Evolution of digit identity in the three-toed Italian skink Chalcides chalcides: A new case of digit identity frame shift

Evolution and Development

Volumn 11, Issue 6, 2009, Pages 647-658

  Young, Rebecca L ^a   Caputo, Vincenzo ^b   Giovannotti, Massimo ^b   Kohlsdorf, Tiana ^a,c   Vargas, Alexander O ^a,d   May, Gemma E ^a   Wagner, Günter P ^a  

^a YALE UNIVERSITY   (United States)

^b UNIVERSITÀ POLITECNICA DELLE MARCHE   (Italy)

^c UNIVERSITY OF SÃO PAULO   (Brazil)

^d UNIVERSITY OF CHILE   (Chile)

Author keywords

[No Author keywords available]

Indexed keywords

HOMEODOMAIN PROTEIN;

ANATOMY; EMBRYONIC DEVELOPMENT; EVOLUTIONARY BIOLOGY; GENE EXPRESSION; HYPOTHESIS TESTING; LIZARD; NINETEENTH CENTURY; PHYLOGENETICS;

AMINO ACID SEQUENCE; ANIMAL; ARTICLE; BIOLOGICAL MODEL; BONE DEVELOPMENT; FEMALE; GENE EXPRESSION REGULATION; GENETICS; HISTOLOGY; IN SITU HYBRIDIZATION; LIMB; LIZARD; METABOLISM; MOLECULAR CLONING; MOLECULAR EVOLUTION; MOLECULAR GENETICS; PHYLOGENY; PHYSIOLOGY; SEQUENCE HOMOLOGY;

AMINO ACID SEQUENCE; ANIMALS; BONE DEVELOPMENT; CLONING, MOLECULAR; EVOLUTION, MOLECULAR; EXTREMITIES; FEMALE; GENE EXPRESSION REGULATION; HOMEODOMAIN PROTEINS; IN SITU HYBRIDIZATION; LIZARDS; MODELS, GENETIC; MOLECULAR SEQUENCE DATA; PHYLOGENY; SEQUENCE HOMOLOGY, AMINO ACID;

AVES; CHALCIDES CHALCIDES;

EID: 70350503373     PISSN: 1520541X     EISSN: 1525142X     Source Type: Journal    
DOI: 10.1111/j.1525-142X.2009.00372.x     Document Type: Article

References (69)

1. Brandley, M. C., Huelsenbeck, J. P. Wiens, J. J. 2008. Rates and patterns in the evolution of snake-like body form in squamate reptiles: evidence for repeated re-evolution of lost digits and long-term persistence for intermediate body forms. Evolution 62 : 2042 2064.
2. Bruno, S. Maugeri, S. 1976. Rettili d'Italia: Tartarughe e Sauri. I. A. Martello, Firenze.
3. Burke, A. C. Alberch, P. 1985. The development and homology of the chelonian carpus and tarsus. J. Morphol. 186 : 119 131.
4. Burke, A. C. Feduccia, A. 1997. Developmental patterns and the identification of homologies in the avian hand. Science 278 : 666 668.
5. Caldwell, M. W. 2003. "Without a leg to stand on": on the evolution and development of axial elongation and limblessness in tetrapods. Can. J. Earth Sci. 40 : 573 599.
6. Caputo, V. 1993. Taxonomy and evolution of the Chalcides chalcides complex (Reptilia, Scincidae) with description of two new species. Bol. Mus. Reg. Sci. Nat., Torino 11 : 47 120.
7. Caputo, V. 2004. The cranial osteology and dentition in the scinicid lizards of the genus Chalcides (Reptilia, Scincidae). Ital. J. Zool. 71 (suppl. 2) : 35 45.
8. Caputo, V., Guarino, F. M. Angelini, F. 2000. Body elongation and placentome evolution in the genus Chalcides Laurenti, 1768. Ital. J. Zool. 67 : 385 391.
9. Caputo, V., Lanza, B. Palmieri, R. 1995. Body elongation and limb reduction in the genus Chalcides Laurenti, 1768 (Squamata: Scincidae). Trop. Zool. 8 : 95 152.
10. Carranza, S., Arnold, E. N., Geniez, P., Roca, J. Mateo, J. A. 2008. Radiation, multiple dispersal, and parallelism in the skinks, Chalcides and Sphenops (Squamata: Scincidea), with comments on Scincus and Scinopus and the age of the Sahara Desert. Mol. Phylogenet. Evol. 46 : 1071 1094.
11. Chatterjee, S. 1998. Counting the fingers of birds and dinosaurs. Science 280 : 355.
12. Chiang, C., et al. 2001. Manifestation of the limb prepattern: limb development in the absence of Sonic Hedgehog function. Dev. Biol. 236 : 421 435.
13. Dahn, R. Fallon, J. F. 2000. Interdigital regulation of digit identify and homeotic transformation by modulated BMP signaling. Science 289 : 438 441.
14. Deschamps, J. 2007. Ancestral and recently recruited global control of the Hox genes in development. Curr. Opin. Genet. Dev. 17 : 422 427.
15. Drossopoulou, K., et al. 2000. A model of anterioposterior patterning of the vertebrate limb based on sequential long- and short range Shh and Bmp signaling. Development 127 : 1337 1348.
16. Feduccia, A. Nowicki, J. 2002. The hand of birds revealed by early ostrich embryos. Naturwissenschaften 89 : 391 393.
17. Ferguson, M. W. J. 1985. Reproductive biology and embryology of the crocodilians. In C. Gans, F. Billet P. F. A. Maderson (eds.). Biology of the Reptilia. John Wiley and Sons, New York, pp. 329 491.
18. Filler, A. G. 2007. Homeotic evolution in the mammalia: diversification of Therian axial seriation and the morphogenetic basis of human origins. PLoS One 2 : e1019.
19. Fürbringer, M. 1870. Die Knocken und Muskeln der Extremitäten bei den shlangernähnlichen Sauriern: Vergleichend Anatomische Abhandlung. Verlag von Wilhelm Engelmann, Leipzig.
20. Galis, F., Kundrát, M. Sinervo, B. 2003. An old controversy solved: bird embryos have five fingers. Trends Ecol. Evol. 18 : 7 9.
21. Garner, J. P. Thomas, A. L. R. 1998. Counting the fingers of birds. Science 280 : 355.
22. Greer, A. E. 1990. Limb reduction in the scincid lizard genus Lerista. 2. Variation in the bone complements of the front and rear limbs and the number of postsacral vertebrae. J. Herpetol. 24 : 142 150.
23. Greer, A. E. 1991. Limb reduction in squamates: identification of the lineages and discussion of the trends. J. Herpetol. 25 : 166 173.
24. Greer, A. E., Caputo, V., Lanza, B. Palmieri, R. 1998. Observation on limb reduction in the scincid lizard genus Chalcides. J. Herpetol. 32 : 244 252.
25. Hall, B. K. 1994. Homology and embryonic development. In M. K. Hecht, R. J. MacIntyre M. T. Clegg (eds.). Evoluitonary Biology. Plenum Press, New York, pp. 1 30.
26. Hanken, J. Wasserug, R. J. 1981. The visible skeleton. Funct. Photography 16 : 22 26.
27. Hinchliffe, J. R. Hecht, M. K. 1984. Homology of the bird wing skeleton: embryological versus palaeontological evidence. Evol. Biol. 30 : 21 39.
28. Kundrat, M., Seichert, V., Russell, A. P. Smetana, K. 2002. Pentadactyl pattern of the avian wing autopodium and pyramid reduction hypothesis. J. Exp. Zool. 294 : 152 159.
29. Lande, R. 1978. Evolutionary mechanisms of limb loss in tetrapods. Evolution 32 : 73 92.
30. Larsson, H. C. E. Wagner, G. P. 2002. Pentadactyl ground state of the avian wing. J. Exp. Zool. 294 : 146 151.
31. McLeod, M. J. 1980. Differential staining of cartilage and bone in whole mouse fetuses by alcian blue and alizarin red S. Teratology 22 : 299 301.
32. Montavon, T., Le Garrec, J.-F., Kerszberg, M. Duboule, D. 2008. Modeling Hox gene regulation in digits: reverse collinearity and the molecular origin of thumbness. Genes Dev. 22 : 346 359.
33. Morgan, B. A., Izpisua-Belmonte, J. C., Duboule, D. Tabin, C. J. 1992. Targeted misexpression of Hox-4.6 in the avian limb bud causes apparent homeotic transformations. Nature 358 : 236 239.
34. Morse, E. S. 1872. On the tarsus and carpus of birds. Ann. Lyceum Nat. Hist. New York 10 : 141 158.
35. Müller, G. B. Alberch, P. 1990. Ontogeny of the limb skeleton in Alligator mississippiensis - developmental invariance and change in the evolution of archosaur limbs. J. Morphol. 203 : 151 164.
36. Nelson, C., et al. 1996. Analysis of Hox gene expression in the chick limb bud. Development 122 : 1449 1466.
37. Nieto, M. A., Patel, K. Wilkinson, D. G. 1996. In situ analysis of chick embryos in whole mount and tissue sections. In M. Bronner-Fraser (ed.). Methods in Cell Biology. Academic Press, New York, pp. 219 235.
38. Orsini, J.-P. Cheylan, M. 1981. Chalcides chalcides (Linnaeus 1758)-Erzschleiche. In W. Böhme (ed.). Handbuch der Reptien und Amphibien Europas. Akademische Verlagsgesellschaft, Wiesbaden, pp. 318 337.
39. Panman, L., et al. 2006. Differential regulation of gene expression in the digit forming area of the mouse limb bud by SHH and gremlin 1/FGF-mediated epithelial-mesenchymal signalling. Development 133 : 3419 3428.
40. Pasteur, G. 1981. A survey of the species of Old World scincid genus Chalcides. J. Herpetol. 15 : 1 16.
41. Raynaud, A., Clerque-Gazeau, M., Bons, J. Brabet, J. 1987. Nouvelles observations, fondées sur les caractères du métatarsien latéral et sur la structure du tarse, relatives à la formule digitale du Seps tridactyle (Chalcides chalcides, L.). Bull. Soc. Hist. Nat. Toulouse 123 : 127 132.
42. Raynaud, A., Clerque-Gazeau, M. Brabet, J. 1986. Remarques préliminaires sur la structure de la patte du Seps Tridactyle (Chalcides chalcides, L.). Bull. Soc. Hist. Nat. Toulouse 122 : 109 111.
43. Raynaud, A., Perret, J.-L. Clerque-Gazeau, M. 1989. Modalités de réduction digitale chez quelque Scincidés africains (Reptiles). Rev. Suisse Zool. 96 : 779 802.
44. Renous-Lecuru, S. 1973. Morphologie comparee du carge chez les Lepidosauriens actuels (Rhynchocephales, Lacertilens, Amphisbeniens). Gegenbaurs Morphol. Jahrbuch 119 : 727 766.
45. Rewcastle, S. C. 1983. Fundamental adaptations in the lacertilian hind limb: a partial analysis of the sprawling limb posture and gait. Copeia 1983 : 476 487.
46. Rieppel, O. 1992. Studies on skeleton formation in reptiles III: patterns of ossification in the skeleton of Lacerta vivipara (Reptilia, Squamata). Fieldiana Zool. New Series 68 : 1 25.
47. Sereno, P. C. 1999. The evolution of dinosaurs. Science 284 : 2137 2147.
48. Sewertzoff, A. N. 1931. Studien über die Reduktion der Organe der Wirbeltiere. Zool. Jahrb. Abt. Anat. Ontog. Tiere Jena 53 : 611 699.
49. Shapiro, M. D. 2002. Developmental morphology of limb reduction in hemiergis (squamata: scincidae): chondrogenesis, osteogenesis, and heterochrony. J. Morphol. 254 : 211 231.
50. Shapiro, M. D., Shubin, N. H. Downs, J. P. 2007. Limb reduction and diversity in reptilian evolution. In B. K. Hall (ed.). Fins and Limbs: Evolution, Development, and Transformation. University of Chicago Press, Chicago, pp. 225 244.
51. Shubin, N. H. 1994a. History, ontogeny, and evolution of the archetype. In B. K. Hall (ed.). Homology the hierachical basis of comparative biology. Academic Press, San Diego, CA, pp. 249 271.
52. Shubin, N. H. 1994b. The phylogeny of development and the origin of homology. In L. Grande O. Rieppel (ed.). Interpreting the Hierarchy of Nature. Academic Press, San Diego, CA, pp. 210 225.
53. Shubin, N. H. Alberch, P. 1986. A morphogenetic approach to the origin and basic organization of the tetrapod limb. Evol. Biol. 20 : 319 387.
54. Spitz, F., Herkenne, C., Morris, M. A. Duboule, D. 2005. Inversion-induced disruption of the Hoxd cluster leads to the partition of regulatory landscapes. Nature Genet. 37 : 889 893.
55. Steiner, H. Anders, G. 1946. Zur Frage der Entstehung von Rudimenten. Die Redukction der Gliedmassen von Chalcides tridactylus Laur. Rev. Suisse de Zool. 53 : 537 546.
56. *and other methods). Version 4. Sinauer Associates, Sunderland, MA.
57. Tarchini, B. Duboule, D. 2006. Control of Hoxd genes' collinearity during early limb development. Cell 10 : 93 103.
58. Vargas, A. O. Fallon, J. F. 2005a. Birds have dinosaur wings: the molecular evidence. J. Exp. Zool. Part B - Mol. Dev. Evol. 304B : 86 90.
59. Vargas, A. O. Fallon, J. F. 2005b. The digits of the wing of birds are 1, 2, and 3. A review. J. Exp. Zool. Part B - Mol. Dev. Evol. 304B : 206 219.
60. Vargas, A. O., Kohlsdorf, T., Fallon, J. F., VandenBrooks, J. Wagner, G. P. 2008. The evolution of Hoxd11 expression in the bird wing: insights from Alligator mississippiensis. PLoS One 3 : e3325.
61. Vargas, A. O. Wagner, G. P. 2009. Frame-shifts of digit identity in bird evolution and cyclopamine-treated wings. Evol. Dev. 11 : 163 169.
62. Wagner, G. P. 2005. The developmental evolution of avian digit homology: an update. Theory Biosci. 124 : 165 183.
63. Wagner, G. P. 2007. The developmental genetics of homology. Nat. Rev. Genet. 8 : 473 479.
64. Wagner, G. P. Gauthier, J. A. 1999. 1,2,3=2,3,4: a solution to the problem of the homology of the digits in the avian hand. Proc. Nat Acad. Sci. USA 96 : 5111 5116.
65. Welten, M. C. M., Verbeek, F. J., Meijer, A. H. Richardson, M. K. 2005. Gene expression and digit homology in the chicken embryo wing. Evol. Dev. 7 : 18 28.
66. Wiens, J. J., Brandley, M. C. Reeder, T. W. 2006. Why does a trait evolve multiple times within a clade? Repeated evolution of snakelike body form in squamate reptiles. Evolution 60 : 123 141.
67. Wilkins, A. S. 2002. The Evolution of Developmental Pathways. Sinauer Associates Inc., Sunderland, MA.
68. Zákány, J., Fromental-Ramain, C., Warot, X. Duboule, D. 1997. Regulation of number and size of digits by posterior Hox genes: a dose-dependent mechanism with potential evolutionary implications. Proc. Nat. Acad. Sci. 94 : 13695 13700.
69. Zákány, J., Kmita, M. Duboule, D. 2004. A Dual role for Hox genes in limb anterior-posterior asymmetry. Science 304 : 1669 1672.