Development of the retina is altered in the directly developing frog Eleutherodactylus coqui (Leptodactylidae) (original) (raw)
Related papers
Frontiers in Zoology, 2008
Background: Frogs primitively have a biphasic life history with an aquatic larva (tadpole) and a usually terrestrial adult. However, direct developing frogs of the genus Eleutherodactylus have lost a free living larval stage. Many larval structures never form during development of Eleutherodactylus, while limbs, spinal cord, and an adult-like cranial musculoskeletal system develop precociously. Results: Here, I compare growth and differentiation of the retina and tectum and development of early axon tracts in the brain between Eleutherodactylus coqui and the biphasically developing frogs Discoglossus pictus, Physalaemus pustulosus, and Xenopus laevis using morphometry, immunohistochemical detection of proliferating cell nuclear antigen (PCNA) and acetylated tubulin, biocytin tracing, and in situ hybridization for NeuroD. Findings of the present study indicate that retinotectal development was greatly altered during evolution of Eleutherodactlyus mostly due to acceleration of cell proliferation and growth in retina and tectum. However, differentiation of retina, tectum, and fiber tracts in the embryonic brain proceed along a conserved slower schedule and remain temporally coordinated with each other in E. coqui. Conclusion: These findings reveal a mosaic pattern of changes in the development of the central nervous system (CNS) during evolution of the direct developing genus Eleutherodactylus. Whereas differentiation events in directly interconnected parts of the CNS such as retina, tectum, and brain tracts remained coordinated presumably due to their interdependent development, they were dissociated from proliferation control and from differentiation events in other parts of the CNS such as the spinal cord. This suggests that mosaic evolutionary changes reflect the modular character of CNS development.
Journal of Morphology, 1992
Direct development in amphibians is an evolutionarily derived life-history mode that involves the loss of the free-living, aquatic larval stage. We examined embryos of the direct-developing anuran Eleutherodactylus coqui (Leptodactylidae) to evaluate how the biphasic pattern of cranial ontogeny of metamorphosing species has been modified in the evolution of direct development in this lineage. We employed whole-mount immunohistochemistry using a monoclonal antibody against the extracellular matrix component Type I1 collagen, which allows visualization of the morphology of cartilages earlier and more effectively than traditional histological procedures; these latter procedures were also used where appropriate. This represents the first time that initial chondrogenic stages of cranial development of any vertebrate have been depicted in whole-mounts.
Development, 1985
In adult Limnodynastes dorsalis and Heleioporus eyrei regions of high cell density in the retinal ganglion cell layer are normally found along the nasotemporal axis and become apparent only after metamorphosis (Dunlop & Beazley, 1981; Coleman, Dunlop & Beazley, 1984). Eye rotations were performed from embryonic to mid-larval life and cell topography mapped after metamorphosis using cresyl violet-stained wholemounts. Mature cell distributions indicated that from stages equivalent to 30/31 in Xenopus (Nieuwkoop & Faber, 1956) alignment of high cell density regions had already been determined and developed to reflect the degree of eye rotation. We conclude that cell topography in the adult ganglion cell layer is determined from the time at which invagination of the eye cup nears completion. Furthermore, the corre-spondence in adults between alignment of high cell density regions and the orientation of the visuotectal projection suggests that these features could not be dissociated by m...
Journal of …, 2012
Here we present a detailed study of the major events in the retinal histogenesis in a slow-developing elasmobranch species, the small-spotted catshark, during embryonic, postnatal and adult stages using classical histological and immunohistological methods, providing a complete neurochemical characterization of retinal cells. We found that the retina of the small-spotted catshark was fully differentiated prior to birth. The major developmental events in retinal cell differentiation occurred during the second third of the embryonic period. Maturational features described in the present study were first detected in the central retina and, as development progressed, they spread to the rest of the retina following a central-to-peripheral gradient. While the formation of both plexiform layers occurs simultaneously in the retina of the most common fish models, in the small-spotted catshark retina the emergence of the outer plexiform layer was delayed with respect to the inner plexiform layer. According to the expression of the markers used, retinal cell differentiation followed a vitreal-to-scleral gradient, with the exception of Mü ller cells that were the last cell type generated during retinogenesis. This vitreal-to-scleral progression of neural differentiation seems to be specific to slow-developing fish species.
Journal of comparative neurology, 2019
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.
Evolution & Development, 2010
Genetic and developmental alterations associated with the evolution of amphibian direct development remain largely unexplored. Specifically, little is known of the underlying expression of skeletal regulatory genes, which may reveal early modifications to cranial ontogeny in direct-developing species. We describe expression patterns of three key skeletal regulators (runx2, sox9, and bmp4) along with the cartilage-dominant collagen 2a1 gene (col2a1) during cranial development in the directdeveloping anuran, Eleutherodactylus coqui. Expression patterns of these regulators reveal transient skeletogenic anlagen that correspond to larval cartilages, but which never fully form in E. coqui. Suprarostral anlagen in the frontonasal processes are detected through runx2, sox9, and bmp4 expression. Previous studies have described these cartilages as missing from Eleutherodactylus cranial ontogeny. These transcriptionally active suprarostral anlagen fuse to the more posterior cranial trabeculae before they are detectable with col2a1 staining or with the staining techniques used in earlier studies. Additionally, expression of sox9 fails to reveal an early anterior connection between the palatoquadrate and the neurocranium, which is detectable through sox9 staining in Xenopus laevis embryos (a metamorphosing species). Absence of this connection validates an instance of developmental repatterning, where the larval quadratocranial commissure cartilage is lost in E. coqui. Expression of runx2 reveals dermal-bone precursors several developmental stages before their detection with alizarin red. This early expression of runx2 correlates with the accelerated embryonic onset of bone formation characteristic of E. coqui and other direct-developing anurans, but which differs from the postembryonic bone formation of most metamorphosing species. Together these results provide an earlier depiction of cranial patterning in E. coqui by using earlier markers of skeletogenic cell differentiation. These data both validate and modify previously reported instances of larval recapitulation and developmental repatterning associated with the evolution of anuran direct development.
Developmental changes and novelties in ceratophryid frogs
EvoDevo, 2016
The Neotropical frog genera Ceratophrys, Chacophrys and Lepidobatrachus form the monophyletic family Ceratophryidae. Although in- and out-group relationships are not fully resolved, the monophyly of the three genera is well supported by both morphological and molecular data. Much is known about the morphology of the ceratophryids, but there is little comparative information on how modification of a common ancestral developmental pathway played a role in shaping their particular body plans. Herein, we review morphological variation during ceratophryid ontogeny in order to explore the role of development in their evolution. The ceratophryids are collectively characterized by rapid larval development with respect to other anurans, yet the three genera differ in their postmetamorphic growth rates to sexual maturity. Derived traits in the group can be divided into many homoplastic features that evolved in parallel with those of anurans with fossorial/burrowing behaviors in semiarid envir...
Vision Research, 1980
In the frog, as in many other vertebrates, the eye and, consequently the retina, continues to increase in size throughout life. In this paper ganglion cell densities in the retina of a Brasilian tree frog, Hyla raniceps, have been measured from methylene blue stained whole mounts. From a series of retinae, taken from individuals with body sizes ranging from that of a post-metamorphic juvenile to sexually mature adult, isodensity maps of cell density across the whole retina have been prepared. Concomitant measurement of the extent of the visual field of these animals allowed cell counts per mm2 to be converted to cells per unit visual angle. Changes in both cell density and distribution were observed with increasing body size and in central retina these changes resulted in an increasing number of cells representing each degree of visual field. In contrast, in the inferior and superior periphery the angular separation of ganglion cells remained approximately constant. The developmental, physiological and ecological significance of these findings is discussed.