Developmental Heterochrony and the Evolution of Species Differences in Retinal Specializations

  • Kenneth C. Wikler
  • Barbara L. Finlay
Part of the Perspectives in Vision Research book series (PIVR)


The vertebrate retina is relatively stable across phylogeny in the classes and types of cell that compose its radial organization. Mechanistic studies of development have described how aspects of retinal organization common to all retinas emerge, such as the control of neurogenesis of particular cell types, competitive control of cell survival and dendritic organization in the development of retinal lamination, and the mechanics of directed axon outgrowth. However, vertebrate eyes also differ markedly between species in overall size, shape, and resolving power as well as in the number and arrangement of cells in the retina. Thus, studies of retinal neurogenesis must account for the development of species differences in eye conformation and retinal organization and address the evolutionary regulation of these developmental programs.


Ganglion Cell Retinal Ganglion Cell Ganglion Cell Layer Retinal Specialization Developmental Duration 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Alberch, P., and Alberch, A., 1981, Heterochronic mechanisms of morphological diversification and evolutionary change in the neotropical salamander, Bolitoglossa occidentalis (Amphibia: Plethodontidae), J. Morphol. 167:249–264.CrossRefGoogle Scholar
  2. Alberch, P., Gould, S. J., Oster, G. F., and Wake, D. B., 1979, Size and shape in ontogeny and phylogeny. Paleobiology 5:296–317.Google Scholar
  3. Ambros, V., and Horvitz, H. R., 1984, Heterochronic mutants of the nematode Caenorhabditis elegans. Science 226:409–416.PubMedCrossRefGoogle Scholar
  4. Black, I. B., 1986, Trophic molecules and the evolution of the nervous system, Proc. Natl. Acad. Sci. U.S.A. 83:8249–8252.PubMedCrossRefGoogle Scholar
  5. Bonner, J. T. (ed.), 1980, Evolution and Development, Springer-Verlag, New York.Google Scholar
  6. Bruckner, G., Mares, V., and Biesold, D., 1976, Neurogenesis in the visual system of the rat: An autoradiographic investigation, J. Comp. Neurol. 166:245–256.PubMedCrossRefGoogle Scholar
  7. Calder, W. A., 1984, Size, Function and Life History, Harvard University Press, Cambridge, MA.Google Scholar
  8. Creighton, G. K., and Strauss, R. E., 1986, Comparative patterns of growth and development in cricetine rodents and the evolution of ontogeny. Evolution 4:94–106.CrossRefGoogle Scholar
  9. Drager, U., 1985, Birthdates of cells giving rise to the crossed and uncrossed optic projections in the mouse, Proc. R. Soc. London Ser. B 224:57–77CrossRefGoogle Scholar
  10. Drager, U. C., and Olsen, J., 1981, Ganglion cell distribution in the retina of the mouse, Invest. Ophthalmol Vis. Sci. 20:285–293.PubMedGoogle Scholar
  11. Dreher, B., and Robinson, S. R., 1988, Development of the retinofugal pathway in birds and mammals: Evidence for a common "time table," Brain Behav. Evol. 31:325–392.CrossRefGoogle Scholar
  12. Dreher, B., Potts, R. A., Ni, S. Y. K., and Bennett, M. R., 1984, The development of heterogeneities in distribution and soma sizes of rat retinal ganglion cells, in Development of Visual Pathways in Mammals (J. Stone, B. Dreher, and D. Rapaport, eds.), pp. 39–57, Alan R. Liss, New York.Google Scholar
  13. Dreher, B., Sefton, A. J., Ni, S. Y. K., and Nisbett, G., 1985, The morphology, number, distribution and central projections of Class I retinal ganglion cells in albino and hooded rats, Brain Behav. Evol. 26:10–48.PubMedCrossRefGoogle Scholar
  14. Eisenberg, J. F., 1981, The Mammalian Radiations: An Analysis of Trends in Evolution, Adaptation and Behavior, The University of Chicago Press, Chicago.Google Scholar
  15. Emerson, V. F., 1980, Grating acuity of the golden hamster: Effects of stimulus orientation and luminance, Exp. Brain Res. 38:43–52.PubMedCrossRefGoogle Scholar
  16. Finlay, B. L., Wikler, K. C., and Sengelaub, D. R., 1987, Regressive events in brain development and scenarios for vertebrate brain evolution. Brain Behav. Evol. 519:102–117.CrossRefGoogle Scholar
  17. Goodwin, B. C., Holder, N., and Wylie, C. C. (eds.), 1983, Development and Evolution, Cambridge University Press, Cambridge.Google Scholar
  18. Gould, S. J., 1977, Ontogeny and Phylogeny, Harvard University Press, Cambridge, MA.Google Scholar
  19. Greiner, J. V., 1981, Histogenesis of the ferret retina, Exp. Eye Res. 33:315–332.PubMedCrossRefGoogle Scholar
  20. Greiner, J. V., and Weidman, T. A., 1980, Histogenesis of the cat retina, Exp. Eye Res. 30:439–453.PubMedCrossRefGoogle Scholar
  21. Hallet, P. E., 1987, The scale of the visual pathways of mouse and rat, Biol. Cybern. 57:275–286.CrossRefGoogle Scholar
  22. Henderson, Z., 1985, Distribution of ganglion cells in the retina of adult pigmented ferret. Brain Res. 358:221–228.PubMedCrossRefGoogle Scholar
  23. Henderson, Z., Finlay, B. L., and Wikler, K. C., 1988, Development of ganglion cell topography in ferret retina, J. Neurosci. 8:1194–1205.PubMedGoogle Scholar
  24. Horsburgh, G. H., and Sefton, A. J., 1987, Cellular degeneration and synaptogenesis in the developing retina of the rat, J. Comp. Neurol. 263:553–556.PubMedCrossRefGoogle Scholar
  25. Hughes, A., 1977, The topography of vision in mammals of contrasting lifestyle: Comparative optics and rednal organization, in Handbook of Sensory Physiology, Vol. VII, 5th ed. (F. Crescitelli, ed.), pp. 613–756, Springer-Verlag, Berlin.Google Scholar
  26. Ingle, D. J., 1981, New methods for analysis of vision in gerbils, Behav. Brain Res. 3:151–175.PubMedCrossRefGoogle Scholar
  27. Jerison, H. J., 1973, Evolution of the Brain and Intelligence, Academic Press, New York.Google Scholar
  28. Kelling, S. T., Sengelaub, D. R., Wikler, K. C., and Finlay, B. L., 1989, Differential Elasticity of the Immature Retina: a Contribution to the Development of the Area Centralis? Vis Neurosci 2, in Press.Google Scholar
  29. Lia, B., Williams, R. W., and Chalupa, L. M., 1987, Non-uniform growth of the fetal retina can account for the prenatal development of regional specialization in the ganglion cell layer of the cat. Science 236:848–851.PubMedCrossRefGoogle Scholar
  30. Mann, M. D., Glickman, S. E., and Towe, A. L., 1988, Brain/body relationships among myomorph rodents. Brain Behav. Evol. 31:111–124.PubMedCrossRefGoogle Scholar
  31. Mastronarde, D. M., Thibeault, M. A., and Dubin, M. W., 1984, Non-uniform postnatal growth of the cat retina, J. Comp. Neurol. 288:598–608.CrossRefGoogle Scholar
  32. Morest, D. K., 1970, The pattern of neurogenesis in the retina of the rat, Z. Anat. Entwicklungsgesch. 131:45–67.PubMedCrossRefGoogle Scholar
  33. Perry, V. H., Henderson, Z., and Linden, R., 1983, Postnatal changes in retinal ganglion cell and optic axon populations in the pigmented rat, J. Comp. Neurol. 219:356–368.PubMedCrossRefGoogle Scholar
  34. Provis, J. M., 1987, Patterns of cell death in the ganglion cell layer of the human fetal retina, J. Comp. Neurol. 259:237–246.PubMedCrossRefGoogle Scholar
  35. Provis, J. M., van Driel, D., Billson, F. A., and Russell, P. 1985a, Development of the human retina: Patterns of cell distribution and redistribution in the ganglion cell layer, J. Comp. Neurol. 233:429–452.PubMedCrossRefGoogle Scholar
  36. Provis, J. M., van Driel, D., Billson, F. A., and Russell, P., 1985b, Human fetal optic nerve: Overproducdon and eliminadon of retinal axons during development, J. Comp. Neurol 238:92–100.PubMedCrossRefGoogle Scholar
  37. Raff, R. A., and Kaufman, T. C., 1983, Embryos, Genes, and Evolution, Macmillan, New York.Google Scholar
  38. Rapaport, D. H., and Stone, J., 1982, The site of commencement of maturation in mammalian redna: Observations in the cat. Dev. Brain Res. 5:273–279.CrossRefGoogle Scholar
  39. Remtulla, S., and Hallet, P. E., 1985, A schematic eye for the mouse and comparisons with the rat. Vision Res. 25:21–31.PubMedCrossRefGoogle Scholar
  40. Robinson, S. R., 1987, Ontogeny of the area centralis in the cat, J. Comp. Neurol. 254:50–71.CrossRefGoogle Scholar
  41. Robinson, S. R., Dreher, B., Horsburgh, G. M., and McCall, M. J., 1986, Development of ganglion cell density in the rabbit, Soc. Neurosci. Abstr. 12:985.Google Scholar
  42. Sacher, G. A., 1982, The role of brain maturation in the evolution of the primates, inPrimate Brain Evolution: Methods and Concepts (E. A. Armstrong and D. Falk, eds.), Plenum Press, New York.Google Scholar
  43. Sengelaub, D. R., and Finlay, B. L., 1982, Cell death in the mammalian visual system during normal development: 1. Retinal ganglion cells, J. Comp. Neurol 204:311–317.PubMedCrossRefGoogle Scholar
  44. Sengelaub, D. R., Dolan, R. P., and Finlay, B. L., 1986, Cell generation, death, and retinal growth in the development of the hamster retinal ganglion cell layer, J. Comp. Neurol. 246:527–543.PubMedCrossRefGoogle Scholar
  45. Sidman, R. L., 1961, Histogenesis of mouse retina studied with thymidine-3H, in Structure of the Eye (G. K. Smelser, ed.), pp. 487–506, Academic Press, New York.Google Scholar
  46. Stone, J., 1965, A quantitative analysis of the distribution of ganglion cells in the cat’s retina, J. Comp. Neurol. 124:337–352.PubMedCrossRefGoogle Scholar
  47. Stone, J., 1978, The number and distribution of ganglion cells in the cat’s retina, J. Comp. Neurol. 180:753–772.PubMedCrossRefGoogle Scholar
  48. Stone, J., 1983, Parallel Processing in the Visual System, pp. 265–325, Plenum Press, New York.Google Scholar
  49. Stone, J., Rapaport, D. H., Williams, R. W., and Chalupa, L., 1982, Uniformity of cell distribution in the ganglion cell layer of prenatal cat retina: Implications for mechanisms of retinal development, Dev. Brain Res. 2:231–242.CrossRefGoogle Scholar
  50. Stone, J., Egan, M., and Rapaport, D. H. 1985, The site of commencement of retinal maturation in the rabbit. Vision Res. 25:309–317.PubMedCrossRefGoogle Scholar
  51. Wall, G. L., 1942, The Vertebrate Eye and Its Adaptive Radiation, Hafner, New York.CrossRefGoogle Scholar
  52. Webster, M., 1985, Cytogenesis, histogenesis and morphological differentiation of the retina, Ph.D. dissertation. University of New South Wales, N.S.W. Australia.Google Scholar
  53. Wikler, K. C., 1987, Developmental heterochrony and the development of species differences in retinal specializations, Ph.D. dissertation, Cornell University, New York.Google Scholar
  54. Wikler, K. C., Perez, G., and Finlay, B. L., 1988, Neurogenesis in the gerbil retina: a comparative analysis of the effects of developmental duration or retinal conformation, unpublished manuscript.Google Scholar
  55. Wong, R. O. L., and Hughes, A., 1987, Role of cell death in the topogenesis of neuronal distributions in the developing cat retinal ganglion cell layer, J. Comp. Neurol. 262:496–511.PubMedCrossRefGoogle Scholar

Copyright information

© Plenum Press, New York 1989

Authors and Affiliations

  • Kenneth C. Wikler
    • 1
  • Barbara L. Finlay
    • 2
  1. 1.Section of Neuroanatomy, School of MedicineYale UniversityNew HavenUSA
  2. 2.Department of PsychologyCornell UniversityIthacaUSA

Personalised recommendations