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Eye development in the Cape dune mole rat

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Abstract

Studies on mammalian species with naturally reduced eyes can provide valuable insights into the evolutionary developmental mechanisms underlying the reduction of the eye structures. Because few naturally microphthalmic animals have been studied and eye reduction must have evolved independently in many of the modern groups, novel evolutionary developmental models for eye research have to be sought. Here, we present a first report on embryonic eye development in the Cape dune mole rat, Bathyergus suillus. The eyes of these animals contain all the internal structures characteristic of the normal eye but exhibit abnormalities in the anterior chamber structures. The lens is small but develops normally and exhibits a normal expression of α- and γ-crystallins. One of the interesting features of these animals is an extremely enlarged and highly pigmented ciliary body. In order to understand the molecular basis of this unusual feature, the expression pattern of an early marker of the ciliary zone, Ptmb4, was investigated in this animal. Surprisingly, in situ hybridization results revealed that Ptmb4 expression was absent from the ciliary body zone of the developing Bathyergus eye.

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References

  • Avivi A, Joel A, Nevo E (2001) The lens protein alpha-B-crystallin of the blind subterranean mole-rat: high homology with sighted mammals. Gene 264:45–49

    Article  CAS  PubMed  Google Scholar 

  • Beebe DC (1986) Development of the ciliary body: a brief review. Trans Ophthalmol Soc U K 105(Pt 2):123–130

    PubMed  Google Scholar 

  • Bennett NC, Faulkes CG (2000) African mole-rats: ecology and eusociality

  • Breitman ML, Bryce DM, Giddens E, Clapoff S, Goring D, Tsui LC, Klintworth GK, Bernstein A (1989) Analysis of lens cell fate and eye morphogenesis in transgenic mice ablated for cells of the lens lineage. Development 106:457–463

    CAS  PubMed  Google Scholar 

  • Carmona FD, Jimenez R, Collinson JM (2008) The molecular basis of defective lens development in the Iberian mole. BMC Biol 6:44

    Article  PubMed Central  PubMed  Google Scholar 

  • Cernuda-Cernuda R, Garcia-Fernandez JM, Gordijn MC, Bovee-Geurts PH, DeGrip WJ (2003) The eye of the African mole-rat Cryptomys anselli: to see or not to see? Eur J Neurosci 17:709–720

    Article  PubMed  Google Scholar 

  • Chow RL, Lang RA (2001) Early eye development in vertebrates. Annu Rev Cell Dev Biol 17:255–296

    Article  CAS  PubMed  Google Scholar 

  • Cooper HM, Herbin M, Nevo E (1993) Visual system of a naturally microphthalmic mammal: the blind mole rat, Spalax ehrenbergi. J Comp Neurol 328:313–350

    Article  CAS  PubMed  Google Scholar 

  • Coulombre AJ, Coulombre JL (1957) The role of intraocular pressure in the development of the chick eye: III. Ciliary body. Am J Ophthalmol 44:85–93

    CAS  PubMed  Google Scholar 

  • Crish SD, Dengler-Crish CM, Catania KC (2006) Central visual system of the naked mole-rat (Heterocephalus glaber). Anat Rec A: Discov Mol Cell Evol Biol 288:205–212

    Article  Google Scholar 

  • Etchevers HC, Vincent C, Le Douarin NM, Couly GF (2001) The cephalic neural crest provides pericytes and smooth muscle cells to all blood vessels of the face and forebrain. Development 128:1059–1068

    CAS  PubMed  Google Scholar 

  • Fuhrmann S (2010) Eye morphogenesis and patterning of the optic vesicle. Curr Top Dev Biol 93:61–84

    Article  PubMed Central  PubMed  Google Scholar 

  • Genis-Galvez JM (1966) Role of the lens in the morphogenesis of the iris and cornea. Nature 210:209–210

    Article  CAS  PubMed  Google Scholar 

  • Graw J (2010) Eye development. Curr Top Dev Biol 90:343–386

    Article  PubMed  Google Scholar 

  • Harrington L, Klintworth GK, Secor TE, Breitman ML (1991) Developmental analysis of ocular morphogenesis in alpha A-crystallin/diphtheria toxin transgenic mice undergoing ablation of the lens. Dev Biol 148:508–516

    Article  CAS  PubMed  Google Scholar 

  • Hough RB, Avivi A, Davis J, Joel A, Nevo E, Piatigorsky J (2002) Adaptive evolution of small heat shock protein/alpha B-crystallin promoter activity of the blind subterranean mole rat, Spalax ehrenbergi. Proc Natl Acad Sci U S A 99:8145–8150

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Jeffery WR (2001) Cavefish as a model system in evolutionary developmental biology. Dev Biol 231:1–12

    Article  CAS  PubMed  Google Scholar 

  • Klein KL, Klintworth GK, Bernstein A, Breitman ML (1992) Embryology and morphology of microphthalmia in transgenic mice expressing a gamma F-crystallin/diphtheria toxin A hybrid gene. Lab Invest 67:31–41

    CAS  PubMed  Google Scholar 

  • Kott O, Sumbera R, Nemec P (2010) Light perception in two strictly subterranean rodents: life in the dark or blue? PLoS One 5:e11810

    Article  PubMed Central  PubMed  Google Scholar 

  • Napier HR, Kidson SH (2005) Proliferation and cell shape changes during ciliary body morphogenesis in the mouse. Dev Dyn 233:213–223

    Article  CAS  PubMed  Google Scholar 

  • Nemec P, Burda H, Peichl L (2004) Subcortical visual system of the African mole-rat Cryptomys anselli: to see or not to see? Eur J Neurosci 20:757–768

    Article  PubMed  Google Scholar 

  • Nemec P, Cvekova P, Benada O, Wielkopolska E, Olkowicz S, Turlejski K, Burda H, Bennett NC, Peichl L (2008) The visual system in subterranean African mole-rats (Rodentia, Bathyergidae): retina, subcortical visual nuclei and primary visual cortex. Brain Res Bull 75:356–364

    Article  PubMed  Google Scholar 

  • Nemec P, Cvekova P, Burda H, Benada O, Peichl L (2007) Visual systems and the role of vision in subterranean rodents: diversity of retinal properties and visual system designs. In: Begall S, Burda H, Schleich CE (eds) Subterranean rodents: news from underground. Springer, Heidelberg, pp 129–160

    Chapter  Google Scholar 

  • Nevo E (1979) Adaptive convergence and divergence of subterranean mammals. Ann Rev Ecol Syst 10:269–308

    Article  Google Scholar 

  • Nevo E (1999) Mosaic evolution of subterranean mammals: regression, progression and global convergence. Oxford Uniuversity Press, Oxford

    Google Scholar 

  • Nikitina NV, Maughan-Brown B, O'Riain MJ, Kidson SH (2004) Postnatal development of the eye in the naked mole rat (Heterocephalus glaber). Anat Rec A: Discov Mol Cell Evol Biol 277:317–337

    Article  Google Scholar 

  • Pei YF, Rhodin JA (1970) The prenatal development of the mouse eye. Anat Rec 168:105–125

    Article  CAS  PubMed  Google Scholar 

  • Peichl L, Nemec P, Burda H (2004) Unusual cone and rod properties in subterranean African mole-rats (Rodentia, Bathyergidae). Eur J Neurosci 19:1545–1558

    Article  PubMed  Google Scholar 

  • Quilliam TA (1966) The problem of vision in the ecology of Talpa europaea. Exp Eye Res 5:63–78

    Article  CAS  PubMed  Google Scholar 

  • Sanyal S, Jansen HG, de Grip WJ, Nevo E, de Jong WW (1990) The eye of the blind mole rat, Spalax ehrenbergi. Rudiment with hidden function? Invest Ophthalmol Vis Sci 31:1398–1404

    CAS  PubMed  Google Scholar 

  • Sinn R, Wittbrodt J (2013) An eye on eye development. Mech Dev 130:347–358

    Article  CAS  PubMed  Google Scholar 

  • Stroeva OG (1967) The correlation of the processes of proliferation and determination in the morphogenesis of iris and ciliary body in rats. J Embryol Exp Morphol 18:269–287

    CAS  PubMed  Google Scholar 

  • Theiler K (1989) The house mouse: atlas of embryonic development

  • Thut CJ, Rountree RB, Hwa M, Kingsley DM (2001) A large-scale in situ screen provides molecular evidence for the induction of eye anterior segment structures by the developing lens. Dev Biol 231:63–76

    Article  CAS  PubMed  Google Scholar 

  • Wegner RE, Begall S, Burda H (2006) Light perception in "blind" subterranean Zambian mole-rats. Anim Behav 72:1021–1024

    Article  Google Scholar 

  • Yamamoto Y, Jeffery WR (2000) Central role for the lens in cave fish eye degeneration. Science 289:631–633

    Article  CAS  PubMed  Google Scholar 

  • Yamamoto Y, Stock DW, Jeffery WR (2004) Hedgehog signalling controls eye degeneration in blind cavefish. Nature 431:844–847

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We are thankful to our grant sponsors: the South African Medical Research Council (MRC) and the University of Cape Town. We are very grateful to Prof Hisato Kondoh (Osaka University, Japan) and Dr Linlin Ding (Joseph Horwitz Laboratory, Jules Stein Eye Institute, University of California) for their generous gifts of anti-crystallin antibodies.

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Authors and Affiliations

  1. Department of Human Biology, Faculty of Health Sciences, University of Cape Town, Observatory, 7925, Cape Town, South Africa

    Natalya V. Nikitina & Susan H. Kidson

  2. School of Molecular and Cell Biology, University of the Witwatersrand, Private Bag 3, Wits, 2050, Johannesburg, South Africa

    Natalya V. Nikitina

Authors
  1. Natalya V. Nikitina
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  2. Susan H. Kidson
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Correspondence to Natalya V. Nikitina.

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Communicated by Andreas Kispert

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Nikitina, N.V., Kidson, S.H. Eye development in the Cape dune mole rat. Dev Genes Evol 224, 107–117 (2014). https://doi.org/10.1007/s00427-014-0468-x

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  • DOI: https://doi.org/10.1007/s00427-014-0468-x

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