Abstract
The retina is a complex, multilayered tissue responsible for the perception of visual stimuli from the environment. Contrary to mammals, the capacity for postnatal eye growth in fish and amphibians, and to a lower extent in birds, is coordinated with a progenitor population residing in the ciliary marginal zone (CMZ) at the retinal peripheral margin. However, little is known about embryonic retinogenesis and postnatal retinal growth in squamates (lizards, snakes), despite their exceptional array of ecologies and ocular morphologies. Here, we address this gap by performing the first large‐scale study assessing both ontogenetic and adult changes in the stem/progenitor activity of the squamate peripheral retina. Our study reveals for the first time that squamates exhibit a source of proliferating progenitors persisting post embryogenesis in a newly identified retinociliary junction anteriorly adjacent to the retina. This region is strikingly similar to the vertebrate CMZ by its peripheral location and pseudostratified nature, and shares a common pattern of slow‐cycling cells, spatial differentiation gradient, and response to postnatal ocular growth. Additionally, its proliferative activity varies considerably among squamate species, in correlation with embryonic and postnatal differences in eye size and growth. Together our data indicate that squamates possess a proliferative peripheral retina that acts as a source of progenitors to compensate, at least in part, for postnatal ocular growth. Our findings also highlight the remarkable variation in activity and location of vertebrate retinal progenitors, indicating that the currently accepted scenario of reduced CMZ activity over the course of evolution is too simplistic.
Highlights
The eyes of vertebrates, despite possessing a similar overall appearance, structure, and physiology, differ widely in architecture and scaling, which is well related to environmental factors and life characteristics
Together our data indicate that squamates possess a proliferative peripheral retina that acts as a source of progenitors to compensate, at least in part, for postnatal ocular growth
To the ciliary marginal zone (CMZ) situation in other vertebrates (Centanin et al, 2011; Raymond, Barthel, Bernardos, & Perkowski, 2006; Wan et al, 2016; Xue & Harris, 2012), our data indicate that the squamate peripheral retina contains slowcycling cells at its extreme periphery, and accumulates proliferating progenitors expressing conserved retinal progenitor/stem and differentiation markers in a spatial order that recapitulates developmental gene expression
Summary
Squamates represent the second most diversified group of tetrapods, with more than 10,000 species, and are well known to exhibit substantial variation in eye size and postnatal growth throughout their lifespan (Hallmann & Griebeler, 2018; Shine & Charnovt, 1992) This geographically widespread group displays an exceptional array of lifestyles, ecologies, and morphological adaptations in eye and visual system related to visual performance and activity pattern (Hall, 2008, 2009; Liu et al, 2012; Werner, 1969; Werner & Seifan, 2006), strongly suggesting that interspecies and/or intraspecies variations in the peripheral retina activity might exist throughout life, as already shown for avians (Fischer & Reh, 2000; Kubota et al, 2002). This set of new results coherently and conclusively indicates that squamates possess a proliferative peripheral retina that acts as a source of progenitors to compensate, at least in part, for postnatal ocular growth
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