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J Anat. Apr 1998; 192(Pt 3): 379–390.
PMCID: PMC1467782

Limb development and evolution: a frog embryo with no apical ectodermal ridge (AER)

Abstract

The treefrog Eleutherodactylus coqui is a direct developer — it has no tadpole stage. The limb buds develop earlier than in metamorphosing species (indirect developers, such as Xenopus laevis). Previous molecular studies suggest that at least some mechanisms of limb development in E. coqui are similar to those of other vertebrates and we wished to see how limb morphogenesis in this species compares with that in other vertebrates. We found that the hind limb buds are larger and more advanced than the forelimbs at all stages examined, thus differing from the typical amniote pattern. The limb buds were also small compared to those in the chick. Scanning and transmission electron microscopy showed that although the apical ectoderm is thickened, there was no apical ectodermal ridge (AER). In addition, the limb buds lacked the dorsoventral flattening seen in many amniotes. These findings could suggest a mechanical function for the AER in maintaining dorsoventral flattening, although not all data are consistent with this view. Removal of distal ectoderm from E. coqui hindlimb buds does not stop outgrowth, although it does produce anterior defects in the skeletal pattern. The defects are less severe when the excisions are performed earlier. These results contrast with the chick, in which AER excision leads to loss of distal structures. We suggest that an AER was present in the common ancestor of anurans and amniotes and has been lost in at least some direct developers including E. coqui.

Keywords: Eleutherodactylus , limb bud, anurans, direct development, heterochrony

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Selected References

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  • Averof M, Cohen SM. Evolutionary origin of insect wings from ancestral gills. Nature. 1997 Feb 13;385(6617):627–630. [PubMed]
  • Dollé P, Price M, Duboule D. Expression of the murine Dlx-1 homeobox gene during facial, ocular and limb development. Differentiation. 1992 Mar;49(2):93–99. [PubMed]
  • Elinson RP. Leg development in a frog without a tadpole (Eleutherodactylus coqui). J Exp Zool. 1994 Oct 1;270(2):202–210. [PubMed]
  • Fang H, Elinson RP. Patterns of distal-less gene expression and inductive interactions in the head of the direct developing frog Eleutherodactylus coqui. Dev Biol. 1996 Oct 10;179(1):160–172. [PubMed]
  • Ferrari D, Sumoy L, Gannon J, Sun H, Brown AM, Upholt WB, Kosher RA. The expression pattern of the Distal-less homeobox-containing gene Dlx-5 in the developing chick limb bud suggests its involvement in apical ectodermal ridge activity, pattern formation, and cartilage differentiation. Mech Dev. 1995 Aug;52(2-3):257–264. [PubMed]
  • Géraudie J. Scanning electron microscope study of the developing trout pelvic fin bud. Anat Rec. 1978 Jul;191(3):391–394. [PubMed]
  • Hanken J, Klymkowsky MW, Summers CH, Seufert DW, Ingebrigtsen N. Cranial ontogeny in the direct-developing frog, Eleutherodactylus coqui (Anura: Leptodactylidae), analyzed using whole-mount immunohistochemistry. J Morphol. 1992 Jan;211(1):95–118. [PubMed]
  • Klymkowsky MW, Hanken J. Whole-mount staining of Xenopus and other vertebrates. Methods Cell Biol. 1991;36:419–441. [PubMed]
  • Laufer E, Dahn R, Orozco OE, Yeo CY, Pisenti J, Henrique D, Abbott UK, Fallon JF, Tabin C. Expression of Radical fringe in limb-bud ectoderm regulates apical ectodermal ridge formation. Nature. 1997 Mar 27;386(6623):366–373. [PubMed]
  • Morasso MI, Mahon KA, Sargent TD. A Xenopus distal-less gene in transgenic mice: conserved regulation in distal limb epidermis and other sites of epithelial-mesenchymal interaction. Proc Natl Acad Sci U S A. 1995 Apr 25;92(9):3968–3972. [PMC free article] [PubMed]
  • Moury JD, Hanken J. Early cranial neural crest migration in the direct-developing frog, Eleutherodactylus coqui. Acta Anat (Basel) 1995;153(4):243–253. [PubMed]
  • Mullen LM, Bryant SV, Torok MA, Blumberg B, Gardiner DM. Nerve dependency of regeneration: the role of Distal-less and FGF signaling in amphibian limb regeneration. Development. 1996 Nov;122(11):3487–3497. [PubMed]
  • Niswander L, Tickle C, Vogel A, Booth I, Martin GR. FGF-4 replaces the apical ectodermal ridge and directs outgrowth and patterning of the limb. Cell. 1993 Nov 5;75(3):579–587. [PubMed]
  • Panganiban G, Irvine SM, Lowe C, Roehl H, Corley LS, Sherbon B, Grenier JK, Fallon JF, Kimble J, Walker M, et al. The origin and evolution of animal appendages. Proc Natl Acad Sci U S A. 1997 May 13;94(10):5162–5166. [PMC free article] [PubMed]
  • Richardson MK. Heterochrony and the phylotypic period. Dev Biol. 1995 Dec;172(2):412–421. [PubMed]
  • Richardson MK, Hanken J, Gooneratne ML, Pieau C, Raynaud A, Selwood L, Wright GM. There is no highly conserved embryonic stage in the vertebrates: implications for current theories of evolution and development. Anat Embryol (Berl) 1997 Aug;196(2):91–106. [PubMed]
  • Rodriguez-Esteban C, Schwabe JW, De La Peña J, Foys B, Eshelman B, Izpisúa Belmonte JC. Radical fringe positions the apical ectodermal ridge at the dorsoventral boundary of the vertebrate limb. Nature. 1997 Mar 27;386(6623):360–366. [PubMed]
  • Sentein P. Methods of fixing, sectioning and staining amphibian eggs for cytological study. Microsc Acta. 1976 Nov;78(5):427–438. [PubMed]
  • Shubin N, Tabin C, Carroll S. Fossils, genes and the evolution of animal limbs. Nature. 1997 Aug 14;388(6643):639–648. [PubMed]
  • Spurr AR. A low-viscosity epoxy resin embedding medium for electron microscopy. J Ultrastruct Res. 1969 Jan;26(1):31–43. [PubMed]
  • Summerbell D. A quantitative analysis of the effect of excision of the AER from the chick limb-bud. J Embryol Exp Morphol. 1974 Dec;32(3):651–660. [PubMed]
  • Tarin D, Sturdee AP. Early limb development of Xenopus laevis. J Embryol Exp Morphol. 1971 Oct;26(2):169–179. [PubMed]
  • TSCHUMI PA. The growth of the hindlimb bud of Xenopus laevis and its dependence upon the epidermis. J Anat. 1957 Apr;91(2):149–173. [PMC free article] [PubMed]
  • Vogel A, Tickle C. FGF-4 maintains polarizing activity of posterior limb bud cells in vivo and in vitro. Development. 1993 Sep;119(1):199–206. [PubMed]
  • Wanek N, Muneoka K, Holler-Dinsmore G, Burton R, Bryant SV. A staging system for mouse limb development. J Exp Zool. 1989 Jan;249(1):41–49. [PubMed]
  • Wood A. Early pectoral fin development and morphogenesis of the apical ectodermal ridge in the killifish, Aphyosemion scheeli. Anat Rec. 1982 Dec;204(4):349–356. [PubMed]

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