Ocular elongation and retraction in foveated reptiles

Abstract

Background: Pronounced asymmetric changes in ocular globe size during eye development have been observed in a number of species ranging from humans to lizards. In contrast, largely symmetric changes in globe size have been described for other species like rodents. We propose that asymmetric changes in the three-dimensional structure of the developing eye correlate with the types of retinal remodeling needed to produce areas of high photoreceptor density. To test this idea, we systematically examined three-dimensional aspects of globe size as a function of eye development in the bifoveated brown anole, Anolis sagrei.Results: During embryonic development, the anole eye undergoes dynamic changes in ocular shape. Initially spherical, the eye elongates in the presumptive foveal regions of the retina and then proceeds through a period of retraction that returns the eye to its spherical shape. During this period of retraction, pit formation and photoreceptor cell packing are observed. We found a similar pattern of elongation and retraction associated with the single fovea of the veiled chameleon, Chamaeleo calyptratus.Conclusions: These results, together with those reported for other foveated species, support the idea that areas of high photoreceptor packing occur in regions where the ocular globe asymmetrically elongates and retracts during development.

Maturation and Refinement of the Maculae and Foveae in the Anolis sagrei lizard

“…Eyes were processed using PBS, ethanol, and Xylene solutions along with paraffin waxes as previously reported (Rasys, Pau, Irwin, Luo, Kim, Wahle, Trainor, et al, 2021). Eyes were then serial sectioned in paraffin wax on the horizontal plane along the dorsal-ventral axis.…”

“…Outside of primates and birds, the only other foveated vertebrate to have the development of its eye studied is the brown anole lizard ( Anolis sagrei ) (Rasys, Pau, Irwin, Luo, Kim, Wahle, Trainor, et al, 2021; Rasys, Pau, Irwin, Luo, Kim, Wahle, Menke, et al, 2021; Rasys, Pau, Irwin, Luo, Menke, et al, 2021). This species relies on sight as its principal sense and requires a high degree of visual acuity for hunting its prey and communicating and socially interacting with others of its kind (Fleishman et al, 1995; Fleishman & Pallus, 2010).…”

“…This species relies on sight as its principal sense and requires a high degree of visual acuity for hunting its prey and communicating and socially interacting with others of its kind (Fleishman et al, 1995; Fleishman & Pallus, 2010). The brown anole retina is adapted for high-acuity diurnal vision and develops two distinct foveae in each eye during embryogenesis, one located in the center of the retina and one oriented in the temporal region (Fleishman, 1992; Makaretz & Levine, 1980; Rasys, Pau, Irwin, Luo, Kim, Wahle, Trainor, et al, 2021; Rasys, Pau, Irwin, Luo, Kim, Wahle, Menke, et al, 2021). The central fovea is deep and convexiclivate in morphology while the temporal fovea is shallower and more variable in shape and retinal location across different anole species (Fite & Lister, 1981; Fite & Rosenfield-Wessels, 1975).…”

“…However, the temporal foveal region retains these layers during the formation of the pit. Photoreceptor cell packing in the foveal areas also occurs during this period, and by the time of hatching, the anole can hunt (Rasys, Pau, Irwin, Luo, Kim, Wahle, Trainor, et al, 2021; Rasys, Pau, Irwin, Luo, Kim, Wahle, Menke, et al, 2021). Although this might suggest a high degree of visual acuity, it is unclear whether photoreceptor numbers in the foveal region continue to increase during post-hatchling periods as the eye continues to expand.…”

Generation of Lens Progenitor Cells and Lentoid Bodies from Pluripotent Stem Cells: Novel Tools for Human Lens Development and Ocular Disease Etiology

“…The human eye contains a unique anatomical structure called the macula and its central portion, the fovea, rich in cone photoreceptors [ 72 , 73 ]. The morphogenetic processes underlying cone-dominant foveal development can be only partially inferred from other model organisms (e.g., 13-line ground squirrels, chameleons, and other reptiles) [ 74 , 75 , 76 ]. The human eye can accommodate lenses to both near-sight focus and over a distance of several hundreds of meters.…”