Skip to main content
Log in

Ontogeny of the photoreceptors in the embryonic retina of the viviparous guppy, Poecilia reticulata P. (Teleostei)

An electron-microscopical study

  • Published:
Cell and Tissue Research Aims and scope Submit manuscript

Summary

Ultrastructural analyses of retinal development in the guppy embryo show that at midgestation all types of photoreceptors are differntiated in the fundus, and at birth differentiation extends over the whole retina. Formation of discs of outer segments is more rapid in rods than in cones. Double cones differentiate simultaneously with long single cones and are formed by the adhesion of two primordial inner segments; short single cones develop last. Wherever cones are differentiated, they are arranged in an adult-type square mosaic. The rods in the embryo, as opposed to the adult, are likewise regularly arranged within the mosaic unit.

These results are at variance with the generally held opinion that adult teleosts which possess duplex retinae have larvae with pure cone retinae, and that rods, double cones and mosaics appear in late larval life or only at metamorphosis.

In the double cones of the guppy embryo subsurface cisternae develop along the adjoining primordial inner segments. Additionally, regularly distributed subsurface cisternae are formed in the regions of intimate contact of long single cones with double cones and rods.

We suggest that the early development of rods and double cones, and a square-mosaic with regular distribution of rods and subsurface cisternae, provide the newly born with a fully functional optical apparatus, especially suited to perception of movements. This is necessary for its survival against predatory, especially maternal, attacks.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Ahlbert JB (1973) Ontogeny of double cones in the retina of perch fry (Perca fluviatilis. L., Teleostei). Acta Zool 54:241–254

    Google Scholar 

  • Ahlbert JB (1976) Organisation of the cone cells in the retinae of salmon (Salmo salar) and trout (Salmo trutta trutta) in relation to their feeding habits. Acta Zool 57:13–35

    Google Scholar 

  • Ali MA (1959) The ocular structure, retinomotor and photobehavioural responses of juvenile Pacific salmon. Can J Zool 37:965–996

    Google Scholar 

  • Baburina EA (1961) Development of eyes and their function in the embryos and larvae of Lucioperca lucioperca. Trudy Inst Norf Zhivot 33:151–172

    Google Scholar 

  • Bathelt D (1970) Experimentelle und vergleichend morphologische Untersuchungen am visuellen System von Teleostiern. Zool Jb Anat 87:402–470

    Google Scholar 

  • Berger ER (1967) Subsurface membranes in paired cone photoreceptor inner segments of adult and neonatal Lebistes retinae. J Ultrastruct Res 17:220–232

    Google Scholar 

  • Blaxter JHS (1968) Visual thresholds and spectral sensitivity of herring larvae. J Exp Biol 48:39–53

    Google Scholar 

  • Blaxter JHS (1975) The eyes of larval fish. In: Ali MA (ed) Vision in fishes. Plenum Press, New York, pp 427–450

    Google Scholar 

  • Blaxter JHS, Jones MP (1967) The development of the retina and retinomotor responses in the herring. J Mar Biol Ass UK 47:677–697

    Google Scholar 

  • Boehlert GW (1978) Intraspecific evidence on the function of single and double cones in the teleost retina. Science 202:309–311

    Google Scholar 

  • Borwein B (1981) The retinal receptor: Adescription. In: Enoch JM, Tobey FL (eds) Vertebrate photoreceptor Optics. Springer, Berlin Heidelberg New York pp 19, 23, 47

    Google Scholar 

  • Callaghan E, Kunz Y (1980) Ellipsosomes, organelles of mitochondrial origin in retinal cones of certain fish. Proc Roy Microsc Soc 15: Suppl 5; 15

    Google Scholar 

  • Coulombre AJ (1965) The eye. In: De Haan RL, Ursprung H (eds) Organogenesis. Holt, Rinehart, Winston New York, pp 219–251

    Google Scholar 

  • Fisher SK, Goldman K (1975) Subsurface cisterns in the vertebrate retina. Cell Tissue Res 164:473–480

    Google Scholar 

  • Fürst CM (1904) Zur Kenntnis der Histogenese und des Wachstums der Retina. Acta Univ Lund 40:1–45

    Google Scholar 

  • Grün G (1975) Structural basis of the functional development of the retina in the cichlid Tilapia leucosticta (Teleostei). J Embryol Exp Morphol 33:243–257

    Google Scholar 

  • Johns PR, Fernald RD (1981) Genesis of rods in teleost fish retina. Nature 293:141–142

    Google Scholar 

  • Kuenzer P, Wagner HJ (1969) Bau und Anordnung der Sehzellen und Horizontalen in der Retina von Nannacara anomala (Cichlidae, Teleostei). Z Morph Tiere 65:209–224

    Google Scholar 

  • Kunz Y (1963) Die embryonale Harnblase von Lebistes reticulatus (guppy). Rev Suisse Zool 70:291–297

    Google Scholar 

  • Kunz YW (1964) Morphologische Studien über die embryonale und postembryonale Entwicklung bei Teleostiern mit besonderer Berücksichtigung des Dottersystems und der Leber. Rev Suisse Zool 71:445–525

    Google Scholar 

  • Kunz YW (1971a) Histological study of greatly enlarged pericardial sac in the embryo of the viviparous teleost Lebistes reticulatus. Rev Suisse Zool 78:187–207

    Google Scholar 

  • Kunz YW (1971b) Distribution of lactate dehydrogenase (and its E-isozymes) in the developing and adult retina of the guppy (Lebistes reticulatus). Rev Suisse Zool 78:761–776

    Google Scholar 

  • Kunz YW (1980) Cone mosaics in a teleost retina: Changes during light and dark adaptation. Experientia 36:1371–1374

    Google Scholar 

  • Kunz YW, Wise C (1974) Development of the photoreceptors in the embryonic retina of Lebistes reticulatus (Peters). Electron-microscopical investigations. Rev Suisse Zool 81:697–701

    Google Scholar 

  • Kunz YW, Wise C (1977) Structure and ultrastructure of the argentea and sciera of the eye of Poecilia reticulata. Zoomorphologie 87:203–215

    Google Scholar 

  • Kunz YW, Wise C (1978) The development of photoreceptors in the embryo of Poecilia reticulata. Abstr. VIIIth Intern Congr ISDB, Tokyo

  • Le Beaux YJ (1972) Subsurface cisterns and lamellar bodies: particular forms of the endoplasmic reticulum in neurons. Z Zellforsch 133:327–352

    Google Scholar 

  • Lyall AH (1957a) The growth of the trout retina. Q J Microsc Sc 98:101–110

    Google Scholar 

  • Lyall AH (1957b) Cone arrangements in teleost retina. Q J Microsc Sc 98:189–201

    Google Scholar 

  • MacNichol EF, Kunz YW, Levine JS, Harosi FI, Collins BA (1978) Ellipsosomes: organelles containing a cytochrome-like pigment in the retinal cones of certain fishes. Science 200:549–551

    Google Scholar 

  • Müller H (1952) Bau und Wachstum der Netzhaut des Guppy (Lebistes reticulatus). Zool Jb Abt Allg Zool Physiol 63:275–324

    Google Scholar 

  • Rosenbluth J (1962) Subsurface cisterns and their relationship to the neuronal plasma membrane. J Cell Biol 13:405–421

    Google Scholar 

  • Sandy JF, Blaxter JHS (1980) A study of retinal development in larval herring and sole. J Mar biol Assoc UK 60:59–71

    Google Scholar 

  • Scholes JH (1976) Neuronal connections and cellular arrangement in the fish retina. In: Zettler F, Weiler R (eds) Neuronal principles in vision. Springer, Berlin Heidelberg New York, pp 63–93

    Google Scholar 

  • Shaklee JB, Whitt GS (1981) Lactate dehydrogenase isozymes of gadiform fishes: Divergent patterns of gene expression indicate a heterogeneous taxon. Copeia 3:(3) 563–578

    Google Scholar 

  • Yacob A, Wise C, Kunz YW (1977) The accessory outer segment of rods and cones in the retina of the guppy, Poecilia reticulata P (Teleostei). Cell Tissue Res 177:181–193

    Google Scholar 

  • Yamada E, Ishikawa T (1965) Some observations on the submicroscopic morphogenesis of the human retina. In: Rohen JW (ed) Eye structure, II. Symp. Schattauer, Stuttgart, pp 5–16

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Additional information

This work was in part subsidized by a grant from the Medical Research Council of Ireland to Y.W.K.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kunz, Y.W., Ennis, S. & Wise, C. Ontogeny of the photoreceptors in the embryonic retina of the viviparous guppy, Poecilia reticulata P. (Teleostei). Cell Tissue Res. 230, 469–486 (1983). https://doi.org/10.1007/BF00216193

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00216193

Key words

Navigation