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Keywords:

  • eyelids;
  • spectacle;
  • comparative morphology

ABSTRACT

  1. Top of page
  2. ABSTRACT
  3. MATERIAL AND METHODS
  4. RESULTS
  5. DISCUSSION
  6. ACKNOWLEDGEMENTS
  7. LITERATURE CITED

The anatomy and development of the eyelids in squamate reptiles are still relatively unknown, considering its variation within the group. The neotropical Gymnophthalmini are traditionally characterized by having lost the eyelids, but their structure is not well described. In this study, the embryonic development and the adult morphology of the gymnophthalmid eye, with special attention to the eyelids, the nictitating membrane, and the spectacle are described. The eye in some Gymnophthalmini is covered by a spectacle, formed by the embryonic fusion of the dorsal and ventral eyelids, a character possibly synapomorphic to the tribe. The genus Tretioscincus, which floats either as sister to all other Gymnophthalmini, or is nested within the group, is unique in showing functional and movable eyelids. Thus, the presence of functional eyelids can be either considered as the primitive condition for the gymnophthalmini or as a re-acquisition of the character, showing the importance of a well-established phylogenetic hypothesis for understanding morphological evolution. Anat Rec, 297:496–504, 2014. © 2014 Wiley Periodicals, Inc.

The eyelids, or palpebral elements, are two horizontal skin folds that appear during embryonic development as dermal thickenings above and under the eye and grow concentrically to cover the cornea (Walls, 1942; Underwood, 1970). Together with the oculomotor muscles, the nictitating membrane, and the lachrymal apparatus, the eyelids compose the ocular adnexa (Walls, 1942). In terrestrial vertebrates the lids act as a physical barrier that protects the eyes against mechanical damage and desiccation, also regulating the amount of light that passes through the pupil (Walls, 1942).

In adult squamates, the eyelids are covered by epidermal scales (Greer, 1983). The ventral eyelid is usually larger than the dorsal, which is generally fixed; the ventral one moves downwards through the contraction of the depressor palpebrae inferioris muscle, attached to its base (Underwood, 1970). The conjunctive space is delimited between the eyelids and the cornea (Underwood, 1970). The nictitating membrane is a movable fold located between the eyelids and the cornea, that slides over the latter acting as a third lid (Walls, 1942); the exocrine secretion of the Harderian gland (which is attached to the medial region of the orbit; Bellairs and Boyd, 1947), lubricates its sliding movement (Payne, 1994). This membrane is associated with three semicircular cartilages arranged vertically (Underwood, 1970).

Movable eyelids are the generalized and primitive condition for Squamata (Kearney, 2003), but in some lineages functional eyelids have been lost and a distinct unmovable structure covers the eye (Walls, 1942; Underwood, 1970; Kearney, 2003). In Amphisbaenia and Dibamidae, for example, the eye is covered by scales while in other squamates, such as some species of Pygopodidae, Gekkonidae, Gymnophthalmidae, Phyllodactylidae, Scincidae, Sphaerodactylidae, and Serpentes, the eye is covered by a transparent and rigid structure, called spectacle, or brille (Bellairs and Boyd, 1947). Usually, species that have a spectacle have lost the nictitating membrane (Bellairs and Boyd, 1947; Bellairs, 1948; Rehorek et al., 2000).

It is hypothesized that the spectacle in squamates has evolved as a modification of the nictitating membrane (Johnson, 1927) or of the eyelids (Schwarz-Karsten, 1933; Neher, 1935). Johnson's observations of adult geckos and lacertid lizards led him to conclude that the spectacle was derived from an over-developed nictating membrane, which became transparent and fused with the inner margin of the dorsal eyelid. The latter two authors, on the other hand, showed that the spectacle of natricid and viperid snakes was derived from the embryonic fusion of the eyelids (Schwarz-Karsten, 1933; Neher, 1935). A few years later, Walls (1942) supported the idea of the spectacle being derived from a modification of the eyelids after having analyzed the morphology of such structure in adult vertebrates.

The development of the spectacle in lizards has never been investigated. Even so, some authors (Bellairs and Boyd, 1947; Greer 1983, 1989) attempted to propose an evolutionary scenario for the palpebral origin of the lizard spectacle based on the analysis of the morphological variation of eyelids and spectacle in several lizard taxa, some of which showed intermediate morphologies. These authors proposed, therefore, that the evolution of the spectacle would be the result of a series of gradual transformations: a ventral movable eyelid covered with pigmented scales, followed by a condition in which the scales become gradually transparent and the eyelid progressively immovable, and then finally fusing with the dorsal eyelid. Greer (1989) illustrated this series of transformation in some Australian skinks: in Eulamprus murrayi the ventral eyelid is totally scaled and pigmented; in Pseudemoia entrecasteauxii it is covered by a large transparent scale; in Morethia butleri it is also covered by a non-pigmented scale and is no longer movable but still not fused to the dorsal eyelid; and in Morethia taeniopleura the fused ventral and dorsal eyelids represent the so called spectacle. However, their proposal (Bellairs and Boyd, 1947; Greer 1983, 1989), of this progressive morphological transformation of the eyelids into a spectacle had no phylogenetic support.

The spectacled gymnophthalmids are placed in the monophyletic tribe Gymnophthalmini (sensu Pellegrino et al., 2001; Castoe et al., 2004; Rodrigues and dos Santos, 2008), a neotropical group of lizards comprising nine genera: Calyptommatus, Gymnophthalmus, Micrablepharus, Nothobachia, Procellosaurinus, Psilophthalmus, Scriptosaura, Vanzosaura, and Tretioscincus. The latter is the only genus with fully movable eyelids. In the topology obtained from the morphological data of Rodrigues (1991b), Tretioscincus is recovered as basal to the remaining Gymnophthalmini, while in the more recent molecular phylogenies (Pellegrino et al., 2001; Castoe et al., 2004, and Pyron and Wiens, 2013) this genus is nested within the group. Micrablepharus, recovered by Rodrigues (1991b) as sister to Tretioscincus and to the remaining Gymnophthalmini, comprises two species, each showing a different eyelids morphology: M. maximilliani has an immovable ventral lid that is partially separated from the dorsal eyelid, while M. atticolus has completely fused eyelids (Rodrigues, 1996). In the molecular topologies, Micrablepharus is also nested within the group, being recovered as basal to Tretioscincus (Pellegrino et al., 2001) or as sister to it (Castoe et al., 2004). The remaining genera have been traditionally referred to as being “eyelidless”; however, a detailed analysis of eye morphology within the group has never been undertaken.

Here we present a comparative study of the embryology and adult anatomy of some eye's adnexa in gymnophthalmid lizards and establish a hypothesis for the homology and evolution of the eyelids and of the spectacle in the tribe Gymnophthalmini.

MATERIAL AND METHODS

  1. Top of page
  2. ABSTRACT
  3. MATERIAL AND METHODS
  4. RESULTS
  5. DISCUSSION
  6. ACKNOWLEDGEMENTS
  7. LITERATURE CITED

Study Group

We sampled most Gymnophthalmini genera, as well as carefully chosen outgroup species with the intention of including at least one representative of each of the subgroups of the Gymnophthalmidae. The material examined is listed in Table 1.

Table 1. Material examined with respective description of adult eye morphology, the stage analysed, voucher numbers, and techniques used for analysis
Major groupSpeciesEye morphologyDevelopmental stageExamined materialTechnique
  1. Collections acronyms: CJ, Carlos Jared; MZUSP, Coleção de Herpetologia do Museu de Zoologia da Universidade de São Paulo; MTR, Miguel Trefaut Rodrigues. Abbreviations: DO—direct observation; SEM—scanning electron microscopy; H—histological sections.

AlopoglossinaeAlopoglossus angulatusVentral eyelid with transparent palpebral scales; vestigial nictitating membraneAdultMZUSP 53683/78128/100487; MTR 67487DO/SEM/H
CercosaurinaeBachia flavescensVentral eyelid with transparent palpebral scaleAdultMZUSP 95396DO
 Bachia scolecoidesVentral eyelid palpebral scaleAdultMZUSP 82526DO
 Cercosaura ocellataVentral eyelid with transparent palpebral scale; vestigial nictitating membraneAdultMZUSP 91700/95275DO/H
EcpleopodinaeEcpleopus gaudichaudiiVentral eyelid with transparent palpebral scalesAdultMZUSP 93440DO
GymnophthalminiCalyptommatus sinebrachiatusEyelids fused into spectacle; nictitating membrane absentAdult/embryo stages 1–12MRT 18049/18485/70407; CJ 81DO/SEM/H
 Gymnophthalmus vanzoiEyelids fused into spectacleAdultMZUSP 95215DO
 Micrablepharus atticolusEyelids fused into spectacleAdult/embryo stages 8, 11MZUSP 95263DO
 Micrablepharus maximilianiEyelids partially fused into spectacle; vestigial nictitating membraneAdultMZUSP 17347/97131; CJ 72/73DO/SEM/H
 Nothobachia ablepharaEyelids fused into spectacle; nictitating membrane absentAdult/embryo stages 1–12MZUSP 77948/76893; CJ 946DO/SEM/H
 Psilophthalmus paeminosusEyelids fused into spectacleEmbryo stage 10MZUSP 71900DO
 Procellosaurinus erythrocercusEyelids fused into spectacleAdult/embryo stage 8MZUSP 92896DO
 Procellosaurinus tetradactylusEyelids fused into spectacle; nictitating membrane absentAdultMZUSP 71604; CJ 957DO/H
 Scriptosaura catimbauEyelids fused into spectacleAdultCJ 116DO
 Tretioscincus agilisMovable, with transparent scaleAdultMZUSP 78316/78132DO
 Tretioscincus oriximinensisVentral eyelid with transparent palpebral scale; movable nictitating membraneAdultMZUSP 78128; MTR 35255DO/SEM/H
 Vanzosaura rubricaudaEyelids fused into spectacleAdult/embryo stages 5, 7, 8, 12MZUSP 71844DO
HeterodactyliniColobodactylus dalcyanusVentral eyelid with transparent palpebral scaleAdult/embryo stages 9, 12MZUSP 95598DO
IphisiniColobosaura modestaVentral eyelid with transparent palpebral scale; well-developed nictitating membraneAdult/embryo stages 8, 11/12, 12MZUSP 88697/94424DO/H
RhachisaurinaeRhachisaurus brachilepisVentral eyelid with transparent palpebral scaleAdultMZUSP 20389DO

External Morphology

Adults

Adult individuals representing all species included in this study were analyzed under a stereomicroscope and digitally photographed.

Embryos

Embryos of a few gymnophthalmid species (Table 1), staged according to Roscito and Rodrigues (2012), were also analyzed under the stereomicroscope.

Scanning electron microscopy (SEM)

The eyes of adult individuals representing five species (Table 1) were investigated by scanning electron microscopy. Species were chosen based on eye morphology (representatives with movable and immovable eyelids) and also on their phylogenetic placement within the group. The head of the specimens used for analysis by SEM was split sagittally into right and left halves, mounted on metal stubs, dried by the critical point method, coated with gold in a sputtering device, and finally examined in a FEI Quanta 250 scanning electron microscope, operating at 10 kV.

Histology

The heads of selected adult specimens (Table 1) were decalcified in 4% EDTA for 4 weeks, dehydrated in ethanol and embedded in glycol methacrylate (Leica). Serial transverse sections (3 μm) were stained with toluidine blue-fuchsin, and analyzed using an Olympus BX51 light microscope equipped with a digital camera (Leica DM 2500).

RESULTS

  1. Top of page
  2. ABSTRACT
  3. MATERIAL AND METHODS
  4. RESULTS
  5. DISCUSSION
  6. ACKNOWLEDGEMENTS
  7. LITERATURE CITED

Embryological Development of the Eyelids

The eyelids of Calyptommatus sinebrachiatus, Nothobachia ablephara, and Vanzosaura rubricauda are first observed between stages 5 and 6 as dermal thickenings at the ventral and dorsal margins of the optic cup.

In Calyptommatus sinebrachiatus, Colobosaura modesta and Micrablepharus atticolus, the lids at the stage 8 (Figs. 1A,B and 2A,B) grew over the optic cup and covered partially the lateral region of the eye (Figs. 1 and 2).

image

Figure 1. Embryonic development of the eye in Colobosaura modesta A, B. Stage 8 embryo seen in lateral and frontal views, respectively. C, D. Stage 11–12 embryo seen in lateral and frontal views, respectively. E, F. Stage 12 embryo seen in lateral and frontal views, respectively. Scale bars for A and B = 0.2 mm; C–F = 0.5 mm. Abbreviations: del, dorsal eyelid; i, iris region; p, pupil region; si, infraocular scale; vel, ventral eyelid; vet, translucid disc of ventral eyelid.

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image

Figure 2. Embryonic development of the eye in Micrablepharus maximiliani A, B. Stage 8 embryo seen in lateral and frontal views, respectively. C, D. Stage 11 embryos seen in lateral and frontal views, respectively. Scale bars for A, B, D = 0.2 mm; C = 0.5 mm. Abbreviations: del, dorsal eyelid; i, iris region; p, pupil region; sb, sclerotic bone; spu, unfused region of spectacle; vel- ventral eyelid.

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Colobodactylus dalcyanus has at stage 9 eyelids in a more developed morphology covering partially the optic cup margins, but did not reach the iris region of the eye.

In Psilophthalmus paeminosus at the stage 10 the ventral reaches the iris region while the dorsal is restricted to the dorsal margin of optic cup.

At stage 11 the dorsal eyelid is above the region of the iris, while the ventral eyelid extends beyond the level of the pupil contacting the dorsal eyelid (Figs. 1C,D and 2C,D). The final patterns of scaling and pigmentation are only seen around stage 12 (Fig. 1E,F). In all gymnophthalmid embryos examined, the ventral and dorsal eyelids show different growth rates: growth of the ventral lid is much more pronounced than that of the dorsal one (Fig. 1C,D), which results in the lens being covered by the ventral lid only (Figs. 1E,F and 2C,D). Scaling and pigmentation are only seen around stage 12 (Fig. 1E).

Interspecific differences regarding eyelid development are manifested from stage 11 onward: in Colobosaura modesta and Colobodactylus dalcyanus, the eyelids remain separated from each other (Fig. 1), while in Calyptommatus sinebrachiatus and Micrablepharus maximiliani the ventral and dorsal eyelids are totally or partially fused, respectively, above the iris region (Fig. 2; Roscito and Rodrigues, 2012).

Adult Comparative Morphology

The eyelids

In Alopoglossus angulatus (Fig. 3A,B), Bachia flavescens, B. scolecoides, Cercosaura ocellata, Colobodactylus dalcyanus, Colobosaura modesta, Ecpleopus gaudichaudii, Rhachisaurus brachylepis, Tretioscincus agilis, and T. oriximinensis (Fig. 3C,D), both eyelids are distinct and movable, but the ventral eyelid is larger than the dorsal.

image

Figure 3. The eye of gymnophthalmids lizards, seen in lateral view. A, B. Alopoglossus angulatus. C. Tretioscincus agilis; D. Tretioscincus oriximinensis; E, F. Micrablepharus maximiliani; G, H Nothobachia ablephara I, J. Calyptommatus sinebrachiatus. A, C, E, G, I taken under the stereomicroscope; B, D, F, H, J correspond to scanning electron microscopy images. Scale bars for A, C, E, G–J = 0.5 mm; B = 2.0 mm; D, F = 1.0 mm.

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In Alopoglossus angulatus (Figs. 3A,B and 4A), Bachia flavescens, B. scolecoides, Cercosaura ocellata (Fig. 4B), Colobodactylus dalcyanus, Colobosaura modesta (Fig. 4C), Ecpleopus gaudichaudii, Rhachisaurus brachylepis, Tretioscincus agilis (Fig. 3C), and T. oriximinensis (Figs. 3D and 4D), the scales that cover the ventral eyelid are translucent, and the ventral lid is surrounded by small granular scales. In A. angulatus (Fig. 3A,B) and E. gaudichaudii two or three palpebral scales cover the ventral eyelid, while in Bachia flavescens, B. scolecoides, and C. modesta a single scale covers the ventral eyelid.

image

Figure 4. Longitudinal sections of the eye of gymnophthalimd lizards. A. Alopoglossus angulatus; B. Cercosaura ocellata; C. Colobosaura modesta; D. Tretioscincus oriximinensis; E. Micrablepharus maximiliani; F. Procellosaurinus tetradactylus; G. Nothobachia ablephara; H. Calyptommatus sinebrachiatus. Scale bars for A–F = 0.5 mm; G = 0.2 mm; H = 0.1 mm. Abbreviations: co, cornea; cs, conjunctival space; del, dorsal eyelid; l, lens; nm, nictitating membrane; nc, nictating membrane cartilage; re, retina; si, infraocular scale; sl, internal space of the ventral lid; ss, supraciliary scale; sp, spectacle; spu, unfused region of spectacle; vel, ventral eyelid; vet, translucid disc of ventral eyelid.

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In Micrablepharus maximiliani the ventral lid is partially separated from the dorsal eyelid (Fig. 4E). The ventral eyelid is fixed and completely covers the eye, while the dorsal eyelid is greatly reduced in size; a small slit remains in between them that is concealed under the superciliaries scales and surrounded by a line of small granules (Rodrigues, 1996), and can only be seen externally, by manipulation of the ventral lid. Sand grains were observed inside the conjunctival space or sub-brillar space, showing that, despite the position of the slit, substrate particles can still enter through it.

In Procellosaurinus tetradactylus (Fig. 4F), Nothobachia ablephara (Figs. 3G,H and 4G), and Calyptommatus sinebrachiatus (Figs. 3I,J and 4H) the eye is covered by a single transparent structure, resulting in the closure of the conjunctival space. This structure is referred to as the spectacle. When seen in cross-section, the spectacle of N. ablephara and C. sinebrachiatus (Fig. 4G,H) is thicker than that of M. maximiliani and P. tetradactylus (Fig. 4E,F). The fused eyelids of C. sinebrachiatus (Fig. 3I,J) are partially covered by a modified scale (Rodrigues, 1991a).

The nictitating membrane

The nictitating membrane is located between the eyelids and the cornea, and is quite variable among the gymnophthalmids analyzed. A well-developed nictitating membrane, associated with nictitating cartilages, completely covers the cornea of Colobosaura modesta (Fig. 4C) and Tretioscincus oriximinensis (Fig. 4D). On the other hand, in Alopoglossus angulatus (Fig. 4A), Cercosaura ocellata (Fig. 4B), and Micrablepharus maximiliani (Fig. 4E) this membrane is reduced to a small projection at the base of the cornea and of the ventral eyelid. In Procellosaurinus tetradactylus, (Fig. 4F), Nothobachia ablephara, (Fig. 4G) and Calyptommatus sinebrachiatus (Fig. 4H), the nictitating membrane is absent.

DISCUSSION

  1. Top of page
  2. ABSTRACT
  3. MATERIAL AND METHODS
  4. RESULTS
  5. DISCUSSION
  6. ACKNOWLEDGEMENTS
  7. LITERATURE CITED

The data from the present study supports that this single structure in some gymnophthalmini is formed by the embryonic fusion of the dorsal and ventral eyelids, and not derived from the nictitating membrane as proposed by Johnson (1927) for a few squamate taxa. The Gymnophthalmini lizards have been traditionally referred to as eyelidless lizards (Boulenger, 1885; Rodrigues and dos Santos, 2008). However, our results made clear that the eyelids are present in all species of the group and fused, in a subset of it. The embryonic fusion of the eyelids in Gymnophthalmini is possibly a synapomorphic character of the tribe.

In the material examined it is possible to see that the ventral eyelid is much larger than the dorsal one, contributing to a greater extent to the spectacle; because of that, palpebral fusion in the gymnophthalmini embryos analyzed takes place above the pupil region (Fig. 2C,D). This pattern is in sharp contrast to what is seen in colubrid and viperid snakes, in which the eyelids grow concentrically and fuse at the level of the pupil (Schwarz-Karsten, 1933; Neher, 1935). The scarce information of amphisbaenian embryology (Montero et al., 1999) supports the hypothesis that the scale covering their eyes seems to be formed by the fusion of the eyelids (Kearney, 2003). However, based on the description of Montero et al. (1999) we were unable to compare their embryonic developmental pattern and determine if it was similar to that described for snakes.

The only gymnophthalmini with eyelids and nictitating membrane is Tretioscincus, and the present results do not reveal any relevant morphological difference when compared to the eye of other gymnophthalmids that have similar eye morphology—including the genus Alopoglossus, which is consistently retrieved as basal to the remaining gymnophthalmids (Pellegrino et al., 2001; Castoe et al., 2004). The remaining gymnophthalmini genera analyzed here show some kind of modification: the nictitating membrane is reduced or absent and the eyelids are either fixed but still distinct, or partially/completely fused.

The phylogenetic position of Tretioscincus within the Gymnophthalmini is not yet resolved, and this allows for different possible evolutionary scenarios to explain the evolution of palpebral elements in the group. Rodrigues (1991b) and Benozzati and Rodrigues (2003) place Tretioscincus as basal to the tribe, and the genus Micrablepharus as the sister group of the remaining spectacled gymnophthalmini.

On the other hand, the three most comprehensive molecular phylogenies for the Gymnophthalmidae reveal Tretioscincus deeply nested within the Gymnophthalmini (Pellegrino et al., 2001; Castoe et al., 2004; Pyron et al., 2013), recovering Gymnophthalmus, a spectacled lizard, as basal to the group (Castoe et al., 2004) or the lower relationships unresolved (Pellegrino et al., 2001) or not highly supported (Pyron et al., 2013). In the topology of Pellegrino et al. (2001), the genus Micrablepharus is recovered as basal to Tretioscincus, while in that of Castoe et al. (2004), these two genera are recovered as sister-groups. This is also the case in Pyron and colleagues (2013) where Tretioscincus and Micrablepharus are sister to a clade comprising Vanzosaura and Procellosaurinus.

There are two possible scenarios to explain the occurrence of spectacles in the Gymnophthalmini. The spectacle could have been evolved several times independently, or movable eyelids have been reacquired in Tretioscincus (at least in Tretioscincus oriximinensis).

The reacquisition of functional eyelids finds support in other hypotheses of relationships proposed for squamate taxa. One example are the eublepharid lizards, the only gekkotan clade with fully movable eyelids (Bellairs, 1948), and are placed in a derived position with respect to the spectacled diplodactilids and pygopodids (Kluge, 1967; Conrad and Norrell, 2006; Conrad, 2008; Gamble et al., 2008, 2011; Gauthier et al., 2012).

The homology hypothesis of the spectacle, in which this structure arises from the embryonic fusion of the eyelids, is confirmed for a few snake species (Schwarz-Karsten, 1933; Neher, 1935). Based on such information, it is generally accepted that the spectacle in Gekkota, Anguidae and Scincidae lizards (Bellairs and Boyd, 1947; Kearney, 2003) is formed by similar processes, although no embryological study has been conducted in order to confirm such hypothesis. The data presented in this work adds embryological evidence to the formation of the spectacle in lizards. The anatomy of the lizard eye is still poorly understood, considering the diversity of forms and occupied habitats, which is intimately related to morphological adaptations of all body systems, including the eye. Eyelids associated scales and other membranes that cover the cornea, as is the case of the nictitating membrane present in a few species, show a great variation among squamate reptiles, and are valuable characteristics that can be used for understanding the evolutionary relationships between species.

ACKNOWLEDGEMENTS

  1. Top of page
  2. ABSTRACT
  3. MATERIAL AND METHODS
  4. RESULTS
  5. DISCUSSION
  6. ACKNOWLEDGEMENTS
  7. LITERATURE CITED

The authors are grateful to H. Zaher and C. Castro-Melo for granting access and loaning of specimens under their care at Museu de Zoologia da Universidade de São Paulo, and the use of the optical facilities. They thank D. Pavan, E. Santos, and F. Curcio for help in the field.

LITERATURE CITED

  1. Top of page
  2. ABSTRACT
  3. MATERIAL AND METHODS
  4. RESULTS
  5. DISCUSSION
  6. ACKNOWLEDGEMENTS
  7. LITERATURE CITED
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