Open Access

The embryology of the retinal pigmented epithelium in dwarf geckos (Gekkota: Sphaerodactylinae): a unique developmental pattern

BMC Developmental Biology201414:29

DOI: 10.1186/1471-213X-14-29

Received: 31 July 2013

Accepted: 12 June 2014

Published: 30 June 2014

Abstract

Background

The retinal pigmented epithelium (RPE) is a rounded shaped structure in almost all lizards. In the New World dwarf geckos, this structure shows an unusual morphology. In addition to this ocular character, we describe notable differences in the development of these geckos in comparison with available developmental staging tables for other geckos and squamate reptiles.

Results

We identified two main patterns of development of the RPE for squamates. These patterns were mapped onto a metatree of concordant hypotheses of squamates based on molecular data. During post-ovopositional stages the representative species of sphaerodactyls exhibit a RPE layer that transforms gradually from an ovoid form into the generalized spherical form. Sphaerodactyls are the only group of squamates in which this pattern is known.

Conclusions

This transition might be circumstantial evidence that the accessory RPE plays a role in providing additional protection for their apomorphic concaviclivate temporal fovea. We also report the presence of conjunctival papillae in a developmental stage prior to the formation of scleral ossicles. This developmental progression is similar to that of birds and turtles.

Keywords

Squamata Eye development Concaviclivate temporal fovea Conjunctival papillae

Background

The New World dwarf geckos (Sphaerodactylinae) or ‘sphaerodactyls’ include about 164 species, accounting for more than 11% of the known diversity of the Gekkota [13]. Originally the term “sphaerodactyls” was used to refer exclusively to members of genus Sphaerodactylus[49], but it has more recently been used to include the genera Gonatodes, Lepidoblepharis, Chatogekko, Coleodactylus, Pseudogonatodes, and Sphaerodactylus[1, 10, 11]; in this paper, we follow the latter usage.

Sphaerodactyls are diurnal and represent some of the most extremely miniaturized extant amniotes (viz. Sphaerodactylus ariasae and S. parthenopion, [12, 13]), equaled only by tiny leaf chameleons from Madagascar [14, 15]. Some sphaerodactyls are climbers and utilize vertical surfaces [16, 17], but the majority of them are surface dwellers, found in forest or littoral leaf litter [4, 18, 19]. They combine their small size with a secretive lifestyle, which is common among lizards [20] and is an ecological niche that is known to have been occupied by members of Squamata as early as 120 million years ago [21].

Sphaerodactyls are diurnal and develop a shallow, bowl-like or concaviclivate temporal fovea in the retinal tissue [22, 23]. These geckos are also known to be affected by variations of environmental factors such as illumination [24]. For example, Sphaerodactylus macrolepis from forested habitats detects motion better in dim light than conspecifics from coastal areas, which detect movement better in much brighter conditions [25].

Binocularity (stereopsis) for deep perception in this group might also be facilitated because of their large eyes and generally narrow snouts [JDD, pers. obs.], analogous to other squamates with binocular vision, such as vine snakes [26]. Narrow snouts coupled with ocular adaptations to diurnal habits suggest that this group of geckos may exhibit some anatomical differences from other lizards, including nocturnal geckos.

Sixty years ago, Garth Underwood developed a classification of geckos using visual system characters [22, 2729]. Under this classification, sphaerodactyls were placed in a separate family based on several morphological characters, such as presence of a temporal fovea, a round pupil (elliptical with straight vertical margins when closed), and presence of a brille covering the eye [22, 29], in combination with additional osteological [30] and integumentary [31] characters.

Subsequent to Underwood’s classification of geckos [29], morphological evidence has been accumulated in support of the monophyly of the sphaerodactyls and their relationships with other gekkotan genera [11, 3239]. Recent molecular evidence has corroborated the split of sphaerodactyls from the Gekkonidae sensu stricto and grouped them together in an expanded Family Sphaerodactylidae with the Caribbean genus Aristelliger and the Old World genera Euleptes, Pristurus, Quedenfeldtia, Saurodactylus and Teratoscincus ([1, 2], Figure 1). Although Underwood’s classification is outdated, some of the characters that he used still have taxonomic utility [40], for example, the eye morphology that he attributed to the sphaerodactyls has also been found in most of the genera recently placed in the family (e.g., Aristelliger, Pristurus, Quedenfeldtia, Saurodactylus, Teratoscincus).
https://static-content.springer.com/image/art%3A10.1186%2F1471-213X-14-29/MediaObjects/12861_2013_Article_800_Fig1_HTML.jpg
Figure 1

Two alternate hypotheses for the relationships of Sphaerodactylidae. A) Molecular hypothesis [2]; B) Morphological hypothesis [38]. Gray shading indicates the sphaerodactyl group.

However, the latest molecular and morphological hypotheses of relationships within the Sphaerodactylidae are not entirely congruent [2, 39]. Molecular data indicate a single origin for the sphaerodactyls (Figure 1A) whereas morphology suggests that the Northeast African/Middle Eastern genus Pristurus is nested within the sphaerodactyls (Figure 1B). These two hypotheses also differ from the previous phylogenetic hypothesis based on morphology of the group [11].

Here we investigate in detail a preliminary observation by Werner [41] on eye development in Sphaerodactylus argus in postovopositional stages. Although Werner did not describe in text the changes of the eye during development, he did illustrate a remarkable change in eye morphology across the embryological stages of this species. Using Werner’s staging for Sphaerodactylus argus, it can be seen that in embryos at approximately stages 30–31, the outer layer of the optic cup contains an ovoid retinal pigment epithelium (henceforth RPE), extending considerably towards the posterolateral portion of the eye. After stage 31, the iris is clearly differentiated but this pigmentation extends posteriorly, forming an ovoid extension and creating the appearance of a bandit’s mask in the embryo. This posterior extension of RPE remains until approximately stage 35 when it gradually becomes less accentuated and the iris becomes more rounded (Figure five in [41]).

In this paper we present information on the embryology of sphaerodactyls, making special reference to eye development and the retinal pigmented epithelium, and contrast this with embryological information from other lizard families, including some nocturnal gekkotans. To date most contributions to the study of gekkotan ontogeny have been descriptions of the external morphology across developmental series [4145] and osteological descriptions of a few species [4651]. Only some studies have evaluated the phylogenetic significance of embryological data for squamate systematics [5257]. This study explores the distribution of two contrasting patterns of development for the eye, and has the potential to provide additional morphological evidence for the understanding of the evolution of this diurnal clade of geckos.

Methods

Obtaining complete developmental series from natural populations of geckos is difficult because of their small egg clutches. Sphaerodactylids lay a maximum of two eggs per clutch, and most sphaerodactyl species lay only one [1]. We describe morphological changes in squamate specimens during post-ovopositional stages 28–42. We mainly used the developmental diagrams of Sphaerodactylus argus[41] to assess the stages, which follow a previous study [58] on Lacerta agilis. We tried to find some agreement between these development tables and the recently described table for the eublepharid gecko Eublepharis macularius[45], which is based on Gallus gallus[59], but there are substantial differences between comparable stages among species. This observation is congruent with previous comparisons of embryos from different species in which variation in form due to allometry, heterochrony, and differences in body plan and somite number have been reported [60]. We determined the developmental stage by examining external characters such as pharyngeal clefts, eyelids, tympanic aperture, limbs, scale morphology, and pigmentation. These structures have been used in recent developmental staging studies [44, 45, 6163].

Direct observations of eye development were observed in 88 embryos of nine species. We examined eye development in embryos from different sphaerodactyl species (Chatogekko amazonicus, Coleodactylus meridionalis, Coleodactylus sp., Gonatodes albogularis, Gonatodes humeralis, Sphaerodactylus macrolepis), representatives from other gekkotan clades (i.e., Gekkonidae, Phyllodactylidae), and other squamate families (Amphisbaenidae, Anguidae, Iguanidae, Polychrotidae, Scincidae, Teiidae, Tropiduridae, Dipsadidae). All squamate embryos in this study were extracted from eggs collected in the field, and cataloged at the Museu de Zoologia, Universidade de São Paulo, Brazil (MZUSP), Museo de Zoología de la Universidad de Puerto Rico, Río Piedras Campus, San Juan, Puerto Rico (UPRRP), and Aaron M. Bauer personal collection at Villanova University, USA (AMB).

The observed visual system characters and additional morphological changes were compared with previous descriptions of the embryology of other squamate groups (i.e., Agamidae, Chamaeleonidae, Dactyloidae, Eublepharidae, Scincidae, Lacertidae) based on literature sources [41, 44, 45, 58, 6369], see Additional file 1 for details on the source of specimens. Development patterns of the REP were mapped as a single character onto a metatree of squamates using the Module Ancestral State Reconstruction (parsimony ancestral states) on Mesquite Version 2.75 [70].

Animals were euthanized according to an approved protocol for ectothermic embryo use (available at: http://www.iacuc.org). The embryos were removed from the egg and immersed in a solution of ethyl 3-aminobenzoate methanesulfonate 0.2%. This protocol of euthanasia has been approved by Comissão de Ética no Uso de Animais do Instituto Butantan (Protocol CEUAIB 944/12), Sao Pablo, Brazil and entirely meets the terms of the Institutional Animal Care and Use Committees (IACUC, U.S.A.) and the Federal Constitution (FC, Brazil) Law 11974/2008 for breeding and using animals in teaching and scientific research.

Specimens were photographed at the Museu de Zoologia, Universidade de São Paulo using a modular Leica M205 stereo microscope (Leica Microsystems GmbH, Wetzlar Germany) with a digital color Leica DFC425 microscope camera. Images were processed on a desktop computer running Leica LAS Montage software. Snout-vent length (SVL) measurements were taken for each embryo. Figures in the text are numbered sequentially and include a coordinate system composed of a letter and number. Each letter represents a species, and all the embryos referable to that species are organized sequentially following the letter in their corresponding embryological stage (number in the horizontal rows), for example Figure 2A-28, refers to Gonatodes albogularis at stage number 28.
https://static-content.springer.com/image/art%3A10.1186%2F1471-213X-14-29/MediaObjects/12861_2013_Article_800_Fig2_HTML.jpg
Figure 2

Embryos from five species of sphaerodactyls. Inset, eye detail at the stage 33 of Gonatodes albogularis. A) Gonatodes albogularis; B) Gonatodes humeralis; C) Chatogekko amazonicus; D) Coleodactylus meridionalis and Coleodactylus sp.; E) Sphaerodactylus macrolepis mimetes. Specimen numbers: A-28) MZUSP 99997; A-31) MZUSP 99998; A-33) MZUSP 99999; A-40) MZUSP 100117; A-41) MZUSP 100113; B-29) MZUSP 101107; B-35) MZUSP 101108; B-41) MZUSP 101109; C-34) MZUSP 101105; D-36, upper) MZUSP 101099; D-36, lower) MZUSP 101103; E35, E42) UPRRP uncataloged. Numbers at the left side indicate the approximated embryonic stage between oviposition (O) and eclosion (E) based on the developmental table of Eublepharis macularius[48]. Scale bar equals 1 mm.

Results and discussion

Post-ovopositional embryology in sphaerodactyls with emphasis on the eye

Stage 28–29

Non-ocular remarks: The mesencephalon bulges at the back of the head, and the pharyngeal clefts I and II are open. At this stage, forelimb and hindlimb buds are visible, with the former larger than the latter. The paddle-shaped autopodium starts to develop by stage 29. The tip of the maxillary process reaches the level of the choroid fissure. These stages are represented by two embryos, one of Gonatodes albogularis (Figure 2A-28), and one of G. humeralis (Figure 2B-29).

Eye: An ovoid portion of the eye of specimen in these stages is covered by the RPE, including the posterior region; the choroid is pigmented by a homogeneous layer and the iris is undefined. There is a concentration of melanosomes at the posterior side of the area that corresponds to the iris. The margins of the choroid fissure are still in contact with one another, and persist until about stage 29, as seen in G. humeralis (Figure 2B-29).

Comparison with other squamates: At this stage sphaerodactyls appear similar to Hemidactylus mabouia (Figure 3A-29); the choroid fissure persists, melanosomes of the RPE are concentrated on the equatorial region, and the limb buds show further development, with a paddle-shaped autopodium. In other lizards at a corresponding stage (e.g., Eublepharis macularius, Lacerta agilis, Anolis sagrei), the choroid fissure is present, and the limb buds appear as mere protuberances [45, 58, 64]. Sphaerodactyls differ from other lizards in the ovoid shape of the RPE of the eye (Figure 2A-28, 2B-29).
https://static-content.springer.com/image/art%3A10.1186%2F1471-213X-14-29/MediaObjects/12861_2013_Article_800_Fig3_HTML.jpg
Figure 3

Embryos from four species used as reference material. A) Hemidactylus mabouia; B) Phyllopezus pollicaris; C) Tupinambis merianae; D) Polychrus acutirostris. Specimen numbers: A-29) MZUSP 101110; A-34) MZUSP 101102; A-41) MZUSP 101106; B-33) MZUSP 101098; B-36) MZUSP 101100; C-29) MZUSP 101126; C-33) MZUSP 101130; C-38) MZUSP 101128; D-29) MZUSP 101124; D-32) MZUSP 101122; D-36) MZUSP 101121. Numbers at the left side indicate the approximated embryonic stage between oviposition (O) and eclosion (E) based on the developmental table of Eublepharis macularius[45]. Scale bar equals 1 mm.

Stage 31–32

Non-ocular remarks: The mesencephalic bulge is less prominent, and the pharyngeal clefts I and II are closed. The maxillary process reaches the nasal capsule and the mandibular process is very close to anterior margin of the eye. Forelimbs and hindlimbs are similar to the previous stage, the autopodium is flat and paddle-like. The stylopodium and zeugopodium are undifferentiated. This stage is represented by Gonatodes albogularis (Figure 2A-31).Eye: The pigmentation is more uniform than previous stage, the upper eyelid is visible, and the choroid fissure is closed (Figure 2A-31). The iris starts to become delimited, the RPE larger around the iris area than in the posterior part.

Comparison with other squamates: At this stage, the RPE of sphaerodactyls has a distinct ovoid shape; Eublepharis macularius has been described as having a kidney-shaped eye during this stage [45], but its overall shape tends to be more rounded, as it is in other lizards (e.g., Lacerta agilis, Anolis sagrei) [58, 63]. This can also be seen in slightly later stages of Tupinambis merianae and Polychrus acutirostris (Figure 3C-31, 3D-31). Similar to sphaerodactyls, the upper eyelid covers the dorsal surface of the eye in this stage in Lacerta agilis, and although the upper eyelid has been mentioned in Eublepharis macularius by stage 34, some thickening of the epithelium surrounding the eye in Eublepharis macularius can be observed as early as stage 32 (See Figure three in [45]). At stage 32 the conjunctival papillae are visible in Polychrus acutirostris.

Stage 33–34

Non-ocular remarks: The first signs of a tympanic membrane appear between these stages. The parietal area starts to become swollen. The mandibular process is projected beyond the snout tip yielding a prognathous appearance. The hemipenial buds are visible projecting from the cloaca. Digits well differentiated on both fore limbs and hind limbs, but still webbed. These stages are represented by two embryos, one of Gonatodes albogularis (Figure 2A-33), and one of Chatogekko amazonicus (Figure 2C-34).

Eye: The RPE is more uniform than in the previous stage and both the upper and lower eyelids are visible. The iris is well defined, and the eye still appears ovoid due to the posterior extension of the RPE. Fourteen conjunctival papillae are evident in Gonatodes albogularis at stage 33 (Figure 2A-33). One specimen (MZUSP 100000) at stage 34 had three papillae missing from the posterodorsal region of the eye. The papillae are not visible in stage 34 of Chatogekko amazonicus (Figure 2C-34).

Comparison with other squamates: The tympanic membrane becomes more evident by these stages, as in Hemidactylus mabouia and Tupibambis merianae (Figure 3A-33, 3C-33). In Eublepharis macularius the auditory meatus is apparent by stage 33, whereas this structure is illustrated earlier in Lacerta agilis (Stage 27 in [58]), when the limbs are merely buds. During these stages, digits of sphaerodactyls are more well-differentiated than those of Eublepharis macularius[45], and the degree of interdigital webbing is variable. In sphaerodactyls, Hemidactylus mabouia and Phyllopezus pollicaris the digits are almost free of webbing (Figure 2A-33, 2C-34 and 3A-34, 3B-33), whereas Tupinambis merianae and Polychrus acutirostris are more extensively webbed (Figure 3C-33). Upper and lower eyelids are well developed in sphaerodactyls, Eublepharis macularius, Phyllopezus pollicaris (Figure 3B-33). The conjunctival papillae are visible in Tupinambis merianae (Figure 3C-33), but not in Phyllopezus pollicaris (Figure 3B-33).The RPE of the eye has a roughly circular shape restricted to the iris in all other squamates reviewed, whereas in sphaerodactyls the RPE remains ovoid (Figure 2A-33, 2C-34).

Stage 35

Non-ocular remarks: The parietal swelling is more prominent and the auditory meatus contains a better-defined tympanum than in previous stages. The mandibular process still extends beyond the snout tip. The digits are nearly free of interdigital webs, and scales start covering the epidermis of the embryos. This stage is represented by three embryos, one of Gonatodes albogularis (MZUSP 100001), one of G. humeralis (Figure 2B-35), and one of Sphaerodactylus macrolepis (Figure 2E-35).

Eye: In the embryo of Gonatodes albogularis the eyelid margin approaches to the margin of the pupil, but in G. humeralis and Sphaerodactylus macrolepis the fusion of upper and lower eyelids into an incipient brille occurs, although a faint suture remains. This character is neomorphic with respect to E. macularius (see Figure four in [45]) and it is produced via peramorphism with respect to all other forms with discrete eyelids. Fusion of eyelids in the Gekkota can be interpreted to have either occurred once with one reversal in the Eublepharidae (geckos with unfused eyelids) or to have been a product of two independent fusions in the Pygopodoidea and the Gekkonoidea exclusive of Eublepharidae. Fusion of eyelids has also occurred in the Xantusiidae, snakes, Amphisbaenia, and some gymnophthalmids, scincids and lacertids [52, 7173]. During this stage, the posterior part of the RPE is comparatively smaller and is concentrated around the iris; therefore the pigmented portion of the choroid changes from ovoid to more bilobular, with a smaller posterior hemisphere. In Gonatodes albogularis the reabsorption of the conjunctival papillae is complete.

Comparison with other squamates: By this stage sphaerodactyls and Hemidactylus mabouia have a well developed brille covering the eye, whereas in some geckos (e.g., eublepharids) and other squamates the eyelids remain separated and become thickened, covering the eye laterally and leaving exposed only the area near the iris. It is difficult to establish correspondence of these stages in squamate groups with attenuated bodies (e.g., amphisbaenians, snakes, and some limb-reduced or limbless squamates such as some gymnophthalmids), especially considering that many of the characters used are based on limb development. In these lineages, where the eye is also covered by a brille, the formation of this structure occurs during intermediate embryonic stages, and the complete fusion of eyelids is accomplished within a few stages [68, 73, 74].

Sphaerodactyls show a notable proportional reduction of the RPE posterior to the iris, but their eyes still differ considerably from other lizards with a more circular RPE.

Stage 36–38

Non-ocular remarks: The parietal swelling reduces, the preorbital region of the head is as long or longer than the maximum diameter of the eye, slight mandibular prognathism, digits free of webbing, phalangeal segments begin to differentiate, and initial appearance of claws. Scales cover the whole body except in the parietal region. This stage is represented by two embryos, one each of Coleodactylus meridionalis (Figure 2D-36 upper) and Coleodactylus sp. (Figure 2D-36 lower).

Eye: Fusion of eyelids is completed, forming a brille. The anterodorsal region becomes thickened, forming the supracilliary fold. The RPE posterior to the iris is further reduced in relation to the iris. The eye appears more rounded, but there is some persistent coloration posterior to the iris.

Comparison with other squamates: Integumentary characters such as the development of scales and claws accelerates in all lizards reviewed. In Phyllopezus pollicaris the scales cover the entire body including the parietal area (Figure 3B-36). The size difference between the preorbital region of the head and maximum diameter of the eye is not very marked in sphaerodactyls, which have a high degree of overlap among the snout bones. This overlap reduces the muzzle unit — a common process in miniaturized forms [2, 75]. At approximately this stage in Hemidactylus mabouia, Phyllopezus pollicaris, Eublepharis macularius, and other larger lizards in which the snout is not reduced (e.g., Tupinambis merianae, Polychrus acutirostris, Figure 3C-38, 3D-36), the preorbital area starts to become proportionally larger, appearing more like it does in adults. The RPE of sphaerodactyls is more rounded and the differences with other lizards are less marked, although the RPE in other lizards is more concentrated on the iris area. Gekkotans with eyes covered by a brille differ in size from lizards with eyelids (including Eublepharidae) because the eye in the latter starts to be concealed by the thickened eyelids.

Stage 40

Non-ocular remarks: The external naris appears as a shallow depression, the body is completely covered by scales, and a faint juvenile pigmentation pattern is visible on the dorsum, but not extending onto the limbs. This stage is represented by Gonatodes albogularis (Figure 2A-40).

Eye: The eye approximates the round postnatal form, but some extension of the RPE posterior to the iris is visible.Comparison with other squamates: Lizard embryos at this point exhibit similar dull coloration. Scales around the eye are almost undifferentiated in both lizards with eyelids and ones with a brille (Figure 2A-40).

Stage 41

Non-ocular remarks: The external naris more distinct but remains sealed, pigmentation accentuates and extends to the limbs. This stage is represented by Gonatodes albogularis and G. humeralis (Figure 2A-41, 2B-41).

Eye: The RPE is almost round and restricted to the iris, although there is some posterior extension of the pigmented area covered by the postorbital integument. There are well-defined circumorbital scales around the brille.Comparison with other squamates: Body coloration becomes darker in all embryos. Circumorbital scales more differentiated in both lizards with eyelids and those with brilles (Figure 2A-41, 2B-41, 3A-41).

Stage 42

Non-ocular remarks: The external naris opens, pigmentation becomes accentuated, even extended into the abdominal areas. Egg teeth are present on the upper jaw. This stage is represented by Sphaerodactylus macrolepis (Figure 2E-42).

Eye: The RPE is rounded, with the normal circular pupil of sphaerodactylid geckos. At this stage there is no trace of the supracilliary spine, which is present in several sphaerodactylid genera (e.g. Aristelliger, Gonatodes, Lepidoblepharis, and Sphaerodactylus), which, based on this observation, would appear to develop after eclosion.

Comparison with other squamates: The fine details of the integument such as keeling appear during this stage. This can be seen in Eublepharis macularius and Sphaerodactylus macrolepis (Figure 2E-42). At this stage, Sphaerodactylus macrolepis develops keeled scales in the dorsal part of the body and limbs, but they are not elongated and imbricate as in the adults of this species [76]. The condition of unkeeled granular scales is widespread in sphaerodactyls [31, 32, 39], thus the presence of elongated, keeled, imbricate scales is peramorphic, and it is present in several species of Sphaerodactylus and in the Chatogekko amazonicus complex [2, 77, 78].

Scleral ossicle development

Adult lizards, like many vertebrates, have a series of scleral ossicles that form a bony ring external to the optic cup [79, 80] which maintains the shape of the eyeball [81, 82]. In Gonatodes albogularis, Polychrus and Tupinambis, we observed discrete structures in the conjunctival region of the eyes arranged in a circle surrounding the pupillary region (thereofore identified as conjunctival papillae) at stages 32–33. In Gonatodes albogularis the conjunctival papillae show notable reduction between stages 33 and 34, disappearing altogether by stage 35, indicating that reabsorption took place between these stages (Table 1).
Table 1

Number of scleral ossicles in geckos; presence and conjunctival papillae counts in each embryonic stage

Species

Adult scleral ossicles

Developmental stage

Conjunctival papillae condition

Gonatodes albogularis

14

Stage 31

Absent

14

Stage 33

Present; 14 papillae

14

Stage 34

Present; 11 papillae

14

Stage 35

Absent

Gonatodes humeralis

13-14

Stage 35

Absent

Chatogekko amazonicus

12-14

Stage 34

Absent

Sphaerodactylus macrolepis mimetes

13-14

Stage 34

Absent

Hemidactylus mabouia

?

Stage 34

Absent

Phyllopezus pollicaris

14-15

Stage 33

Absent

Polychrus acutirostris

14

Stage 29

Absent

 

14

Stage 33

Present; 11 papillae

Tupinambis merianae

14

Stage 29

Absent

 

14

Stage 33

Present; 14 papillae

In bird and turtle embryos, the conjunctival papillae appear before the formation of scleral ossicles [83]. The intramembranous ossification of the scleral ossicles has been studied in chicken embryos [84, 85], and they are found to be induced by the conjunctival papillae and, thickenings of the conjunctival epithelium [86, 87]. In a recent study, the presence of the conjunctival papillae was confirmed in the turtle Chelydra serpentina, and it was proposed that this structure plays a similar role in the ossification of the sclerotic ring [85]. The similar position of the scleral ossicles in several groups of Tetrapoda (e.g., chickens and turtles) in conjunction with their similar developmental pattern, has led some authors to claim that they are homologous structures [86]. Our observations of the conjunctival papillae, and their transient apperance in squamate embryos adds evidence to this interpretation of the origin of scleral ossicles in reptiles.

Implications of RPE development in dwarf geckos

Current observations cover most of the squamate clades, including data for at least 24 taxa represented by field-collected embryos and 11 published developmental tables. The pattern of eye development exhibited by the majority of squamates observed involves an outer layer of the optic cup with a RPE that is generally spherical throughout all embryonic stages (Figure 4). This pattern of development is regular across vertebrates [79, 84]. There is, however, some variation within this widespread pattern, e.g., lacertids seem to exhibit a proportionally small pupil at oviposition (Figure 4). Likewise, the conspicuously deviant pattern observed here only among sphaerodactyl geckos is consistent among all constituent taxa sampled (Figure 4).
https://static-content.springer.com/image/art%3A10.1186%2F1471-213X-14-29/MediaObjects/12861_2013_Article_800_Fig4_HTML.jpg
Figure 4

Eye development patterns of the RPE. The terminals in the tree include only those species for which embryological data is available. The two alternative patterns of development of RPE were mapped onto a metatree of Squamata based on molecular hypotheses from four independent studies: Lacertidae [88]; Gekkota [89]; Squamata [90, 91]. Gray branches indicate species with the spherical RPE pattern, black branches ovoid → spherical RPE pattern. Asterisk indicates taxa not observed; orange branches indicate uncertain character state. Diagrams of the RPE at oviposition (O) and eclosion (E) were redrawn from published figures for those species (see text for references). Numbers on the cladogram correspond to the following taxonomic groups: 1-Squamata, 2-Scincidae, 3-Teiidae, 4-Gymnophthalmidae, 5-Lacertidae, 6-Amphisbaenidae, 7-Serpentes, 8-Anguidae, 9-Iguania, 10-Chamaeleonidae, 11-Iguanoidea, 12-Iguanidae, 13-Tropiduridae, 14-Polychrotidae, 15-Dactyloidae, 16-Gekkota, 17-Gekkonoidea, 18-Eublepharidae, 19-Phyllodactylidae, 20-Gekkonidae, 21-Sphaerodactylidae, 22-Sphaerodactylinae (sphaerodactyls). Inset, Sphaerodactylus macrolepis mimetes egg open to expose embryo (Stage 35).

Sphaerodactyls develop an ovoid RPE at oviposition, which gradually changes into a spherical shape when specimens approach eclosion.

Gekkotans including sphaerodactylids have orbits that lack the postorbital bar [50, 92, 93]. A posteriorly open orbit, allows for an increase of eye size, although the orbit in some gekkotans is completed posteriorly by a postorbital tendon between the jugal and the postorbitofrontal, and bounded by adductor muscles [9296]. Although a large eye has the potential to accommodate the posterior extension of RPE, eye size and the posterior extension of the RPE are independent, because the observed eye pattern was not present in other gekkotans with similarly modified skulls [41, 44, 45].

Gonatodes and Spherodactylus have a concaviclivate temporal fovea [22, 23], a type of foveal surface that is also found in primates and some birds with a binocular field of vision. This is in contrast to other reptiles and fish that have deep foveae [97]. A concaviclivate fovea contains an additional concentration of cone cells that has also been regarded as an adaptation to diurnal habits [79, 80]. Since light absorption and filtering are among the functions of the RPE [98, 99], this unique development in sphaerodactyls could potentially serve as protection against light damage in these diurnal geckos. Additionally, a posterior extension of the RPE can provide extra retinal protection to the embryo prior to oviposition, which may prevent damage to the embryo from light exposure to through the thin body wall of gravid females (e.g., from basking or foraging) The latter reduction of RPE observed between stages 34 and 37 (Figure 2) can be linked to changes in eye shape, development of the brille, and origin of the integumentary pigments, which provide accessory protection to the light sensitive photoreceptor cells.

Conclusions

The embryonic development of the eye in the Squamata offers a rich source of variation that potentially can provide new phylogenetic information. A developmental pattern in which the RPE in the outer layer of the optic cup is transformed from ovoid to circular is only known in dwarf geckos. Additional observations on genera closely related to this clade (i.e., Aristelliger, Euleptes, Pristurus, Quedenfeldtia, Saurodactylus, and Teratoscincus) are required to determine precise origin and extension of this character within the Family Sphaerodactylidae.

The development of a posterior extension of RPE is postulated as having the potential to provide an auxiliary protective function to the concaviclivate temporal foveae of dwarf geckos, especially prior to oviposition. The evidence supporting this statement is circumstantial and needs to be tested with experimental data and verified in other diurnal geckos with similar retinal structure.

Declarations

Acknowledgements

We thank the following persons for making embryos available for this study: H Zaher, MT Rodrigues, A Camacho, R Recoder, F Curccio and D Pavan. H Zaher, G Montingelli, JC Arredondo, P Bernardo and ES Freitas provided useful comments that improved this manuscript. To H Zaher for allowing the use of the facilities in Museo de Zoologia da Universidade de São Paulo. JD Daza and AM Bauer were supported by grants DEB 0844523 and DEB 1019943 from the National Science Foundation (USA) and by the Gerald M. Lemole, M.D. Endowed Chair Fund at Villanova University. Additional support for JD Daza was provided by the Department of Biological Sciences and the Office of the Dean of the College of Science at Sam Houston State University.

Authors’ Affiliations

(1)
Museu de Zoologia, Universidade de São Paulo
(2)
Biology Department, Villanova University
(3)
Department of Biological Sciences, Sam Houston State University

References

  1. Gamble T, Bauer AM, Greenbaum E, Jackman TR: Evidence for Gondwanan vicariance in an ancient clade of gecko lizards. J Biogeogr. 2008, 35: 88-104.Google Scholar
  2. Gamble T, Daza JD, Colli GR, Vitt LJ, Bauer AM: A new genus of miniaturized and pug-nosed gecko from South America (Sphaerodactylidae: Gekkota). Zool J Linn Soc. 2011, 163: 1244-1266.View ArticleGoogle Scholar
  3. Uetz P, Hošek J, Hallermann J: The reptile database. http://www.reptile-database.org,
  4. Barbour T: Sphaerodactylus. Mem Mus Comp Zool (Harvard). 1921, 47: 217-278.Google Scholar
  5. Grant C: The sphaerodactyls of Porto Rico, Culebra and Mona Islands. J Dept Agric PR. 1931, 15: 199-213.Google Scholar
  6. Grant C: A new sphaerodactyl from Porto Rico. J Dept Agric PR. 1932, 16: 31-Google Scholar
  7. Grant C: New sphaerodactyls from Cuba and the Isle of Pines. Herpetologica. 1944, 2: 118-125.Google Scholar
  8. Harris DJ, Kluge AG: The Sphaerodactylus (Sauria: Gekkonidae) of Middle America. Occas Pap Mus Zool Univ Mich. 1984, 706: 1-59.Google Scholar
  9. Thomas R, Hedges SB: Two new geckos (Sphaerodactylus) from the Sierra Martin Garcia of Hispaniola. Herpetologica. 1988, 44: 96-104.Google Scholar
  10. Avila-Pires TCS: Lizards of Brazilian Amazonia (Reptilia: Squamata). Zool Verh. 1995, 299: 1-706.Google Scholar
  11. Kluge AG: Cladistic relationships of sphaerodactyl lizards. Am Mus Novit. 1995, 3139: 1-23.Google Scholar
  12. Thomas R: A new gecko from the Virgin Islands. Q J Fla Acad Sci. 1965, 28: 117-122.Google Scholar
  13. Hedges SB, Thomas R: At the lower size limit in amniote vertebrates: a new diminutive lizard from the West Indies. Caribb J Sci. 2001, 37: 168-173.Google Scholar
  14. Raxworthy CJ, Nussbaum RA: Systematics, speciation and biogeography of the dwarf chameleons (Brookesia; Reptilia, Squamata, Chamaeleontidae) of Northern Madagascar. J Zool. 1995, 235: 525-558.View ArticleGoogle Scholar
  15. Glaw F, Köhler J, Townsend TM, Vences M: Rivaling the World’s smallest reptiles: discovery of miniaturized and microendemic new species of leaf chameleons (Brookesia) from Northern Madagascar. PLoS One. 2012, 7: e31314-View ArticleGoogle Scholar
  16. Vitt LJ, Souza RA, Sartorius SS, Avila-Pires TCS, Espósito MC: Comparative ecology of sympatric Gonatodes (Squamata: Gekkonidae) in the Western Amazon of Brazil. Copeia. 2000, 2000: 83-95.View ArticleGoogle Scholar
  17. Vitt LJ, Sartorius SS, Avila-Pires TCS, Zani PA, Espósito MC: Small in a big world: ecology of leaf-litter geckos in New World tropical forest. Herpetol Monogr. 2005, 19: 137-152.View ArticleGoogle Scholar
  18. Vanzolini PE: O gênero Coleodactylus (Sauria, Gekkonidae). Pap Avulsos Zool (São Paulo). 1957, 13: 1-17.Google Scholar
  19. Schwartz A: Sphaerodactylus. Cat Am Amph Rept. 1973, 142: 1-2.Google Scholar
  20. Brandley MC, Huelsenbeck JP, Wiens JJ: Rates and patterns in the evolution of snake-like body form in squamate reptiles: evidence for repeated re-evolution of lost digits and long-term persistence of intermediate body forms. Evolution. 2008, 62: 2042-2064.View ArticleGoogle Scholar
  21. Bolet A, Evans SE: A tiny lizard (Lepidosauria, Squamata) from the Lower Cretaceous of Spain. Palaeontology. 2012, 55: 491-500.View ArticleGoogle Scholar
  22. Underwood G: On the classification and evolution of geckos. Proc Zool Soc Lond. 1954, 124: 469-492.View ArticleGoogle Scholar
  23. Röll B: Gecko vision–retinal organization, foveae and implications for binocular vision. Vis Res. 2001, 41: 2043-2056.View ArticleGoogle Scholar
  24. Dodt E, Heck J: Retinapotentiale der zapfenfreien Netzhaut des Gecko (Sphaerodactylus muralis). Pflügers Arch Gesamte Physiol Menschen Tiere. 1954, 259: 226-230.View ArticleGoogle Scholar
  25. Nava SS, Conway MA, Martins EP: Divergence of visual motion detection in diurnal geckos that inhabit bright and dark habitats. Funct Ecol. 2009, 23: 794-799.View ArticleGoogle Scholar
  26. Schwenk K: Feeding in lepidosaurs. Feeding: Form, Function, and Evolution in Tetrapod Vertebrates. Edited by: Schwenk K. 2000, San Diego: Academic, 175-291.View ArticleGoogle Scholar
  27. Underwood G: Reptilian retinas. Nature. 1951, 167: 183-185.View ArticleGoogle Scholar
  28. Underwood G: Pupil shape in certain geckos. Copeia. 1951, 1951: 211-212.View ArticleGoogle Scholar
  29. Underwood G: Classification of geckos. Nature. 1955, 175: 1089-View ArticleGoogle Scholar
  30. Noble GK: The bony structure and phyletic relations of Sphaerodactylus and allied lacertilian genera, with the description of a new genus. Am Mus Novit. 1921, 4: 1-16.Google Scholar
  31. Parker HW: The neotropical lizards of the genera Lepidoblepharis, Pseudogonatodes, Lathrogecko, and Sphaerodactylus, with the description of a new genus. Ann Mag Nat Hist, Series 9. 1926, 17: 291-301.Google Scholar
  32. Vanzolini PE: Lagartos brasileiros da familia Gekkonidae (Sauria). Arquiv Zool (Sao Paulo). 1968, 17: 1-84.Google Scholar
  33. Vanzolini PE: Geography of the South American Gekkonidae (Sauria). Arquiv Zool (Sao Paulo). 1968, 17: 85-112.Google Scholar
  34. Maderson PFA: The structure and evolution of holocrine epidermal glands in Sphaerodactyline and Eublepharine gekkonid lizards. Copeia. 1972, 1972: 559-571.View ArticleGoogle Scholar
  35. Moffat LA: The concept of primitiveness and it’s bearing on the phylogenetic classification of the Gekkota. Proc Linn Soc New South Wales. 1973, 97: 275-301.Google Scholar
  36. Weber EG: Closure muscles of the external auditory meatus in Gekkonidae. J Herpetol. 1973, 7: 323-329.View ArticleGoogle Scholar
  37. Kluge AG: Cladistic relationship in the Gekkonoidea (Squamata, Sauria). Misc Pub Mus Zool Univ Michigan. 1987, 173: i–iv + 1–54Google Scholar
  38. Arnold EN: Relationships, evolution and biogeography of semaphore geckos, Pristurus (Squamata, Sphaerodactylidae) based on morphology. Zootaxa. 2009, 2060: 1-21.Google Scholar
  39. Daza JD, Bauer AM: A new amber-embedded sphaerodactyl gecko from Hispaniola, with comments on the morphological synapomorphies of the Sphaerodactylidae. Breviora. 2012, 529: 1-28.View ArticleGoogle Scholar
  40. Russell AP, Bauer AM: Underwood’s classification of geckos: a 21st century appreciation. Bull Nat Hist Mus Lond Zool Ser. 2002, 68: 113-121.Google Scholar
  41. Werner YL: The ontogenetic development of the vertebrae in some gekkonid lizards. J Morphol. 1971, 133: 41-92.View ArticleGoogle Scholar
  42. Brock GT: Some developmental stages in the skulls of geckoes, Lygodactylus capensis and Pachydactylus maculosa, and their bearing on certain important problems in lacertilian craniology. S Afr J Sci. 1932, 29: 508-532.Google Scholar
  43. Mahendra BC: Contributions to the bionomics, anatomy, reproduction, and development of the Indian house gecko, Hemidactylus flaviviridis Rüppel. Part I Proc Indian Acad Sci. 1936, 4: 250-281.Google Scholar
  44. Noro M, Uejima A, Abe G, Manabe M, Tamura K: Normal developmental stages of the Madagascar ground gecko Paroedura pictus with special reference to limb morphogenesis. Dev Dyn. 2009, 238: 100-109.View ArticleGoogle Scholar
  45. Wise PA, Vickaryous MK, Russell AP: An embryonic staging table for in ovo development of Eublepharis macularius, the leopard gecko. Anat Rec. 2009, 292: 1198-1212.View ArticleGoogle Scholar
  46. Ganguly DN, Mitra B: On the structure and development of the vertebral column in the house-gecko, Hemidactylus flaviviridis Rüppel. Anat Anz. 1958, 105: 4-25.Google Scholar
  47. El-Toubi MR, Kamal AM: The development of the skull of Ptyodactylus hasselquistii. I. The development of the chondrocranium. J Morphol. 1961, 108: 63-93.View ArticleGoogle Scholar
  48. El-Toubi MR, Kamal AM: The development of the skull of Ptyodactylus hasselquistii. II. The fully formed chondrocranium. J Morphol. 1961, 108: 165-191.View ArticleGoogle Scholar
  49. El-Toubi MR, Kamal AM: The development of the skull of Ptyodactylus hasselquistii. III. The osteocranium of a late embryo. J Morphol. 1961, 108: 193-202.View ArticleGoogle Scholar
  50. Rieppel O: The structure of the skull and jaw adductor musculature of the Gekkota, with comments on the phylogenetic relationships of the Xantusiidae (Reptilia: Lacertilia). Zool J Linn Soc. 1984, 82: 291-318.View ArticleGoogle Scholar
  51. Evans SE: The Skull of lizards and tuatara. Biology of the Reptilia, Volume 20, Morphology H. Edited by: Gans C, Gaunt S, Adler K. 2008, Ithaca: Society for the Study of Amphibians and Reptiles, 1-347.Google Scholar
  52. Bellairs A’A: The eyelids and spectacle in geckos. Proc Zool Soc Lond. 1948, 118: 420-425.View ArticleGoogle Scholar
  53. Adams WE, Pickersgill KW, Underwood G: The development of the carotid arch in Sphaerodactylus argus Gosse, with some remarks on “Inselbildungen” in the aortic arches. J Morphol. 1957, 101: 399-423.View ArticleGoogle Scholar
  54. Rosenberg HI, Rusell AP, Cavey MJ: Development of the subdigital adhesive pads of Ptyodactylus guttatus (Reptilia: Gekkonidae). J Morphol. 1992, 211: 243-258.View ArticleGoogle Scholar
  55. Cohn MJ, Tickle C: Developmental basis of limblessness and axial patterning in snakes. Nature. 1999, 399: 474-479.View ArticleGoogle Scholar
  56. Jackson K: The evolution of venom-conducting fangs: insights from developmental biology. Toxicon. 2007, 49: 975-981.View ArticleGoogle Scholar
  57. Vonk FJ, Admiraal JF, Jackson K, Reshef R, de Bakker MA, Vanderschoot K, van den Berge I, van Atten M, Burgerhout E, Beck A, Mirtschin PJ, Kochva E, Witte F, Fry BG, Woods AE, Richardson MK: Evolutionary origin and development of snake fangs. Nature. 2008, 454: 630-633.View ArticleGoogle Scholar
  58. Peter K: Normentafeln zur Entwicklungsgeschichte der Zauneidechse (Lacerta agilis). Normentafeln zur Entwicklungsgeschichte der Wirbeltiere. Edited by: Keibel F. 1904, Jena: Verlsg Gustav Fischer, 1-165. + 4 pls, Vol. 4Google Scholar
  59. Hamburger V, Hamilton H: A series of normal stages in the development of the chick embryo. J Morphol. 1951, 88: 49-92.View ArticleGoogle Scholar
  60. Richardson MK, Hanken J, Gooneratne ML, Pieau C, Raynaud A, Selwood L, Wright GM: There is no highly conserved embryonic stage in the vertebrates: implications for current theories of evolution and development. Anat Embryol. 1997, 196: 91-106.View ArticleGoogle Scholar
  61. Boughner JC, Buchtova M, Fu K, Diewert V, Hallgrimsson B, Richman JM: Embryonic development of Python sebae - I: staging criteria and macroscopic skeletal morphogenesis of the head and limbs. Zoology. 2007, 110: 212-230.View ArticleGoogle Scholar
  62. Leal F, Tarazona OA, Ramirez-Pinilla MP: Limb development in the gekkonid lizard Gonatodes albogularis: a reconsideration of homology in the lizard carpus and tarsus. J Morphol. 2010, 271: 1328-1341.View ArticleGoogle Scholar
  63. Sanger TJ, Losos JB, Gibson-Brown JJ: A developmental staging series for the lizard genus Anolis: a new system for the integration of evolution, development, and ecology. J Morphol. 2008, 269: 129-137.View ArticleGoogle Scholar
  64. Dufaure JP, Hubert J: Table de développement du lezard vivipare: Lacerta (Zootoca) vivipara Jacquin. Arch Anat Microsc Morphol Exp. 1961, 50: 309-328.Google Scholar
  65. Muthukkarruppan V, Kanakambika P, Manickavel V, Veeraraghavan K: Analysis of the development of the lizard, Calotes versicolor, I. A series of normal stages in the embryonic development. J Morphol. 1970, 130: 479-490.View ArticleGoogle Scholar
  66. Blanc F: Table de développement de Chamaeleo lateralis Gray, 1831. Ann Embryol Morphol. 1974, 7: 99-115.Google Scholar
  67. Dhouailly D, Saxod R: Les stades du développement de Lacerta muralis Laurent entre la ponte et l’éclosion. Bull Soc Zool France. 1974, 99: 489-494.Google Scholar
  68. Montero R, Gans C, Lions ML: Embryonic development of the skeleton of Amphisbaena darwini heterozonata (Squamata: Amphisbaenidae). J Morphol. 1999, 239: 1-25.View ArticleGoogle Scholar
  69. Roscito JG, Rodrigues MT: Embryonic development of the fossorial gymnophthalmid lizards Nothobachia ablephara and Calyptommatus sinebrachiatus. Zoology. 2012, 115: 302-318.View ArticleGoogle Scholar
  70. Maddison WP, Maddison DR: Mesquite: a modular system for evolutionary analysis. Version 2.75 2011, http://mesquiteproject.org
  71. Camp CL: Classification of the lizards. Bull Am Mus Nat Hist. 1923, 48: 289-307.Google Scholar
  72. Conrad JL: Phylogeny and systematics of Squamata (Reptilia) based on morphology. Bull Am Mus Nat Hist. 2008, 310: 1-182.View ArticleGoogle Scholar
  73. Guerra-Fuentes RA, Roscito JG, Sales Nunes PM, Oliveira-Bastos PR, Antoniazzi MM, Jared C, Rodrigues MT: Through the looking glass: the spectacle in gymnophthalmid lizards. Anat Rec. 2014, 297: 496-504.View ArticleGoogle Scholar
  74. Hubert J, Dufaure JP: Table de développement de la vipère aspic, Vipera aspis L. Bull Soc Zool France. 1968, 93: 135-148.Google Scholar
  75. Daza JD, Abdala V, Thomas R, Bauer AM: Skull anatomy of the miniaturized gecko Sphaerodactylus roosevelti (Squamata: Gekkota). J Morphol. 2008, 269: 1340-1364.Google Scholar
  76. Thomas R, Schwartz A: Sphaerodactylus (Gekkonidae) in the greater Puerto Rico region. Bull Fla State Mus. 1966, 10: 193-260.Google Scholar
  77. Moretti R: PhD thesis. Revisão Taxonômica e Biogeografia do Gênero Coleodactylus Parker, 1926 (Squamata: Sphaerodactylidae). 2009, São Paulo, Brazil: Universidade de Saô Pablo, Instituto de BiociênciasGoogle Scholar
  78. Geurgas SR, Rodrigues MT: The hidden diversity of Coleodactylus amazonicus (Sphaerodactylinae, Gekkota) revealed by molecular data. Mol Phyl Evol. 2010, 54: 583-593.View ArticleGoogle Scholar
  79. Walls GL: The vertebrate eye and its adaptive radiation. 1942, Bloomfield Hills: Cranbook Institute of ScienceView ArticleGoogle Scholar
  80. Underwood G: The Eye. Biology of the Reptilia, Volume 2, Morphology B Edited by Gans C and Parsons TS. 1970, London: Academic, 1-97.Google Scholar
  81. Romer AS: The Vertebrate Body 4th Edition. 1970, Philadelphia: WB Saunders CompanyGoogle Scholar
  82. de Queiroz K: The scleral ossicles of sceloporine iguanids: a reexamination with comments on their phylogenetic significance. Herpetologica. 1982, 38: 302-311.Google Scholar
  83. Duench K, Franz-Odendaal TA: BMP and hedgehog signaling during development of scleral ossicles. Dev Biol. 2012, 365: 251-258.View ArticleGoogle Scholar
  84. Chow RL, Lang RA: Early eye development in vertebrates. Annu Rev Cell Dev Biol. 2001, 17: 255-296.View ArticleGoogle Scholar
  85. Franz-Odendaal TA: Intramembranous ossification of scleral ossicles in Chelydra serpentina. Zoology. 2006, 109: 75-81.View ArticleGoogle Scholar
  86. Hall BK: Bones and Cartilage. Developmental and Evolutionary Skeletal Biology. 2005, London: Elsevier Academic PressGoogle Scholar
  87. Franz-Odendaal TA, Hall BK: Skeletal elements within teleost eyes and a discussion of their homology. J Morphol. 2006, 267: 1326-1337.View ArticleGoogle Scholar
  88. Werner M, Mihaela P: The phylogeny of the family Lacertidae (Reptilia) based on nuclear DNA sequences: convergent adaptations to arid habitats within the subfamily Eremiainae. Mol Phyl Evol. 2007, 44: 1155-1163.View ArticleGoogle Scholar
  89. Gamble T, Greenbaum E, Russell AP, Jackman TR, Bauer AM: Repeated origin and loss of toepads in gekkotan lizards. PLoS One. 2012, 7: e39429-View ArticleGoogle Scholar
  90. Wiens JJ, Hutter CR, Mulcahy DG, Noonan BP, Townsend TM, Sites JW, Reeder TW: Resolving the phylogeny of lizards and snakes (Squamata) with extensive sampling of genes and species. Biol Lett. 2012, 8: 1043-1046.View ArticleGoogle Scholar
  91. Pyron RA, Burbrink FT, Wiens JJ: A phylogeny and revised classification of Squamata, including 4161 species of lizards and snakes. BMC Evol Biol. 2013, 13: 93-View ArticleGoogle Scholar
  92. McDowell SBJ, Bogert CM: The systematic position of Lanthanotus and the affinities of the anguinomorphan lizards. Bull Am Mus Nat Hist. 1954, 105: 1-42.Google Scholar
  93. Daza JD, Bauer AM: The circumorbital bones of the Gekkota (Reptilia: Squamata). Anat Rec. 2010, 293: 402-413.View ArticleGoogle Scholar
  94. Daza JD, Diogo R, Johnston P, Abdala V: Jaw adductor muscles across lepidosaurs: a reappraisal. Anat Rec. 2011, 294: 1765-1782.View ArticleGoogle Scholar
  95. Stephenson NG, Stephenson EM: The osteology of the New Zealand geckos and its bearing in their morphological status. Trans Roy Soc N Z. 1956, 84: 341-358.Google Scholar
  96. Wise PAD, Russell AP: Development of the dorsal circumorbital bones in the leopard gecko (Eublepharis macularius) and its bearing on the homology of these elements in the Gekkota. Anat Rec. 2010, 293: 2001-2006.View ArticleGoogle Scholar
  97. Harkness L, Bennet-Clark HC: The deep fovea as a focus indicator. Nature. 1978, 272: 814-816.View ArticleGoogle Scholar
  98. Marmor MF, Wolfensberger TJ: The Retinal Pigment Epithelium: Function and Disease. 1998, New York: Oxford University PressGoogle Scholar
  99. Strauss O: The retinal pigment epithelium in visual function. Physiol Rev. 2005, 85: 845-881.View ArticleGoogle Scholar

Copyright

© Guerra-Fuentes et al.; licensee BioMed Central Ltd. 2014

This article is published under license to BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited.

Advertisement