Abstract
Vestigial biological structures provide an important line of evidence for macroevolution. They abound in the appendicular skeletons of limbless and reduced-limbed members of the skink subfamily Scincinae, which includes a predominantly Asian clade and a predominantly African clade. Reduced appendicular skeletons in the predominantly African clade have received much recent attention, but for most species in the predominantly Asian clade the appendicular skeleton has yet to be described. Here we provide descriptions of the appendicular skeletons of the reduced-limbed skinks Brachymeles bonitae and Ophiomorus blandfordi, the externally limbless skink Ophiomorus punctatissimus, and, for comparison, the pentadactyl skinks Brachymeles gracilis and B. talinis. We used x-ray radiographs to examine the skeletons of these species and to note similarities and differences in the previously-described appendicular skeletal morphology of related species. We found that in B. bonitae the pectoral and pelvic girdles are unreduced, the proximal limb elements are reduced, and the distal limb elements are vestigial. In O. punctatissimus vestigial pectoral and pelvic girdles are present. In O. blanfordi the fifth metatarsal is vestigial. The phylogenetic distribution of morphological features related to appendicular reduction shows that multiple, parallel reduction events have taken place within each of these two genera. In addition, the anatomical distribution of element reduction and loss in these genera shows that the bones are reduced and lost in the same sequence in the predominantly Asian scincine clade as they are in other squamate clades. This suggests a common evolutionary mechanism for appendicular reduction and loss across the Squamata.
Introduction
The existence of vestigial biological structures is an important line of evidence for macroevolution (Lamarck, 1809; Darwin, 1859; Reece et al., 2011; Senter et al., 2015). A plethora of species within the subfamily Scincinae of the lizard family Scincidae (the skinks) exhibit various degrees of limb reduction (fig. 1), including the presence of vestigial limbs and/or girdles. The subfamily includes species with pentadactyl limbs, species with reduced digital formulae, species with vestigial external limbs, and externally limbless species with vestigial pectoral and pelvic girdles. Appendicular skeletal morphology has been described for at least 18 limbless and vestigial-limbed scincine species from ten genera (Fürbringer, 1870; Cope, 1892; Rabanus, 1911; Essex, 1927; Sewertzoff, 1931; Renous and Gasc, 1979; Moch and Senter, 2011; Miralles et al., 2012; Liniewski et al., 2015; Miralles et al., 2015). However, for many limbless and vestigial-limbed scincine species the appendicular skeleton has not yet been described.
Cladogram showing the relationships among genera of the skink clade Scincinae (Pyron et al., 2013; Miralles et al., 2015), including all species of Brachymeles and Ophiomorus, with states of limb reduction indicated. Bold font indicates species for which appendicular skeletons are described here, and an asterisk indicates species for which the appendicular skeleton has already been described. Black squares indicate externally limbless taxa; gray squares indicate taxa in which some but not all members are externally limbless. Black circles indicate digit loss; gray circles indicate taxa in which some but not all individuals exhibit digit loss; more than one symbol on a branch indicates a taxon in which multiple phenotypes are present; a five-pointed star on a branch with other symbols indicates a taxon in which some members are pentadactyl. All lineages unmarked by squares and circles are pentadactyl. Anatomical data for Ophiomorus and Brachymeles are from Greer and Wilson (2001) and Siler et al. (2011). Numbers in rectangles indicate digit formulae (e.g. “3/4” for species with three fingers and four toes). Phylogenetic relationships between genera are illustrated as per Pyron et al. (2013), with genus names of Madagascan skinks updated as per Miralles et al. (2015). Phylogenetic relationships between the species of Ophiomorus are as per Greer and Wilson (2001), and phylogenetic relationships between the species of Brachymeles are as per Siler et al. (2011).
Citation: Amphibia-Reptilia 37, 4 (2016) ; 10.1163/15685381-00003062
The subfamily Scincidae is split into a predominantly Asian clade and a predominantly African clade (Pyron et al., 2013) (fig. 1). Vestigial appendicular structures of the predominantly African clade have received much recent attention in the literature, with numerous new skeletal descriptions and elucidations of evolutionary patterns of appendicular reduction (Whiting et al., 2003; Schmitz et al., 2005; Moch and Senter, 2011; Miralles et al., 2012; Liniewski et al., 2015; Miralles et al., 2015). Within the predominantly-African scincine clade, the phylogenetic distribution of digit and limb loss shows that limb loss has occurred independently in at least seven lineages, and limb reduction that includes digit loss or greater reduction has occurred independently in at least eleven lineages (fig. 1).
Similar attention has not yet been given to members of the predominantly Asian scincine clade, the vestigial appendicular skeletons of which remain undescribed for most species. The predominantly Asian scincine clade has only four genera: Brachymeles, Ophiomorus, Mesoscincus, and Plestiodon (Pyron et al., 2013). Of these, the former two genera contain species with appendicular reduction, whereas the latter two consist of pentadactyl species. Elucidation of patterns of evolutionary reduction in this clade therefore depends on description of the appendicular anatomy of Brachymeles and Ophiomorus. This study is an attempt to contribute towards elucidating evolutionary patterns of appendicular reduction in the predominantly Asian scincine clade, by describing the appendicular skeletons of five species within the clade: Brachymeles bonitae (which has vestigial limbs), B. gracilis (pentadactyl), B. talinis (pentadactyl), Ophiomorus punctatissimus (externally limbless), and O. blanfordi (which has reduced limbs with four fingers per hand and three toes per foot).
The genus Brachymeles is found in the Philippines and Thailand, and initially comprised more than twenty species (Siler and Brown, 2011), but a recent phylogenetic study (Siler et al., 2011) showed that some were paraphyletic with respect to congeners, leaving only thirteen valid species (fig. 1). Of these, six species are pentadactyl, two are externally limbless, and the remaining five exhibit varying degrees of limb reduction (fig. 1), including cases in which the limbs are too reduced to provide propulsion and can therefore be considered vestigial (Siler and Brown, 2011). Fully-limbed, vestigial-limbed, and limbless members of Brachymeles are semi-fossorial, are often found within soft substrates, and use lateral undulation to burrow into loam to escape capture (Brown et al., 2000; Siler et al., 2009). For such burrowing behavior limbs are assumed to be an impediment, because they disrupt streamlining (Hildebrand and Goslow, 2001). The burrowing behavior of Brachymeles is therefore likely the source of the selection pressure that drove the reduction and ultimate loss of limbs in some species of the genus. Currently, recorded knowledge of the appendicular skeleton of Brachymeles is limited to the manual and pedal phalangeal formulae of its pentadactyl species, which are 2-3-3-3-2 and 2-3-4-4-3, respectively (Siler and Brown, 2011).
Radiographs of Brachymeles gracilis (USNM 496798) (top) and B. talinis (USNM 228392) (bottom). The two boxes in the full-body radiographs indicate the position of the enlarged areas. The corners of the sternum are marked by small, white circles. c = carpal element, cl = clavicle, co = coracoid, h = humerus, i = interclavicle, il = ilium, is = ischium, m = metacarpal, mt = metatarsals, p = phalanges, pu = pubis, pub = puboischium, r = radius, s = scapula, st = sternum, sv = sacral vertebrae, t = tarsus, u = ulna.
Citation: Amphibia-Reptilia 37, 4 (2016) ; 10.1163/15685381-00003062
Ophiomorus has eleven known species (Kazemi et al., 2011), which range from Greece to western India (Anderson and Levinton, 1966). The two species at its most western limit, O. punctatissimus and O. latastii, lack external limbs and are found under rocks (Anderson and Levinton, 1966). The eastern species have reduced limbs with the number of fingers and toes varying from three to four and two to three, respectively (fig. 1). They burrow by lateral undulation through loose sand, keeping their forelimbs tucked into grooves on their sides (Anderson and Levinton, 1966; Kazemi et al., 2011). The appendicular skeleton has thus far been described only for O tridactylus (Sewertzoff, 1931).
Materials and methods
Radiographs were made of specimens using a digital micro x-ray machine at the Museum Support Center (MSC) of the U.S. National Museum of Natural History (USNM) in Washington, D.C. Sample size was two in B. gracilis (USNM 496790 and 496798), and four in both B. talinis (USNM 228392, 228393, 229566, and 229567) and B. bonitae (USNM 496945, 519333, 519334, and 519345). Specimen USNM 496945 is catalogued as B. tridactylus, but this “species” is phylogenetically bracketed by specimens identified as B. bonitae and cf. B. bonitae (Siler et al., 2011) and can therefore be considered a junior synonym of B. bonitae. Sample size was one in both O. blanfordi (USNM 148660) and O. punctatissimus (USNM 31956).
To determine ancestral states, we used the cladogram shown in fig. 1. This cladogram shows the relationships between the genera within the subfamily Scincidae, as per Pyron et al. (2013), with genus names of Madagascan skinks updated as per Miralles et al. (2015). The cladogram also shows the relationships of species within the genus Ophiomorus as per Greer and Wilson (2001), and relationships between the species of Brachymeles as per Siler et al. (2011). We mapped states of limb and digit reduction onto the cladogram (fig. 1). We then estimated the number of state changes across the predominantly-Asian scincine clade by applying the principle of parsimony, choosing the scenario that involves the smallest number of state changes.
Left and center columns: radiographs of Brachymeles bonitae: USNM 519333 (top), 519334 (middle), and 19345 (bottom). Right column: radiographs of Brachymeles bonitae (USNM 496945). The two boxes in the full-body radiographs indicate the position of the enlarged areas below. The corners of the sternum are marked by small, white circles. Abbreviations as in fig. 2.
Citation: Amphibia-Reptilia 37, 4 (2016) ; 10.1163/15685381-00003062
Results
In all examined specimens of B. gracilis and B. talinis (fig. 2) the morphology of the appendicular skeleton is essentially similar. The scapula is well-ossified and is anteroposteriorly-narrow with a slight widening at the coracoidal end. The coracoid is cartilaginous or poorly-ossified. It is strongly flared at the sternal end so that there is a pair of widely-separated, anterior and posterior processes that end in an acute angle. It exhibits an ovoid foramen near where its anterior margin meets the scapula. The clavicle is well-ossified only at its scapular end, which is flared. The interclavicle is poorly-ossified and cruciform. The sternum is cartilaginous and pentagonal. The radius is between 35% and 40% the length of the humerus. The bones of the carpus and hand are more poorly ossified than the more proximal forelimb bones, and carpal morphology is difficult to discern. The manual phalangeal formula is 2-3-3-3-2. The bones of the pelvic girdle are well-ossified. The pubes are rodlike, and their bony anterior tips nearly contact each other in the midline. The bony ischia meet in the midline and their medial ends are strongly flared. Their shafts are broader than those of the pubes. The crus is approximately 50% the length of the femur. The bones of the tarsus and foot are more poorly ossified than the more proximal limb bones, but it is possible to discern an intermedium, a fibulare, a centrale, and distal tarsals 2-5. The pedal phalangeal formula is 2-3-4-4-3.
In B. bonitae (fig. 3) the anteroposteriorly-narrow scapula is the only well-ossified bone of the pectoral girdle. The coracoid is better-ossified at the glenoid than elsewhere but is mainly cartilaginous, and its shape is difficult to discern. No interclavicle is visible. A pentagonal, cartilaginous sternum is present in USNM 496945 and 519334; vertebrae obscure the view of the relevant area in the other two specimens. A humerus is present, as well as a radius and ulna, each of which is less than half the length of the humerus. The skeleton of the carpus and hand appear to be absent in USNM 519334, present as a largely-cartilaginous mass with little definition in USNM 496945 and 519333, and present as a tiny, poorly-ossified pair of elements in USNM 519345. The more proximal of these two elements occupies the location of an intermedium, and the more distal element is somewhat elongate and might be a metacarpal. The pelvic girdle includes well-ossified pubes, ischia, and ilia. The pubes and ischia meet in the midline, and the bony ilia closely approach but do not contact the second sacral vertebra. The shafts of the ischia are not as anteroposteriorly broad as in B. gracilis and B. talinis, and flaring of the medial ends is weak. The femur and tibia are well-ossified, but the fibula and distal elements are largely cartilaginous. In each specimen at least one tarsal element is present, followed distally by possibly at least one metatarsal.
Radiographs of Ophiomorus blanfordi (USNM 148660) (left column) and O. punctatissimus (USNM 31956) (right column). The two boxes in the full-body radiographs indicate the position of the enlarged areas below. The corners of the sternum are marked by small, white circles. Abbreviations as in fig. 2.
Citation: Amphibia-Reptilia 37, 4 (2016) ; 10.1163/15685381-00003062
In the specimen of O. blanfordi (fig. 4) the pectoral girdle includes a well-ossified clavicle and scapula, but no interclavicle is visible in the radiograph, and the coracoid and sternum are cartilaginous. The forelimb skeleton is complete and well-ossified from shoulder to wrist, and in the radiograph two metacarpals are visible in each hand, one of which bears at least two phalanges, and the other at least three. Poor positioning of the specimen’s hands made it impossible to evaluate their structure. The pelvic girdle includes well-ossified pubes, ischia, and ilia. The pubes and ischia meet in the midline, and the ilia closely approach the second sacral vertebra. There is a well-ossified femur, tibia, fibula, tibiale, centrale, first distal tarsal, fifth distal tarsal, and metatarsals II-V. The fifth metatarsal is present only as an ovoid vestige at the proximal end of the metatarsus. The phalanges are well-ossified, and the phalangeal formula is x-2-3-4-0.
In the specimen of O. punctatissimus there are no traces of limbs. The pectoral girdle includes a mostly-cartilaginous scapula that is slightly ossified along its posterior margin. A pair of clavicles is present, along with an elongate ventral element that is most likely the interclavicle. Ilia are present, along with puboischia that are not differentiated into pubes and ischia.
The pentadactyl state is the ancestral state for the Scincidae. This is indicated by the fact that at the base of each of the three main clades (Mesoscincus + Ophiomorus, Plestiodon + Brachymeles, and the predominantly-African clade) is a pentadactyl taxon (Mesoscincus, Plestiodon, and Eurylepis + Eumeces + Scincopus + “Eumeces” + Scincus), which means that every limb-reduced taxon is phylogenetically bracketed by pentadactyl taxa. The distribution of limb loss in the predominantly-Asian scincine clade shows that, according to the principle of parsimony, limb loss has occurred independently in at least five lineages (Ophiomorus punctatissimus, O. latastii, Brachymeles apus, B. miriamae, and some B. samarensis), because this is the limb-loss scenario that involves the smallest number of state changes. The distribution of states of limb reduction also shows that within the predominantly-Asian clade, according to the principle of parsimony, digit loss or greater limb reduction has occurred independently in at least ten lineages (O. persicus, O. punctatissimus, O. latastii, O. streeti + O. raithmai + O. tridactlus, B. apus, B. miriamae, B. gracilis, B. elerae + B. muntingkamae, and B. bonitae + B. samarensis, with further reduction in some B. samarensis), because this is the limb-reduction scenario that involves the smallest number of state changes.
Discussion
A simple progression from small to large magnitudes of limb reduction, in which successive sister taxa exhibit successively greater degrees of reduction, is not present across the phylogeny of Ophiomorus or Brachymeles. Instead, within each genus, various degrees of limb reduction have occurred several times in parallel. This underscores the high degree of selection pressure for limb reduction in these two genera. As mentioned in the Introduction, this selection pressure is likely related to fossorial behavior in both genera.
In limbless squamates, ossification of the sternum is usually reduced and lost before that of the bones of the pectoral girdle. Within the pectoral girdle, reduction and loss of ossification tends to occur in the coracoids and interclavicle before it occurs in the scapulae and clavicles (Essex, 1927; Stephenson, 1961). Multiple parallel examples of this sequence of element loss occur within Squamata, e.g. in the Pygopodidae (Stephenson, 1961), in the Anguidae (Sewertzoff, 1931; Stokely, 1947), in the Amphisbaenia (Gans, 1960), in the skink subfamily Acontiinae (Essex, 1927), and in the predominantly-African scincine clade (Sewertzoff, 1931; Miralles et al., 2012, 2015). As shown here, the same pattern is present in the predominantly-Asian scincine clade. In Ophiomorus punctatissimus the sternum and coracoids are lost, while ossified remnants of the more anterior elements of the pectoral girdle remain. In Brachymeles spp. the sternum and coracoids are largely cartilaginous, while the scapula and clavicles retain the highest degree of ossification among the bones of the pectoral girdle. By confirming that this sequence of element loss is present in squamate taxa for which the appendicular skeleton was previously unexamined, these specimens show that this evolutionary pattern is present through a broader phylogenetic spectrum of the Squamata than was previously known. The predominance of the same sequence of reduction/loss in the pectoral girdle across the Squamata suggests a common mechanism for reduction. If this mechanism is related to developmental constraints, it could provide a productive future direction of investigation into squamate developmental patterns.
Interestingly, reduction of ossification in the sternum and coracoids is found not only in reduced-limbed species but also in pentadactyl species of Brachymeles. This feature may reduce the ability to transfer locomotor forces between the forelimbs because of the assumed weaker cartilaginous link between them. This situation would, however, not be expected to compromise lateral undulation in burrowers that do not use their forelimbs in vigorous locomotion. It is therefore not surprising that this trait endures in Brachymeles spp.
Within Brachymeles, girdle morphology is similar between the two reduced-limbed species and the two fully-limbed species examined here. The limbs, however, are quite different. In both reduced-limbed species the stylopodium is reduced and the elements beyond it to an even greater extent. Intraspecific variation exists in the hand skeleton and possibly the foot skeleton in B. bonitae. Intraspecific variation is also common in vestigial structures of non-squamate animals (Darwin, 1859; Omura, 1980; Conrad, 1982; Postacchini and Massobrio, 1983; Tague, 1997; Senter and Moch, 2015). Such variation be due to relaxed selection pressure on vestigial structures to maintain a specific morphology.
The phalangeal formula in lizards is usually 2-3-4-5-4 in the hand and 2-3-4-5-3 in the foot. The reduced phalangeal formula of 2-3-3-3-2 in the hand and 2-3-4-4-3 in the foot of B. gracilis and B. talinis is, however, the norm in pentadactyl members of Brachymeles (Siler and Brown, 2011). Siler and Brown (2011) suggested that this altered phalangeal formula could be due to an alteration of the developmental pattern after reacquisition of lost limbs. However, other studies (e.g. Goldberg and Igić, 2008) suggest that it is more likely that pentadactyl members of Brachymeles retain the limb and digit condition of their ancestors, and that parallel losses of these structures occurred in multiple members of the genus (e.g. Goldberg and Igić, 2008).
The hindlimb skeleton of O. blanfordi bears great resemblance to the previously-described (Sewertzoff, 1931) hindlimb skeleton of O. tridactylus. The phalangeal formula is the same in both cases, and phalangeal proportions are similar. In both cases an ovoid proximal vestige of metatarsal V is present, and metatarsal I is absent altogether. However, the tarsus in the specimen of O. tridactylus described by Sewertzoff (1931) comprises the fourth distal tarsal, while its proximal tarsals are fused into a single element. In the specimen of O. punctatissimus the proximal tarsals are distinct and there are two distal tarsals. A larger sample size in each species will be necessary to determine whether the differing tarsal traits found are characteristic of their respective species or indicative of intraspecific variation.
The vestigial pelvic girdle of O. punctatissimus resembles that of many other limbless squamates, in that the largest element is the ilium, the puboischia do not meet in the midline, and the puboischia are not differentiated into distinct pubes and ischia. In some squamates that retain a vestigial proximal hindlimb the puboischium remains forked so that the tips of the pubis and ischium can be distinguished (Essex, 1927; Stephenson, 1961; Kearney, 2002; Moch and Senter, 2011).
This study elucidates evolutionary patterns in limb reduction in the predominantly-Asian scincine clade, showing that multiple parallel limb reduction events have occurred within the genera Brachymeles and in two species of Ophiomorus. It further shows that the pattern of element loss in these two genera resembles that of other squamate taxa. In addition, it provides a first look at the appendicular skeleton in Brachymeles and in two species of Ophiomorus. It therefore fills gaps in anatomical knowledge of these skink taxa. Many other gaps remain, because in most species of both genera the appendicular skeletons remain undescribed. We therefore recommend documentation of the state of the appendicular skeleton in other members of the clade, so as to further elucidate evolutionary patterns of limb reduction and loss within the predominantly-Asian scincine clade.
Acknowledgements
Jeremy Jacobs and Kenneth Tighe of the U.S. National Museum of Natural History provided access to the skink specimens and x-ray equipment. Parts of this project were included in theses for the Master of Science in Biology degree at Fayetteville State University; for these parts, Eid Haddad and Abdirahman Abokor of Fayetteville State University provided useful input. Two anonymous reviewers also provided helpful input that improved the manuscript.
References
Anderson S.C., Levinton A.E. (1966): A review of the genus Ophiomorus (Sauria: Scincidae) with descriptions of three new forms. Proc. Calif. Acad. Sci. Ser. 4 33: 499-534.
Brown R.M., McGuire J.A., Ferner J.W., Icarangal N. Jr., Kennedy R.S. (2000): Amphibians and reptiles of Luzon Island, II: preliminary report on the herpetofauna of Aurora Memorial National Park, Philippines. Hamadryad 25: 175-195.
Conrad E.C. (1982): True vestigial structures in whales and dolphins. Cr./Ev. 3 (4): 8-13.
Cope E.D. (1892): The osteology of the lizards. Proc. Am. Philos. Soc. 30: 185-221.
Darwin C. (1859): The Origin of Species by Means of Natural Selection or the Preservation of Favored Races in the Struggle for Life. John Murray, London.
Essex R. (1927): Studies in reptilian degeneration. Proc. Zool. Soc. Lond. 4: 879-945.
Fürbringer M. (1870): Die Knochen und Muskeln der Extremitäten bei den Schlangenähnlichen Sauriern. Wilhelm Engelmann, Leipzig.
Gans C. (1960): Studies on amphisbaenids (Amphisbaenia, Reptilia). 1. A taxonomic revision of the Trogonophinae, and a funcational interpretation of the amphisbaenid adapted pattern. Bull. Am. Mus. Nat. Hist. 119: 135-204.
Goldberg E.E., Igić B. (2008): On phylogenetic tests of irreversible evolution. Evolution 62: 2727-2741.
Hildebrand M., Goslow G.E. Jr. (2001): Analysis of Vertebrate Structure. John Wiley and Sons, New York.
Kazemi S.M., Qomi M.F., Kami H.G., Anderson S.C. (2011): A new species of Ophiomorus (Squamata: Scincidae) from Maranjab Desert Isfahan province, Iran, with a revised key to the genus. Amph. Rept. Conserv. 5 (1): 23-33.
Kearney M. (2002): Appendicular skeleton in amphisbaenians (Reptilia: Squamata). Copeia 2002: 719-738.
Lamarck J.-B.P.A. (1809): Philosophie Zoologique. Duminil-Lesueur, Paris.
Liniewski R., Stanely S., Andrade J., Senter P. (2015): Vestigial appendicular skeletons in the African and Malagasy skink species Feylinia grandisquamis, Melanoseps ater, Grandidierina lineata, and Voeltzkowia mira. Af. J. Herpetol. 65: 39-46.
Miralles A., Mirana A., Hipsley C.A., Müller J., Glaw F., Vences M. (2012): Variations on a bauplan: description of a new Malagasy “mermaid skink” with flipper-like forelimbs only (Scincidae, Sirenoscincus Sakata & Hikida, 2003). Zoosystema 34: 701-719.
Miralles A., Hipsley C.A., Erens J., Gehara M., Rakotoarison A., Glaw F., Müller J., Vences M. (2015): Distinct patterns of desynchronized limb regression in Malagasy scincine lizards (Squamata, Scincidae). PLoS ONE 10 (6): e0126074.
Moch J.G., Senter P. (2011): Vestigial structures in the appendicular skeletons of eight African skink species. Journal of Zoology 285: 274-280.
Omura H. (1980): Morphological study of pelvic bones of the minke whale from the Antarctic. Sci. Rep. Whales Res. Inst. 32: 25-37.
Postacchini F., Massobrio M. (1983): Idiopathic coccygodynia. Analysis of fifty-one operative cases and a radiographic study of the normal coccyx. J. Bone Joint Surg. 65: 1116-1124.
Pyron R.A., Burbrink F.T., Wiens J.J. (2013): A phylogeny and revised classification of Squamata, including 4161 species of lizards and snakes. BMC Evol. Biol. 13: 93.
Rabanus K. (1911): Über das Skelett von Voeltzkowia mira Bttgr. Ein Beitrag zur Osteologie und Eidechsen. In: Reise in Ostafrika in den Jahren 1903-1905 mit Mitteln der Hermann und Elise geb. Heckmann Wentzel-Stiftung ausgefürt. Wissenschaftliche Ergebnisse. Band IV. Anatomie und Entwickelungsgeschichte. Heft 3, p. 279-330. Voeltzkow A., Ed., Schweizerbart’sche Verlagsbuchhandlung, Nägele und Dr. Sproesser, Stuttgart.
Reece J.B., Urry L.A., Cain M.L., Wasserman S.A., Minorsky P.V., Jackson R.B. (2011): Campbell Biology, 9th Edition. Benjamin Cummings, Boston.
Renous S., Gasc J.P. (1979): Etude des modalities de reduction des membres chez un Squamate serpentiforme: Scelotes, scincidé afro-malagasche (1). Ann. Sci. Nat. Zool. Paris 1: 99-132.
Schmitz A., Brandley M.C., Mausfeld P., Vences M., Glaw F., Nussbaum R.A., Reeder T.W. (2005): Opening the black box: phylogenetics and morphological evolution of the Malagasy fossorial lizards of the subfamily “Scincinae”. Mol. Phyl. Evol. 34: 118-133.
Senter P., Ambriocio Z., Andrade J.B., Foust K.K., Gaston J.E., Lewis R.P., Liniewski R.M., Ragin B.A., Robinson K.L., Stanley S.G. (2015): Vestigial biological structures: a classroom-applicable test of creationist hypotheses. Am. Biol. Teach. 77: 99-106.
Senter P., Moch J.G. (2015): A critical survey of vestigial structures in the postcranial skeletons of extant mammals. PeerJ 3: e1439.
Sewertzoff A.N. (1931): Studien über die Reduktion der Organe der Wirbeltiere. Zoologische Jahrbücher. Abt. Anat. Ontog. 53: 611-700.
Siler C.D., Brown R.M. (2011): Evidence for repeated acquisition and loss of complex body-form characters in an insular clade of southeast Asian semi-fossorial skinks. Evolution 65: 2641-2663.
Siler C.D., Rico E.L., Duya M.R., Brown R.M. (2009): A new limb-reduced, loam-swimming skink (Squamata: Scincidae: Brachymeles) from central Luzon Island, Philippines. Herpetologica 65: 449-459.
Siler C.D., Diesmos A.C., Alcala A.C., Brown R.M. (2011): Phylogeny of Philippine slender skinks (Scincidae: Brachymeles) reveals underestimated species diversity, complex biogeographical relationships, and cryptic patterns of lineage diversification. Mol. Phyl. Evol. 59: 53-65.
Stephenson N.G. (1961): The comparative morphology of the head skeleton, girdles and hindlimbs in the Pygopodidae. J. Linn. Soc. Zool. 44: 627-644.
Stokely P.S. (1947): Limblessness and correlated changes in the girdles of a comparative morphological series of lizards. Am. Nat. 38: 725-754.
Tague R.G. (1997): Variability of a vestigial structure: first metacarpal in Colobus guereza and Ateles geoffroyi. Evolution 51: 595-605.
Whiting A.S., Bauer A.M., Sites J.W. Jr. (2003): Phylogenetic relationships and limb loss in sub-Saharan African scincine lizards (Squamata: Scincidae). Mol. Phyl. Evol. 29: 582-598.
Footnotes
Associate Editor: Miguel Carretero.
