to the frontal shield, a smooth orbital margin is present. The posterolateral process of the frontal is well developed. Its anterolateral margin bears a distinct groove for the articulation with the postfrontal. On the ventral surface, the frontal cranial crest forms a deep wall along the lateral margin of the bone (Figure 3(C)). The crest is deepest in its mid-region. The crest is sharp anteriorly and blunt posteriorly. Its mid-section is sharp and inclined dorsolaterally. At the junction of the anterior and middle sections of the crest, a small process is present. The anterolateral margin of the frontal is distinctly grooved indicating a strong prefrontal articulation; the articulation extends slightly posterior to the

Figure 3. (A–C) Ophisaurus morphotype 1 SMNS 85974a, photograph of right frontal in dorsal view (A); virtual 3D reconstructions of the same frontal in dorsal (B) and ventral (C) views. (D–F) Ophisaurus morphotype 2, virtual 3D reconstruction of right maxilla SMNS 96576a in lateral (D) and medial (E) views; (F) photograph of right dentary SMNS 96577 in medial view.


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Figure 4. Odaxosaurus piger, photographs of parietal MCZ 3498 in dorsal (A) and ventral (B) views. Frontal MCZ 3499 in dorsal (C) and ventral (D) view. Dentary MCZ 3689 in medial (E) view and detail of teeth in medial view (F).

mid-length of the frontal. A small triangular parietal tab is present on the posterior margin of the frontal. Remarks Although the general shape of the frontal of Ophisaurus morphotype 1 is similar to that of O. holeci, it differs from that of O. holeci in the following features: (1) the anteromedial ornamented shield is absent; (2) the posteromedial margin of the frontal shield is much longer; (3) the posterolateral margin of the frontal shield is much shorter and less anterolaterally orientated; and (4) the middle section of the frontal cranial crest does not reach so far medially as in O. holeci (Klembara 2015). The frontal of Ophisaurus morphotype 1 is in several aspects similar to the frontals of Ophisaurus sp. 1 and Ophisaurus sp. 2 from the early Miocene of the Czech Republic (Klembara 2015), but it differs in several characters from them. Thus, it is not possible to attribute the frontal of the Ophisaurus morphotype 1 to any known species of Ophisaurus or its known morphotypes.

Ophisaurus morphotype 2 Figure 3(D)–(F) Material -maxilla SMNS 96576a; dentary SMNS 96577.

Description Maxilla The maxilla is almost completely preserved (Figure 3(D)–(E)). The lateral surface of the maxilla is smooth. There are six mental foramina preserved; the most posterior one is the largest. The nasal process is about twice as high as the dental portion. The dorsal portion of the nasal process is curved medially and its anterior portion bears a small foramen. The anterior margin of the nasal process is posteriorly concave. The supradental shelf is thin and medially expanded (Figure 3(E)). The superior alveolar foramen lies at the level of the posterior margin of the nasal process, that is also the position of the fourth tooth from posterior. A large palatine articulation lies

HISTORICAL BIOLOGY

immediately medially to the superior alveolar foramen. A distinct groove lying immediately laterally to the superior alveolar foramen marks probably the prefrontal articulation. A deep groove on the dorsal surface of the posterior half of the supradental shelf marks the jugal articulation. At the posteromedial end of the dental portion of the maxilla, a roughly perpendicularly lying surface marks the ectopterygoid articulation. The premaxillary process is partially preserved. A distinct depression divides the root portions of the external ramus from the internal septomaxillary ramus of the premaxillary process. The posterodorsal portion of the nasal process is slightly damaged, but a large prefrontal articulation is distinct at its internal surface. Posteroventrally to it, a distinct lacrimal articulation is present.


Dentary An incomplete right dentary is preserved (Figure 3(F)). The dentary is slender and slightly ventrally arched. The Meckel`s groove is open ventrally. The dental crest is mediolaterally narrow and curved ventrally. Dentition Implantation is pleurodont. The teeth are conical, curved mesially and distally, and have pointed tips. The mesial and distal cutting edges are well developed. The tooth bases are mesiodistally broad. Five maxillary teeth are well preserved and a fragment of a sixth one is also present. At least five additional tooth positions are also present. Although the anterior portion of the external ramus of the premaxillary process is broken, it may be estimated that at least 12 maxillary teeth were present. Four well preserved teeth and six tooth positions are preserved in the dentary. The anterior portion of the dentary is broken. Remarks The maxilla SMNS 96576a corresponds in its general features to those of Ophisaurus acuminatus from the lower late Miocene of Germany (Jörg 1965) and Anguinae morphotype 1 from the early Miocene of the Czech Republic (Klembara 2015). The same holds true for the morphology of the teeth as well. Anguinae indet. Figure 3(A) Material – six osteoderms SMNS 85974b.

Description Osteoderms The preserved osteoderms are rectangular and bear a low, but distinct medial ridge. Dorsally, the osteoderm bears a gliding surface which occupies about one third of its anterior surface; the remaining portion of surface is ornamented. The ornamentation consists of ridges and grooves diverging from the center of the ornamented surface. The lateral bevel is present. On the ventral surface, two nutrition foramina are present. Remarks. Such type of osteoderms comes from the dorsal portion of the integument. Osteoderms of similar morphology

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are present in early Miocene localities in the Czech Republic (e.g. Dolnice, see Klembara 1981), but also in the Eocene localities of the Hampshire Basin in Southern England (Meszoely and Ford 1976; Klembara and Green 2010). However, we do not know the morphology of the osteoderms of extinct Pseudopus species, like P. ahnikoviensis (Klembara 2012) and P. confertus (Klembara 2015; Klembara and Rummel, 2016) from the early Miocene of the Czech Republic, which are of a similar size as those of the contemporaneous species of Ophisaurus. Thus, we designate the osteoderms from Ulm as Anguinae indet.

Phylogenetic analysis It should be noted that all trees presented here are based only on limited fossil material. We restricted our analysis to frontal, parietal and lower jaw characters, because these skeletal elements are the only elements preserved in most of the fossil species of anguines (Klembara and Rummel, 2016 and Supplemental data 1). More complete fossil specimens of extinct anguines are needed to make any more corroborated conclusions. We have added the coding of Ophisaurus holeci based on the virtual 3D models of the parietal and compound bone of lower jaw, as well as available information on the morphology of frontal, parietal and compound bone of lower jaw of other specimens of O. holeci previously described by Klembara (2015), Klembara and Rummel (2016) and Čerňanský and Klembara (2017). Shinisaurus crocodilurus was set as outgroup and Xenosaurus grandis was added in order to test, whether the inclusion of a member of another anguimorph clade (a non-Anguidae lizard) had some effect on the composition of Anguinae (and Anguidae), mainly regarding the fossil taxa. All characters were equally weighted and unordered (ordering of multistate characters produced here only the different bootstrap frequencies, but did not change the results). Heuristic analysis in PAUP produced four equally parsimonious trees (tree length = 81 steps; consistency index CI = 0.5802; retention index RI = 0.6909; rescaled consistency index RC = 0.4009). The results of this analysis are as follows: (1) In all trees, Ophisaurus holeci and Ophisauriscus quadrupes form a monophyletic group with a strong bootstrap frequency of 0.83. This clade is sister to the Ophisaurus + Anguis clade (Figure 5). (2) The Oligocene Ophisaurus roqueprunensis is a sister taxon to all extant members of Ophisaurus used in our analysis (bootstrap frequency 0.51) forming together a monophyletic clade. This supports a previous attribution of this Oligocene taxon as a member of the Ophisaurus lineage (Augé 1992; Čerňanský et al. 2016a; Klembara and Rummel, 2016 Dopasia in Augé 2005; Augé and Smith 2009). An unambiguous synapomorphy of the clade Ophisaurus (except of O. holeci) is represented by the absence of the muscular surface. (3) In all trees (Figure 5(A)–(D)), Anguis + Ophisaurus form a monophyletic group; Anguis is always basal to Ophisaurus species (except of O. holeci). Synapomorphies of the clade Anguis + Ophisaurus (except of O. holeci) are as follows: (a) absence of a long postfoveal crest (longer than one half of length


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Figure 5. (A–D) Four most parsimonious trees recovered by PAUP* v. 4.0b10. (E) Consensus tree of four trees. (F) Bootstrap percentages on a 50% majority-rule consensus tree. Black cross marks indicate extinct taxa.

of juxtafoveal crest); (b) absence of the ventrolateral surface of the supratemporal process, which runs laterally to the ventrolateral ridge and gradually passing to the muscular surface anteriorly; (c) the shape of the supratemporal process: more-or-less widely expanded with the presence of an angle between the base and the rest of the supratemporal process. (4) Pseudopus apodus and P. pannonicus are sister taxa (bootstrap frequency 0.74) as well as P. ahnikoviensis and P. laurillardi (bootstrap frequency 0.66). In all four trees + consensus tree, these four species form a monophyletic group (Figure 5). However, it should be noted that the bootstrap analysis shows only very little support for their monophyly. Only in one tree, P. confertus is sister to all other species of Pseudopus (Figure 5(A)). The topology of this taxon is unresolved in the strict

consensus tree with respect of the rest of Pseudopus (Figure 5(E)). (5) Glyptosaurine lizard Peltosaurus granulosus is sister taxon to all other anguines in three trees (Figure 5(A)–(C)), however, Odaxosaurus piger is inside of Anguinae clade in all four trees (Figure 5(A)–(D) and see Discussion below), although its position in the bootstrap is unresolved.

Discussion The species Ophisaurus holeci was first described from the early Miocene locality Merkur (zone MN 3) in the Czech Republic (Klembara 2015). Localities where O. holeci has been found outside of the Czech Republic are Petersbuch 39-III (zone MN 5), Petersbuch 62 (zone MN 3) in Bavaria, Southern Germany


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(Klembara and Rummel, 2016) and Öhningen (MN 7; Čerňanský and Klembara, 2017). The locality Ulm – Westtangente in BadenWürttemberg is the fourth and the oldest locality (zone MN 2) that has yielded remains of O. holeci in Germany. The parietal of Ophisaurus holeci described here represents the largest parietal of this species. All parietals of O. holeci described previously (Klembara 2015; Klembara and Rummel, 2016; Čerňanský and Klembara, 2017) exhibit the same diagnostic features of this species, but the parietal described here shows the appearance of two features absent in all other smaller specimens of this species. These features are (1) the presence of a narrow muscular surface on the ventral surface of the parietal table, and (2) a short ventrolateral surface lying anterolaterally to the anterior end of the supratemporal ridge of the supratemporal process and immediately posteriorly to the supratemporal process – parietal cranial crest junction. Considering only the extant anguine genera like Ophisaurus, Anguis and Pseudopus, a wide muscular surface continuously passing posteriorly into the ventrolateral surface of the supratemporal process is present only in Pseudopus; the same holds true also for the presence of a long postfoveal crest. The muscular surface and the postfoveal crest are absent in extant Ophisaurus and Anguis. However, the revision of the previous finds of parietals and description of a new parietal of the fossil forms show that the muscular surface and the postfoveal crest appear in various grade of development in various fossil species of anguines. As demonstrated here, a narrow muscular surface and a short postfoveal crest are present in the largest specimen of O. holeci. The same is true as for the largest specimen of the early Miocene O. fejfari (Klembara and Rummel, 2016). Thus, the evaluation of significant characters for taxonomic and phylogenetic purposes strongly depends on the completeness of the fossil record and the ontogenetic stage of the specimen studied. As demonstrated here and elsewhere (Klembara et al. 2010; Klembara 2012, 2015; Klembara and Rummel, 2016), a moreor-less long ventrolateral surface of the supratemporal process is present on the parietal of several anguines like Ophisaurus holeci, O. fejfari, Ophisauriscus quadrupes and Pseudopus ahnikoviensis. However, this feature is also present in the largest specimens of extant Ophisaurus species like O. attenuatus and

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O. ventralis (Figure 6). In the parietal of both species, however, the muscular surface is not present. As it will result from the character analysis below, the appearance of this character of both species is reversal. Relationship and characters evolution We examined the relationship of Ophisaurus holeci to other anguine taxa based on available cranial and lower jaw elements. Ophisaurus holeci shares many morphological features with the middle Eocene Ophisauriscus quadrupes (see e.g. Klembara and Rummel, 2016; Čerňanský and Klembara, 2017). These character states are as follows: (1) Posterior section of the parietal cranial crest is very low at its junction with the anterior end of the posterolateral ridge of the supratemporal process. This can be regarded as an unambiguous synapomorphy of Ophisauriscus quadrupes and Ophisaurus holeci, if their monophyly is considered. (2) Length (measured in median plane) of the smooth area (area levis) is bigger than the length of the occipital ornamented shield. Such a character state is present only in Odaxosaurus piger, but no other anguine lizard. (3) Short postfoveal crest is present (shorter than one half of the juxtafoveal crest length). This character state is present in Pseudopus as well but not in Anguis and all other Ophisaurus species studied here. (4) Narrow muscular surface is present (about one third or less of width spanned between the parietal cranial crest and pineal foramen). Such a character state is present also in Odaxosaurus piger and Pseudopus confertus. (5) Anterior end of the ventrolateral ridge of the supratemporal process joins the parietal cranial crest at or slightly posterior to the level of the posteromedial margin of the parietal fossa floor. This is also present in Ophisaurus rocqueprunensis and Pseudopus pannonicus, but not other anguine lizard. (6) Supratemporal process is straight. This is present in Pseudopus (where it can be observed), but not in Anguis and all other Ophisaurus species studied here.

Figure 6. Photographs of parietals in ventral view of Ophisaurus attenuatus UF 57121 (A) and O. ventralis CM 1411 (B).


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Figure 7. Trace character history analysis in Mesquite: (A) The length of the posterolateral process of the frontal (extremely laterally expanded 0, well expanded, more than half of mediolateral length of the frontal in the mid-length 1, or less 2); (B) the length of area levis (relative to length of occipital ornamented shield; area levis: longer 0, of about the same length 1, shorter 2); (C) Postfoveal crest (absent 0, short – shorter than one half of juxtafoveal crest length 1, long – longer than one half of length of juxtafoveal crest 2); (D) Muscular surface (absent 0, present narrow – about one third or less of width between parietal cranial crest and pineal foramen 1, present wide – about one half of width between parietal cranial crest and pineal foramen 2).

(7) Čerňanský and Klembara (2017) showed that the pelvic girdle of Ophisaurus holeci is composed of three elements – ilium, pubis and ischium, as in Ophisauriscus quadrupes (see Sullivan et al. 1999), and the presence of small but functional limbs is suggested. In all extant members of Anguinae, the pubis and ilium are fused to form a puboischium. However, it should be noted that the morphology of the pelvic girdle of other extinct forms is largely unknown. In our phylogenetic analysis, Ophisauriscus quadrupes and Ophisaurus holeci are close relatives (bootstrap frequency = 0.83), forming together a clade. This clade is a sister lineage to the clade Ophisaurus + Anguis. Such a topology suggests that a new generic name would be justified for the Miocene species Ophisaurus holeci, because it is not monophyletic with other members of the clade Ophisaurus. However, we do not make this change here, because only limited material is attributed to this species and consequently a limited amount of data is available for the phylogenetic analysis. Future findings and more informative phylogenetic analyses would persuasively resolve the relationship of this taxon. As it is well-known, the same selective pressures of an environment can produce very similar morphologies even in not-closely related animals. Another reason of similarity is

usually a sharing of plesiomorphic character states. It is, however, very plausible that this taxon might represent an archaic lineage persisting to the Miocene and new, more complete skull material of O. holeci could bring more support for the generic change of this species in the future. Pseudopus confertus is nested with other members of Pseudopus clade only in one tree. This reflects an archaic morphology of this taxon which displays many plesiomorphic states. Another result of our analysis indicates that the Late Cretaceous and Paleocene Odaxosaurus piger from North America, previously placed in Anguinae (Meszoely 1970) and later in Glyptosaurinae (Sullivan 1979; Gauthier 1982; Longrich et al. 2012), might be in fact a very basal anguine (although bootstrap frequency is less than 0.50). Although the dentary of Odaxosaurus (Figure 4 (E), (F)) shows a glyptosaurine appearance (a glyptosaur-like dentition), its attribution to Anguinae is, on the other hand, supported by the ornamentation of the frontal and parietal ornamented shields. This type of ornamentation does not show the presence of any tubercles as is typical for the clade Glyptosaurinae (e.g. Peltosaurus granulosus, see Digimorph.org 2002–2012). In fact, the ornamentation of these bones in O. piger (Figure 4(A), (C)) resembles very closely to that of members of Anguinae (see Klembara and Rummel, 2016 and references there).


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For trace character history of one frontal and three parietal characters, one of the four equally parsimonious trees (Figure 5(A)) was used. Character optimization in Mesquite supports the presence of a long posterolateral process of frontal as the condition at the basal node of the clade Anguimorpha representing a plesiomorphy. The shortening of this process appeared in basal node of the clade Anguidae (Figure 7(A)). In the clade Pseudopus apodus + P. pannonicus, the reduction of this process is observed. The same character state appeared independently in Ophisauriscus quadrupes (see Figure 7(A)). Character state distribution in Mesquite supports the short smooth area of the parietal as being a plesiomorphy for the clade Anguinae. A distinct elongation of this area can be observed in Ophisauriscus quadrupes and Ophisaurus holeci (Figure 7(B)). The long postfoveal crest of the parietal is supported as being the plesiomorphy for Anguidae. Therefore, the long postfoveal crest in the Pseudopus apodus + P. pannonicus can be regarded as reversal (Figure 7(C)), because there is a change in the character in the tree between the basal anguid node and the node composing P. apodus + P. pannonicus. The absence of this crest characterizes the clade Anguis + Ophisaurus (without O. holeci). The large muscular surface of the parietal is a condition present at the basal node of Anguidae and character optimization in Mesquite supports the change (narrowing of the muscular surface) at the basal node in Anguinae. The presence of a large muscular surface in all Pseudopus, except for P. confertus, can be therefore regarded as reversal (Figure 7(D)). The absence of the muscular surface characterizes the clade Anguis + Ophisaurus (without O. holeci). Remarks on ecology The Ulm material represents the same age as that of Wiesbaden – Amöneburg, showing a broad distribution of anguine lizards in the early Miocene (MN 2) of Central Europe. The Wiesbaden – Amöneburg material is represented by skeletal remains coming from the lower brackish part of the Wiesbaden Formation, where numerous freshwater and terrestrial gastropods, including Gyraulus, Stagnicola and Planorbarius, also occur. The finds are often fragmented in situ, suggesting that formation of the microvertebrates horizon most likely resulted from sporadic but massive freshwater inflows into the lagoonal area (see Čerňanský et al. 2015). The Ulm material does not show evidence of a long transportation. The lower Miocene sediments of Ulm most likely represent a natural environment for Ophisaurus holeci in the early Miocene – an area around a lake. This supports a previous statement on the ecology of this taxon by Čerňanský and Klembara (2017) that this species used to live in the nearby of lakes or rivers. A huge amount of freshwater gastropods appears in the sediments of Ulm locality. This is followed by the occurrence of an amblyodont lacertid lizard – Janosikia ulmensis. Pseudopus has not yet been recognized in Ulm locality and it is possible that this taxon is absent here. This could be caused by a high level of diet competition with above mentioned lacertids occupying the same diet niche. In Wiesbaden, amblyodont lacertids are absent, but the oldest known Pseudopus is present there (P. ahnikoviensis; see Čerňanský et al. 2015). The occurrence of members of the anguine lizards close around lakes with a rich assemblage of gastropods and disappearance of lacertids

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with amblyodont dentition (e.g. Dracaenosaurus, Pseudeumeces or Janosikia) might have been an impulse for anguine to occupy this niche at the beginning of Neogene, and for a transformation of some of them to an amblyodont type (the Pseudopus clade).

Acknowledgement We are greatly indebted to Dr. Dieter Seegis and Dr. Rainer Schoch (Staatliches Museum für Naturkunde Stuttgart) who gave access to specimens. Mr. Olaf Vogel (Senckenberg Research Institute, Frankfurt am Main) prepared the specimens SMNS 96576a, b and 85974a. Special gratitude is to three reviewers (Arnau Bolet and two anonymous) whose careful and constructive comments had considerable impact on the improvement of this paper.

Disclosure statement No potential conflict of interest was reported by the authors.

Funding This project was supported by the Alexander von Humboldt Foundation of Germany.

ORCID Andrej Čerňanský

http://orcid.org/0000-0002-1314-026X

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