A reconsideration of S phaerodactylus dommeli Böhme, 1984 (Squamata: Gekkota: Sphaerodactylidae), a Miocene lizard in amber

Accepted on 22 August 2012 J Zoolog Syst Evol Res doi: 10.1111/jzs.12001

© 2012 Blackwell Verlag GmbH

1

Biology Department, Villanova University, Villanova PA, USA; 2Zoologisches Forschungsmuseum A. Koenig, Bonn, Germany

A reconsideration of Sphaerodactylus dommeli Böhme, 1984 (Squamata: Gekkota: Sphaerodactylidae), a Miocene lizard in amber J UAN D. D AZA 1 , A ARON M. B AUER 1 , P HILIPP W AGNER 1,2 and W OLFGANG B ÖHME 2 Abstract The Miocene gecko in amber, Sphaerodactylus dommeli, is one of the best-preserved fossil gekkotan species; nonetheless, its identity has been questioned and it has been insinuated to be an iguanian referable to the mega-diverse genus Anolis. In this paper, we provide digital X‐rays and new osteological evidence that include 11 characters that reaffirms its placement within the infraorder Gekkota and eight characters that specifically place this fossil within the species-rich genus Sphaerodactylus, in which it was originally described. This contribution seeks to eliminate remaining scepticism about the generic allocation of this species, and to provide a reliable calibration point for ongoing research in squamate phylogenetics, especially for biogeographical studies and molecular dating inference. This contribution also reviews many diagnostic characters for the two genera in question, which is critical for the correct identification of amber-embedded specimens representing the rich Hispaniolan lizard paleocommunity. Key words: Fossil – Anolis – digital X‐rays – osteology – anatomy – Domincan Republic

Introduction Sphaerodactylus dommeli Böhme, 1984 was described based on two specimens from the amber deposits of Hispaniola (Dominican Republic, La Toca Mine). These specimens, together with Yantarogekko balticus, include the best-preserved amber-embedded geckos reported in the literature (Böhme 1984; Poinar 1992; Bauer et al. 2005). Sphaerodactylus dommeli, S. ciguapa (Daza and Bauer 2012), and at least three more specimens (Schlee 1990; Kluge 1995; Grimaldi 1996; Grimaldi et al. 2000) represent the oldest records of the extant genus Sphaerodactylus, otherwise only known before the Holocene from disarticulated material from the late Pleistocene of Puerto Rico (Pregill 1981). These amber-preserved species document the presence of Sphaerodactylus in the Greater Antilles between 15 and 20 MYA (Grimaldi 1995; Iturralde-Vinent and MacPhee 1996), during or before an important stage of Caribbean tectonics, the formation of the Mona Passage, which resulted in the separation of Hispaniola and Puerto Rico (Iturralde-Vinent and MacPhee 1996; MacPhee et al. 2003). Sphaerodactylus fossils dated based on Dominican amber age estimations (Lambert et al. 1985; Grimaldi 1995; Iturralde-Vinent and MacPhee 1996) have been used as calibration points in recent molecular studies (Gamble et al. 2008a,b; Gamble et al. 2011a; Nielsen et al. 2011; Heinicke et al. 2011) and have provided comparisons for estimates of rates of evolution based on other data (Hass and Hedges 1991; Hedges et al. 1991; Hedges 1996). Indeed, S. dommeli is particularly critical in this regard, as there are few fossil-based calibration points within the Gekkota (Lee et al. 2009a; Oliver and Bauer 2011). The few putative gekkotans from the Mesozoic are of uncertain phylogenetic affinity (Alifanov 1989; Borsuk-Białynicka 1990; Arnold and Poinar 2008) as is the Early Eocene gecko Yantarogekko balticus (Bauer et al. 2005). Likewise, most other Tertiary gekkotans are known from fragmentary remains and cannot be Corresponding author: Juan D. Daza ([email protected]) Contributing authors: Aaron M. Bauer ([email protected]), Philipp Wagner ([email protected]), Wolfgang Böhme ([email protected]) Subsequent to the acceptance of this paper, we obtained high resolution X-ray computed tomography imagery for the paratype of Sphaerodactylus dommeli that confirms that it is correctly allocated to genus. Details of its osteology will be reported elsewhere.

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reliably situated in the gekkotan phylogeny. Miocene remains of geckos from St. Bathans, New Zealand have been used as calibration points (Lee et al. 2009a), but these are attributable to the Diplodactylidae, a family of Australo-Pacific geckos that is highly divergent from the Gekkonoidea, the clade to which approximately 85% of extant geckos belong. Likewise, Pygopus hortulanus from Riversleigh, Australia has been used for calibration (Jennings et al. 2003; Oliver et al. 2007; Smith et al. 2007; Gamble et al. 2008b), but in this particular case, there are some discrepancies on the estimated divergence dates, in part attributed to the uncertainty of the fossil’s phylogenetic position (Lee et al. 2009b). Aside from Sphaerodactylus in Dominican amber, the only fossil calibration point within the Gekkonoidea is provided by specimens of the sphaerodactylid Euleptes from the Miocene of Central Europe (Müller 2001; Müller and Mödden 2001; Augé 2005; Čerňanský and Bauer 2010). Given the significance of S. dommeli for understanding the evolution of geckos, it is necessary to address scepticism in the literature regarding its familial allocation. The specimens of S. dommeli exhibit a truly gekkotan habitus and, as was mentioned in the original description, both specimens have the distinctive asymmetric claw sheath of Sphaerodactylus (Böhme 1984; see also Parker 1926; Vanzolini 1957; Peters and DonosoBarros 1970; Schwartz 1973; Kluge 1995; Gamble et al. 2011b). Nonetheless, its assignment to the genus Sphaerodactylus has been questioned and it has been suggested that its general habitus (proportions of limbs, shape of head) is consistent with an anoline lizard (Frost in Kluge 1995). It has additionally been recommended that the type material of ‘Sphaerodactylus’ dommeli must be re-examined in order to correctly reclassify the species (Kluge 1995). This uncertainty has been repeated in several subsequent publications (MacPhee and Iturralde-Vinent 1995; de Queiroz et al. 1998; Pregill 1999). De Queiroz et al. (1998), based on published photographs of S. dommeli (Böhme 1984; Schlee 1990), determined that the distal position of the toe pads of the holotype was inconsistent with this specimen being an anole, but they did not comment on the paratype, because the toe pads were not clearly visible on the photographs available to them, leaving open the possibility that at least the paratype of S. dommeli might not be a gecko. In this paper, we review skeletal characters in the holotype and external morphology of the paratype of S. dommeli to provide evidence that refutes its identification as an Anolis (Kluge 1995). In order to verify the taxonomic allocation of S. dommeli,

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Fig. 1. Digital X-ray of the holotype of Sphaerodactylus dommeli in dorsoventral view (ZFMK 66238) showing the entire skeleton. Abbreviations: 1cb, first ceratobranchial; ac, acetabulum; at, atlas; ax, axis; ca6, caudal vertebra 6th; cv#, cervical vertebra #; clvf, clavicular fenestra; cr4, rib for the cervical vertebra 4th; fe, femur; fi, fibula; h, humerus; il, illium; pu, pubis; ra, radius; tp, tibial patella; ul, ulna; ti, tibia

we evaluate the presence of morphological characters used previously for diagnosing the Gekkota and the genus Sphaerodactylus. Additionally, we revise some anatomical characters used to describe this fossil taxon, such as its elongated neck (Böhme 1984), and compared it with representatives of all extant sphaerodactyl genera, including 42 congeners, among them S. ciguapa from the same fossiliferous geological formation.

Material and Methods Digital X-rays of the holotype of S. dommeli (ZFMK 66238) were obtained at the Zoologisches Forschungsmuseum Alexander Koenig, Bonn using a Faxitron® LX-60 Cabinet X-ray System (Faxitron Bioptics, LLC, Tucson, AZ, USA), set to 20 kV with a typical image acquisition time of 20 s. Additional specimens from 52 extant sphaerodactyl geckos, including representatives from each genus (viz. Chatogekko, Coleodactylus, Gonatodes, Lepidoblepharis, Pseudogonatodes, Sphaerodactylus) were X-rayed using a KevextTM (Thermo Fisher Scientific, Waltham, MA, USA) PXS10-16W Micron Spot MicroFocus X-ray Source and Varian Amorphous Silicon Digital X-ray Detector PaxScanH 4030R set to 130 kV at the United States National Museum (Smithsonian Institution). Specifically, we used all the reference material employed in the recent description of Sphaerodactylus ciguapa, another amber-embedded gecko from the same formation as S. dommeli (Daza and Bauer 2012), to address the claim that the holotype of S. dommeli is an anole, and morphometric data to show that this fossil is a distinct species of Sphaerodactylus differing from congeners in its body proportions. We considered all morphological characters available for diagnosing both Gekkota and ‘Polychrotidae’ s.l. (Estes et al. 1988; Frost and Etheridge 1989; Lee 1998; Conrad and Norell 2007; Conrad et al. 2007; Conrad 2008; Evans 2008; Smith 2009; Daza et al. 2012; see below) and evaluated their presence in the holotype. Anolis, the other lizard genus

J Zoolog Syst Evol Res (2013) 51(1), 55--63 © 2012 Blackwell Verlag GmbH

often found in Dominican amber and with which S. dommeli has been confounded, has long been included in the Polychrotidae. Phylogenetic data has demonstrated that ‘Polychrotidae’ is not monophyletic (Frost et al. 2001; Schulte et al. 2003; Schulte and Cartwright 2009) and Anolis has been removed to a family of its own, Dactyloidae (Townsend et al. 2011). Yet, characters of the Polychrotidae (sensu Estes et al. 1988; Etheridge and de Queiroz 1988) are both applicable to Anolis and well characterized and are used here for comparative purposes. We measured the length of the skull (from the anterior tip of the premaxilla to middle point of the occipital condyle), the cumulative length of the cervical vertebrae (the anteriormost eight vertebrae) and of the entire presacral vertebral column. These measurements were obtained from each specimen with Adobe® Illustrator® CS3 software (Adobe Systems Incorporated, San Jose, CA, USA). Measurements from X-rays may help to reduce the error associated with measurements made when viewed through amber, which has a refractive index (n) of 1.55. Both skull and cervical length were plotted against the presacral length using R (R Core Team 2012) in order to visualize the correlations between these variables.

Results Why S. dommeli is not an iguanian Sphaerodactylus dommeli can be differentiated from iguanian ‘polychrotids’ by ten characters: (1) subolfactory processes of frontal in contact at midline, (2) lack of rugosities in skull dermal roofing bones (although Diplolaemus and some anoles also lack these), (3) jugal and squamosal not in contact, (4) parietal not trapezoidal or V- or Y-shaped, (5) pineal foramen of parietal absent, (6) retroarticular process with medial offset and lateral

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Fig. 3. Lateral view of the right manus of the holotype of Sphaerodactylus dommeli (ZFMK 66238). Digits IV and III show better the characteristic asymmetrically enlarged ungual sheath. Abbreviations: I–V, indicates manual digit number; oil, outer infero-lateral scale (=ventro-lateral in Kluge 1995) Photograph by Wolfgang Weitschat

scales and (7) digits with the distal-most superolateral scales in contact. Fig. 2. Above, digital X-ray of the holotype of Sphaerodactylus dommeli (ZFMK 66238) magnified showing the cephalic-cervical region. Below, a reconstruction of the dorsal view of S. dommeli. Abbreviations: 1cb, first ceratobranchial; co, coronoid; cob, compound bone; d, dentary; ect, ectopterygoid; en, external nares; ept, epipterygoid; f, frontal; j, jugal; mx, maxilla; mxfp, facial process of maxilla; n, nasal; occ, occipital condyle; ocr, occipital recess; oto, otooccipital; par, parietal; pmx, premaxilla; pof postorbitofrontal; ppp, postparietal process; prf, prefrontal; pt, pterygoid; q, quadrate; rap, retroarticular process; sa, surangular; sq, squamosal; so, supraoccipital; sr, sclerotic ring

notch forming a waist proximally, (7) retroarticular process posterior to waist broader than jaw immediately anterior to waist, (8) autotomy planes located at the transverse processes, (9) lack of a gular fold and (10) subdigital scansorial pad borne distally, beneath the ungual (terminal) and penultimate phalanges (versus beneath the antepenultimate and more proximal phalanges in Anolis; Estes et al. 1988; Frost and Etheridge 1989; de Queiroz et al. 1998; Conrad 2008; Smith 2009; Figs 1–3). In contrast, S. dommeli exhibits 11 of 31 characters recently identified for the Gekkota (J.D. Daza, A.M. Bauer, unpublished data): (1) jugal reduced to a small splint of bone barely extending beyond the posterior margin of the maxilla, (2) jugal and postorbitofrontal not in contact, (3) supratemporal not present, (4) squamosal and postorbitofrontal (or postorbital or postfrontal) not in contact, (5) palpebral bone not present, (6) sphenooccipital tubercle located anteriorly; therefore, the crista tuberalis is inclined posterodorsally, (7) occipital recess visible in ventral view, 8) quadrate suspended mainly from the otooccipital, (9) articular, prearticular, and angular fused, (10) shortened metatarsal V and (11) eyelids fused into a spectacle or brille. In addition to its possession of the asymmetric claw sheath that is diagnostic of Sphaerodactylus (Fig. 3), seven additional characters for this genus (Daza and Bauer 2012) affirm the generic allocation of S. dommeli: (1) anterorbital portion of the skull constitutes 30% or less of the total skull length, (2) postorbitofrontal with large lateral process, (3) postparietal process length less than half the length anterior to the parietal notch, (4) 12–13 premaxilllary teeth, (5) body with keeled scales, (6) 2–6 loreal

Osteology of S. dommeli The holotype of S. dommeli (ZFMK 66238) has a well-preserved skeleton (Figs 1–2). Observed through the amber, the specimen appears to have a tail as long as its trunk, but on the X-rays there are no vertebrae posterior to the 6th caudal vertebra; therefore, we assume that the tail of the holotype is regenerated. Regeneration occurred at the basal most and most frequently utilized autotomy plane among Sphaerodactylus (pers. obs.) and geckos in general (Russell and Bauer 1992). Two radio-opaque elements obscure the anterior basicranial and abdominal areas; the first one is a preservation artefact, while the position, shape and size of the second one strongly suggest that this element is an egg. Gravidity together with the terminal fusion of the epiphyses to the diaphyses of the long bones are strong indicators of the skeletal maturity of the holotype (Maisano 2000, 2002). Skull osteology The arrangement of skull bones in S. dommeli (Fig. 2) is similar to that described for S. roosevelti (Daza et al. 2008), but the snout is narrower, having a longer narial area. The premaxilla is unpaired and exclusively forms the tip of the snout and bears about 12 teeth. Dorsally, this bone bears an elongated ascending nasal process that separates the nasal bones anteriorly. The nasal bones are paired and overlap the anterior border of the frontal, leaving exposed two well-defined anterolateral processes of the frontal. The maxilla exhibits a taller facial process than in S. roosevelti, overlapping extensively the anterior portion of the prefrontal and developing a more extensive contact with the frontal; this bone bears about 29 tooth loci. The frontal bone is tubular (i.e. fused both ventrally and dorsally) and is slightly curved posteriorly. The jugal bone is small and contacts the posterodorsal surface of the maxilla and the ventral edge of the orbitonasal flange, probably, participating on the lacrimal foramen. The frontal and parietal are clasped by the postorbifrontal. The parietal bones are paired and rectangular and have a short posterolateral process (i.e. supratemporal process). This process contacts the otooccipital portion of the braincase and the squamosal; there is no trace of a temporal bone. At least the left quadrate is still J Zoolog Syst Evol Res (2013) 51(1), 55--63 © 2012 Blackwell Verlag GmbH

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articulated in joints with the otooccipital, articular part of the compound bone, and pterygoid. The left epipterygoid is visible connecting the pterygoid and the prootic crista alaris. With this type of preparation, it is not possible to provide more details about the basicranium or the palatal bones, but there are two conspicuous structures visible in the braincase: (1) the right occipital recess, which is rounded and probably visible in ventral view (i.e. not hidden by the sphenoccipital tubercle) and (2) the occipital condyle, which is bicondylar as in the majority of gekkotans (Cope 1900; Gardiner 1982; but see Lialis burtonis, Stephenson 1962; Daza 2008) and articulated with the atlas. On the X-ray, it is possible to distinguish four bones of the jaw, the dentary, coronoid, surangular and the compound bone (articular, pre-articular and angular; Daza et al. 2008). The dentary bears at last 26 teeth. The coronoid is low and hardly elevated above jaw outline as in all sphaerodactyls (Daza and Bauer 2012). The retroarticular portion of the compound bone is spoon shaped and waisted, as in many geckos (Evans 2008). The splenial bone is probably fused to the coronoid as in other sphaerodactyl geckos (Gamble et al. 2011b; Daza and Bauer 2012). Postcranial osteology One of the distinct features of S. dommeli is its elongated neck (Böhme 1984). In lizards, as in many limbed tetrapods, the pectoral girdle connects the upper limb with the axial skeleton by means of the musculotendinous scapulocostal joint (McGonnell 2001; Russell and Bauer 2008; Kardong 2012). This floating type of joint allows several gliding movements including the protraction and retraction of the scapulocoracoid. A lizard trapped in the viscous resin that forms amber might be expected to fully retract or even hyperextend the scapulocostal joint while trying to escape. The holotype was preserved with the neck fully extended and the forelimbs bent backwards and extended. Based on this position of the limbs, it is conceivable that the apparently elongate neck is, in part, the result of a posterior displacement (or even dislocation) of the pectoral girdle. Yet, the later observation is not confirmed with the morphometric data. Among the sampled sphaerodactylids, S. dommeli has the longest cervical region relative to the total presacral length (27.25%. Fig. 4, Table 1), followed by Gonatodes antillensis (27.23%) and Sphaerodactylus copei (26.02%). In absolute terms, S. dommeli has a cervical region as long as that of the much longer-bodied Gonatodes geckos (Table 1). Unfortunately, only the posterior portion of the skull is preserved in the holotype of another amber-preserved Sphaerodactylus, S. ciguapa, so a comparison is limited to mainly postcranial and external features (see also Daza and Bauer 2012). In S. ciguapa, the relative length of the cervical region to the entire presacral column (23.53%) was lower than in S. dommeli and similar to that of the extant S. armstrongi (23.56%). In the holotypes of both S. dommeli and S. ciguapa, the second cervical vertebra (axis) is slightly enlarged, having a centrum nearly four times the length of the atlas, contra three times in extant congeners. The ratio of skull to presacral length in S. dommeli is similar to that in S. micropithecus (Fig. 4, Table 1), but the latter has a shorter neck. Sphaerodactylus dommeli has a stout humerus with a right-angled entepicondylar side. It has the normal manual and pedal formulae for Sphaerodactylus, namely 2 : 3 : 4 : 5 : 3 and 2 : 3 : 4 : 5 : 4, respectively, with phalanges 2 and 3 of digit 4 of both manus and pes shortened. In terms of pectoral and pelvic elements, there is not much that can be described, but the clavicular fenestrae are not enlarged, a feature distinguishing it from S. ciguapa (Daza and Bauer 2012) and the pelvis exhibits the characteristically large and ventrally directed pectineal process of sphaerodactyls. J Zoolog Syst Evol Res (2013) 51(1), 55--63 © 2012 Blackwell Verlag GmbH

Fig. 4. Results from the morphometric analysis, indicating the proportionally longer cervical region of Sphaerodactylus dommeli with respect to all other sphaerodactyls. Above, scatter plot of cervical length against presacral length of 55 species of sphaerodactyls. Below, scatter plot of skull length contra presacral length of 54 species of sphaerodactyls

Discussion Identity of the the holotype of S. dommeli The skeletal structure of the holotype S. dommeli reaffirms its gekkotan identity, being very distinct from that of Hispaniolan anoles in amber, which generally have relatively wider skulls and longer and more slender limb bones, resembling trunk-crown ecomorphs of the Anolis chlorocyanus species group (Rieppel 1980; de Queiroz et al. 1998; Polcyn et al. 2002). Extant species of Caribbean Anolis are highly variable in limb and body proportions (Williams 1983; Losos et al. 1998), but even considering this variation, their habitus differs considerably from that of Sphaerodactylus. Indeed, the only sphaerodactylids that present a certain degree of osteological similaritiy with anoles are some species of the Old World genus Pristurus, which have slender elongate limbs and tail (e.g. Pristurus carteri, Daza and Bauer 2012). The presence of an egg in the abdomen is a strong indicator of skeletal maturity of the holotype. Miniaturised Sphaerodacty-

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Table 1. Skull, cervical and presacral length of representative sphaerodactyl geckos Species +

Sphaerodactylus dommeli Sphaerodactylus ciguapa+ Sphaerodactylus altavelensis Sphaerodactylus argus Sphaerodactylus ariasae Sphaerodactylus armstrongi Sphaerodactylus asterulus Sphaerodactylus beattyi Sphaerodactylus cinereus Sphaerodactylus copei Sphaerodactylus corticola Sphaerodactylus darlingtoni Sphaerodactylus difficilis Sphaerodactylus elegans Sphaerodactylus ladae Sphaerodactylus leucaster Sphaerodactylus levinsi Sphaerodactylus lineolatus Sphaerodactylus macrolepis Sphaerodactylus microlepis Sphaerodactylus micropithecus Sphaerodactylus notatus Sphaerodactylus oliveri Sphaerodactylus oxyrhinus Sphaerodactylus pacificus Sphaerodactylus parkeri Sphaerodactylus parthenopion Sphaerodactylus ramsdeni Sphaerodactylus rhabdotus Sphaerodactylus richardsoni Sphaerodactylus roosevelti Sphaerodactylus rosaurae Sphaerodactylus sabanus Sphaerodactylus samanensis Sphaerodactylus savagei Sphaerodactylus semasiops Sphaerodactylus sommeri Sphaerodactylus sputator Sphaerodactylus streptophorus Sphaerodactylus thompsoni Sphaerodactylus torrei Sphaerodactylus townsendi Sphaerodactylus vincenti Chatogekko amazonicus Coleodactylus guimaraesi Coleodactylus septentrionalis Gonatodes albogularis Gonatodes annularis Gonatodes antillensis Gonatodes humeralis Lepidoblepharis buchwaldi Lepidoblepharis festae Lepidoblepharis heyerorum Pseudogonatodes guianensis Pseudogonatodes peruvianus

Specimen No.

Skull length

Cervical length (C)

Presacral length (PS)

% C/PS

ZFMK 66238 MCZR 186380 USNM 328548 USNM 251977 USNM 541808 USNM 260046 USNM 328949 USNM 304481 USNM 292296 USNM 118881 USNM 211428 USNM 328962 USNM 328965 USNM 27625 USNM 512253 USNM 197338 USNM 220921 USNM 120497 USNM 221462 USNM 222901 USNM 229891 USNM 494822 USNM 140431 USNM 292289 USNM 157532 USNM 328281 USNM 221593 USNM 309772 USNM 292328 USNM 252126 USNM 327042 USNM 570205 USNM 236098 USNM 319135 USNM 260157 USNM 305435 USNM 292313 USNM 236118 USNM 541813 USNM 328977 USNM 512267 USNM 291193 USNM 286941 USNM 288763 USNM 304122 USNM 302285 USNM 297802 USNM 535791 USNM 94980 USNM 568645 USNM 234568 USNM 166141 USNM 217635 USNM 166138 USNM 343190

9.234 7.029 6.450 3.551 5.577 6.766 6.950 7.760 8.944 7.946 6.006 7.846 9.849 7.135 7.300 6.837 8.089 5.963 8.117 9.188 6.548 7.728 9.125 9.441 10.200 6.277 7.898 7.918 9.842 9.055 9.531 7.366 7.557 6.914 7.463 8.919 7.225 5.253 8.318 9.805 5.534 8.661 4.937 4.971 6.888 9.508 11.032 8.228 9.724 6.014 7.774 6.581 5.794 5.876

6.429 5.968 4.490 3.276 2.082 3.376 3.794 4.174 4.567 5.369 4.552 3.423 4.423 5.789 4.198 4.147 4.161 4.832 3.525 5.075 5.160 3.431 4.800 5.065 5.860 5.063 3.944 5.027 4.624 6.157 5.534 5.864 4.080 4.411 4.274 3.594 5.582 5.054 3.174 4.923 5.951 3.233 4.766 2.549 3.393 4.505 6.858 6.752 4.674 5.829 4.024 4.647 5.241 3.804 4.172

23.585 25.353 18.752 16.368 9.149 14.329 16.914 17.256 19.899 20.630 18.560 14.640 19.734 23.251 19.464 17.011 19.795 20.040 15.217 21.787 22.474 15.975 19.197 22.364 24.638 21.152 17.157 21.939 18.604 25.964 23.740 22.977 17.789 17.844 19.239 15.200 22.148 20.149 14.437 20.507 24.723 13.551 20.933 12.916 13.809 19.233 26.994 27.631 17.163 24.168 17.328 18.991 21.933 15.533 16.998

27.259 23.539 23.942 20.017 22.755 23.561 22.431 24.190 22.953 26.024 24.527 23.385 22.414 24.899 21.568 24.378 21.023 24.110 23.162 23.296 22.961 21.478 25.005 22.649 23.786 23.937 22.990 22.914 24.855 23.714 23.311 25.523 22.937 24.719 22.217 23.641 25.203 25.085 21.988 24.008 24.070 23.859 22.767 19.735 24.568 23.423 25.406 24.438 27.233 24.118 23.221 24.471 23.895 24.487 24.546

+

Fossil species are indicated by a cross

Fig. 5. Digital X-ray of a gravid female of Sphaerodactylus ladae (USNM 512251)

lus develop a single elongated, oval egg (Krysko et al. 2003; Kratochvíl and Frynta 2005; Regalado 2006), which is large compared with its body size, being as long as the skull lengthways (Figs 1 and 5). Sphaerodactylus geckos develop single-egg clutches (Barbour 1921; Carr 1940; Taylor 1956; Duellman and Schwartz 1958; Fitch 1970; Krysko et al. 2003), a character that is widespread among the family Sphaerodactylidae (Gamble et al. 2008a; Daza and Bauer 2012), but that is also present in anoles (Losos 2009). The external and internal anatomy of the holotype of S. dommeli confirms that this taxon is a member of the Family Sphaerodactylidae, providing a reliable calibration point for biogeoJ Zoolog Syst Evol Res (2013) 51(1), 55--63 © 2012 Blackwell Verlag GmbH

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(b)

(c)

Fig. 6. (a) Dorsal view of the paratype of Sphaerodactylus dommeli (modified from picture by K. Wolf-Schwenninger, SMNS). (b) Silhouette of a live specimen of Sphaerodactylus klauberi. (c) Silhouette of a live specimen of Anolis cristatellus

graphical and molecular dating inferences, this is very important considering that using erroneously identified and dated fossils may result in incorrect divergence dates (Hutchinson et al. 2012). Identity of the paratype of S. dommeli We cannot provide any details of the skeletal anatomy of the paratype of S. dommeli, but the habitus of this specimen (Fig. 6a; Böhme 1984; Schlee 1990) is more similar to Sphaerodactylus than to Anolis. This opinion is shared by Dr. Richard Thomas, an expert in both groups, and who has described about 20 species of the former genus. Although we cannot meaningfully postulate its position within Sphaerodactylus, we favour its position within the Gekkota based on seven morphological characters: (1) presence of granular scales on the parietal area, (2) no signs of a parietal eye, (3) the apparent presence of a spectacle on the left eye (Fig. 6a), (4) short and stout limbs as in Sphaerodactylus (Fig. 6b), (5) short digits as in Sphaerodactylus (Fig. 6b), (6) lack of expanded pads on the antepenultimate phalanges (see left hand and foot Fig. 6a) and (7) the longest pedal digit being the third instead of the fourth, as in Anolis (Fig. 6c). The holotype and the paratype differ considerably in size, but based on the shared-elongated neck, these two specimens were placed in the same species, and the paratype considered a juvenile (Böhme 1984). Although relative head size might give an indication of whether an individual is a juvenile, X-rays allowing the visualisation of terminal fusions of long bones in the paratype need to be obtained for better comparisons between the two specimens assigned to S. dommeli and other Sphaerodactylus in amber. With current information, we cannot discount the possibility that the paratype is an adult (16.5-mm SVL), representing an extremely miniaturised species; such small sizes are seen, for example, in the extant S. ariasae (~16-mm SVL) from Isla Beata in the Dominican Republic (Hedges and Thomas 2001). Morphological distinctness of sphaerodactyl amber geckos The two described sphaerodactyls in amber each exhibit autapomorphic skeletal morphology; S. dommeli has an elongate cervical vertebral segment (Fig. 4, Table 1) and S. ciguapa has J Zoolog Syst Evol Res (2013) 51(1), 55--63 © 2012 Blackwell Verlag GmbH

unusual enlarged clavicular fenestrae (Daza and Bauer 2012). The long neck of S. dommeli is an apomorphic feature and is not due to posterior displacement or dislocation of the pectoral girdle, although the retracted position of the specimen’s fore limbs exaggerates this feature. This morphology is not found in any of the extant sphaerodactyls sampled. These two osteological characters confirm their distinctiveness and validate their recognition as formally described taxa.

Conclusions Sphaerodactylus geckos exhibit great variation in their body proportions; a more comprehensive quantification of this variation is being evaluated (D. Scantlebury, pers. comm.), and has the potential to reveal morphological groups (ecomorphs) associated with particular environmental correlates, in an analogous way to the more widely studied Anolis lizards from the same geographical region (Williams 1983; Losos et al. 1998; Losos 2009). Sphaerodactylus and Anolis, along with Typhlops, and Eleutherodactylus, are the four reptile and amphibian genera recorded from Dominican inclusions (Grimaldi 1996; Poinar and Poinar 1999). Today, these groups comprise 156 of 243 species of amphibians and reptiles found on Hispaniola (Hedges 2012). Although these genera are represented by only a few described amber inclusions each (Rieppel 1980; Böhme 1984; Poinar and Cannatella 1987; Kluge 1995; de Queiroz et al. 1998; Polcyn et al. 2002; Daza and Bauer 2012), a relatively large number of specimens of both Sphaerodactylus and Anolis remain to be described from Dominican amber (Poinar and Poinar 1999; D.A. Grimaldi, pers. comm. 2009), raising the possibility that it may be possible to at least partially reconstruct the Hispaniolan herpetofauna of the Miocene and to evaluate ecomorphological data, to infer something about palaeocommunity structure. The data presented herein should help to facilitate the unambiguous allocation of as yet unstudied Dominican amber lizard fossils to the correct genus. The unambiguous confirmation of S. dommeli as a member of the genus Sphaerodactylus further validates its past and continued use as a calibration point for time tree analyses of gekkotan lizards. Sphaerodactylus is estimated to have diverged from its nearest relatives in the Late Cretaceous (Gamble et al. 2011b);

A reconsideration of Sphaerodactylus dommeli thus, the age of Dominican amber fossils is relatively recent within the history of the group. At present, S. dommeli and S. ciguapa provide a minimum age for Sphaerodactylus within the gekkotan tree. Yet, further resolution of their phylogenetic positions within this genus, which may be possible in the context of a taxon-complete phylogeny combining both molecular (S.B. Hedges in prep., pers comm.) and morphological data will render them, and other amber dwarf geckos, even more useful in this context as the confidence envelope around their temporal placement will be greatly constrained.

Acknowledgements We thank Wolfgang Weitschat for polishing the holotype of S. dommeli at the Paleontology Institute in Hamburg and his help with photographs. Kyle Luckenbill and Ned Gilmore (Academy of Natural Sciences in Philadelphia) and Sandra Raredon and Kenneth Tighe (National Museum of Natural History, Smithsonian Institution) for their kind help with the Xrays. For access to comparative material, we thank Colin McCarthy (BMNH), Richard Thomas (RT, UPRRP), Kevin de Queiroz, Roy McDiarmid, Ron Heyer, George Zug, Jeremy Jacobs, Steve Gotte (USNM), Jonathan Losos and José Rosado (MCZ). This research was supported by the Gerald M. Lemole, M.D. Endowed Chair in Integrative Biology Fund and by grant DEB 0844523 from the National Science Foundation of the United States.

Zusammenfassung Erneute Bewertung der miozänen Bernsteinechse Sphaerodactylus dommeli Böhme, 1984 (Squamata: Gekkota: Sphaerodactylidae) Der miozäne Bernsteingecko Sphaerodactylus dommeli Böhme, 1984 ist einer der am besten erhaltenen fossilen Vertreter der Gekkota, wenngleich seine taxonomische Identität in Frage gestellt und dabei unterstellt wurde, dass es sich eher um einen Vertreter der hoch-diversen Gattung Anolis (Iguania) handeln könnte. Die vorliegende Arbeit liefert durch digitale Röntgen-Aufnahmen neue osteologische Belege, von denen 11 Merkmale die Stellung dieser Art innerhalb der Gekkota bestätigen, und acht Merkmale die Zugehörigkeit zur artenreichen Gattung Sphaerodactylus, zu der sie ja ursprünglich auch gestellt worden war. Unser Beitrag möchte mögliche weiter bestehende Zweifel an der Gattungszugehörigkeit dieser Art ausräumen und einen verlässlichen Kalibrationspunkt für weitergehende Forschung zur Phylogenie der Squamaten liefern, speziell für biogeographische Studien and molekulare Datierungen. Dieser Beitrag erörtert auch viele diagnostische Kennzeichen für die beiden in Frage stehenden Gattungen, was für die korrekte Zuordnung von bernstein-konservierten Exemplaren entscheidend ist, die die reiche hispaniolische Echsen-Paläozönose gebildet haben.

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