Development and retinal remodeling in the brown anole lizard (Anolis sagrei)

Abstract

Background. The fovea, a pit in the retina, is believed to be important for high-acuity vision and is a feature found in the eyes of humans and a limited number of vertebrate species that include certain primates, birds, lizards, and fish. At present, model systems currently used for ocular research lack a foveated retina and studies investigating fovea development have largely been limited to histological and molecular studies in primates. As a result, progress towards understanding the mechanisms involved in regulating fovea development in humans is limited and is completely lacking in other, non-primate, vertebrates. To address this knowledge gap, we provide here a detailed histological atlas of retina and fovea development in the bifoveated Anolis sagrei lizard, a novel reptile model for fovea research. We also further test the hypothesis that retinal remodeling, which leads to fovea formation and photoreceptor cell packing, is related to asymmetric changes in eye shape. Results. Anole retina development follows the conventional spatiotemporal patterning observed in most vertebrates, where retina neurogenesis begins within the central retina, progresses throughout the temporal retina, and concludes in the nasal retina. One exception to this general rule is that areas that give rise to the fovea undergo retina differentiation prior to the rest of the retina. We find that retina thickness changes dynamically during periods of ocular elongation and retraction. During periods of ocular elongation, the retina thins, while during retraction it becomes thicker. Ganglion cell layer mounding is also observed in the temporal fovea region just prior to pit formation. Conclusions. Anole retina development parallels that of humans, including the onset and progression of retinal neurogenesis followed by changes in ocular shape and retinal remodeling that leads to pit formation in the retina. We propose that anoles are an excellent model system for fovea development research.

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

“…A drop in cellularity from hatchling to adulthood raises the question of whether cell death is occurring within the retina. Studies in embryonic rodents, chicks, turtles and anoles have shown that a significant portion of cell death occurs in retina cell layers during development, but that cell death slows and largely ceases shortly after birth or hatching (Beazley et al, 1987; Cook et al, 1998; Francisco-Morcillo et al, 2004; Rasys, Pau, Irwin, Luo, Kim, Wahle, Trainor, et al, 2021; Rasys, Pau, Irwin, Luo, Kim, Wahle, Menke, et al, 2021). Although we did not specifically look for markers of cell death in retinal sections, we did not observe any evidence of pyknotic cells within our sections across the age groups, suggesting that if cell death is occurring, it is likely minimal.…”

“…Foveal areas undergo periods of localized elongation followed by retraction. During ocular retraction, pit formation and the majority of photoreceptor packing occurs (Rasys, Pau, Irwin, Luo, Kim, Wahle, Trainor, et al, 2021; Rasys, Pau, Irwin, Luo, Kim, Wahle, Menke, et al, 2021). It is possible that ocular retraction, particularly along the z-axis, may persist for a brief period after hatching and during ocular expansion.…”

“…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.…”