New developmental evidence supports a homeotic frameshift of digit identity in the evolution of the bird wing

Frontiers in Zoology

Volumn 11, Issue 1, 2014, Pages

  Salinas Saavedra, Miguel ^a   Gonzalez Cabrera, Cristian ^a   Ossa Fuentes, Luis ^a   Botelho, Joao F ^a   Ruiz Flores, Macarena ^a   Vargas, Alexander O ^a  

^a UNIVERSITY OF CHILE   (Chile)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84899476625     PISSN: None     EISSN: 17429994     Source Type: Journal    
DOI: 10.1186/1742-9994-11-33     Document Type: Article

References (50)

1. Holmgren N. Studies on the phylogeny of birds. Acta Zool 1955, 36:243-328.
2. Hinchliffe JR. " One, two, three" or " two, three, four" : an embryologist's view of the homologies of the digits and carpus of modern birds. Beginnings of birds 1985, 141-147. Eichstätt: Freunde des Jura-Museum, Hecht M, Ostrom JH, Viohl G, Wellnhofer P.
3. Burke C, Feduccia A. Developmental patterns and the identification of homologies in the Avian Hand. Science 1997, 278:666-668.
4. Gauthier JA. Saurischian monophyly and the origin of birds. Mem Calif Acad Sci 1986, 8:1-55.
5. Wagner GP, Gauthier JA. 1, 2, 3 = 2, 3, 4: a solution to the problem of the homology of the digits in the avian hand. Proc Natl Acad Sci U S A 1999, 96:5111-5116. 10.1073/pnas.96.9.5111, 21825, 10220427.
6. Rauhut OWM. The interrelationships and evolution of basal theropod dinosaurs. Spec Pap Palaeontol 2003, 69:1-213.
7. Carrano MT, Benson RBJ, Sampson SD. The phylogeny of Tetanurae (Dinosauria: Theropoda). J Syst Palaeontol 2012, 10:211-300.
8. Galis F, Kundrát M, Sinervo B. An old controversy solved: bird embryos have five fingers. Trends Ecol Evol 2003, 18:7-9.
9. Galis F, Kundrát M, Metz JAJ. Hox genes, digit identities and the theropod/ bird transition. J Exp Zool B Mol Dev Evol 2005, 304:198-205.
10. Xu X, Clark JM, Mo J, Choiniere J, Forster CA, Erickson GM, Hone DWE, Sullivan C, Eberth DA, Nesbitt S, Zhao Q, Hernandez R, Jia C, Han F, Guo Y. A Jurassic ceratosaur from China helps clarify avian digit homologies. Nature 2009, 459:940-944. 10.1038/nature08124, 19536256.
11. Seki R, Kamiyama N, Tadokoro A, Nomura N, Tsuihiji T, Manabe M, Tamura K. Evolutionary and Developmental Aspects of Avian-Specific Traits in Limb Skeletal Pattern. Zool Sci 2012, 29:631-644. 10.2108/zsj.29.631, 23030336.
12. Vargas A, Wagner G, Gauthier J. Limusaurus and bird digit identity. Nat Prec 2009, http://precedings.nature.com/documents/3828/version/1.
13. Xu X, Mackem S. Tracing the evolution of Avian Wing Digits. Curr Biol 2013, 23:538-544.
14. Vargas AO, Fallon JF. Birds have dinosaur wings: The molecular evidence. J Exp Zool B Mol Dev Evol 2005, 304:86-90.
15. Vargas AO, Kohlsdorf T, Fallon JF, Van den Brooks J, Wagner GP. The evolution of HoxD11 expression in the bird wing: insights from alligator mississippiensis. PLoS One 2008, 3:e3325. 10.1371/journal.pone.0003325, 2553264, 18833328.
16. Wang Z, Young RL, Xue H, Wagner GP. Transcriptomic analysis of avian digits reveals conserved and derived digit identities in birds. Nature 2011, 477:583-586. 10.1038/nature10391, 21892187.
17. Woltering JM, Duboule D. The origin of digits: expression patterns versus regulatory mechanisms. Dev Cell 2010, 18:526-532. 10.1016/j.devcel.2010.04.002, 20412768.
18. Capek D, Metscher BD, Müller GB. Thumbs down: a molecular-morphogenetic approach to avian digit homology. J Exp Zool B Mol Dev Evol 2014, 322:1-12. 10.1002/jez.b.22545, 24323741.
19. Tamura K, Nomura N, Seki R, Yonei-Tamura S, Yokoyama H. Embryological evidence identifies wing digits in birds as digits 1, 2, and 3. Science 2011, 331:753-757. 10.1126/science.1198229, 21311019.
20. Riddle RD, Johnson RL, Laufer E, Tabin CJ. Sonic hedgehog mediates the polarizing activity of the ZPA. Cell 1993, 75:1401-1416. 10.1016/0092-8674(93)90626-2, 8269518.
21. Drossopoulou G, Lewis KE, Sanz-Ezquerro JJ, Nikbakht N, McMahon AP, Hofmann C, Tickle C. A model for anteroposterior patterning of the vertebrate limb based on sequential long- and short-range Shh signalling and Bmp signalling. Development 2000, 127:1337-1348.
22. Yang Y, Drossopoulou G, Chuang PT, Duprez D, Marti E, Bumcrot D, Vargesson N, Clarke J, Niswander L, McMahon A, Tickle C. Relationship between dose, distance and time in Sonic-Hedgehog-mediated regulation of anteroposterior polarity in the chick limb bud. Development 1997, 124:4393-4404. 23.
23. Harfe BD, Scherz PJ, Nissim S, Tian H, McMahon AP, Tabin CJ. Evidence for an expansion-based temporal Shh gradient in specifying vertebrate digit identities. Cell 2004, 118:517-528. 10.1016/j.cell.2004.07.024, 15315763.
24. Towers M, Signolet J, Sherman A, Sang H, Tickle C. Insights into bird wing evolution and digit specification from polarizing region fate maps. Nat Commun 2011, 2:426.
25. Vargas AO, Wagner GP. Frame-shifts of digit identity in bird evolution and cyclopamine-treated wings. Evol Dev 2009, 11:163-169. 10.1111/j.1525-142X.2009.00317.x, 19245548.
26. Chatterjee S. Counting the fingers of birds and dinosaurs. Science 1998, 280:355a.
27. Chen JK, Taipale J, Cooper MK, Beachy PA. Inhibition of Hedgehog signalling by direct binding of cyclopamine to Smoothened. Genes Dev 2002, 16:2734-2748.
28. Scherz PJ, McGlinn E, Nissim S, Tabin CJ. Extended exposure to sonic hedgehog is required for patterning the posterior digits of the vertebrate limb. Dev Biol 2007, 308:343-354. 10.1016/j.ydbio.2007.05.030, 2100419, 17610861.
29. Dahn RD, Fallon JF. Interdigital regulation of digit identity and homeotic transformation by modulated BMP signaling. Science 2000, 289:438-441. 10.1126/science.289.5478.438, 10903202.
30. Suzuki T, Hasso SM, Fallon JF. Unique SMAD1/5/8 activity at the phalanx -forming region determines digit identity. Proc Natl Acad Sci U S A 2008, 105:4185-4190. 10.1073/pnas.0707899105, 2393776, 18334652.
31. Sears KA, Bormet AK, Rockwell A, Powers LE, Cooper LN, Wheeler MB. Developmental basis of mammalian digit reduction: a case study in pigs. Evol Dev 2011, 13:533-541. 10.1111/j.1525-142X.2011.00509.x, 23016937.
32. Holmgren N. An embryological analysis of the mammalian carpus and its bearing upon the question of the origin of the tetrapod limb. Acta Zool 1952, 33:1-115.
33. Hamrick MW. Developmental mechanisms of digit reduction. Evol Dev 2002, 4:247-248. 10.1046/j.1525-142X.2002.02012.x, 12168616.
34. Vargesson N, Clarke JD, Vincent K, Coles C, Wolpert L, Tickle C. Cell fate in the chick limb bud and relationship to gene expression. Development 1997, 124:1909-1918.
35. Towers M, Mahood R, Yin Y, Tickle C. Integration of growth and specification in chick wing digit-patterning. Nature 2008, 452:882-886. 10.1038/nature06718, 18354396.
36. Di-Poï N, Montoya-Burgos JI, Miller H, Pourquié O, Milinkovitch MC, Duboule D. Changes in Hox genes structure and function during the evolution of the squamate body plan. Nature 2010, 464:99-103. 10.1038/nature08789, 20203609.
37. Young RL, Caputo V, Giovannotti M, Kohlsdorf T, Vargas AO, May GE, Wagner GP. Evolution of digit identity in the three-toed Italian skink Chalcides chalcides: a new case of digit identity frame shift. Evol Dev 2009, 11:647-658. 10.1111/j.1525-142X.2009.00372.x, 19878286.
38. Cohn MJ, Lovejoy CO, Wolpert L, Coates MI. Branching, segmentation and the metapterygial axis: pattern versus process in the vertebrate limb. Bioessays 2002, 24:460-465. 10.1002/bies.10088, 12001269.
39. Sheth R, Marcon L, Bastida MF, Junco M, Quintana L, Dahn R, Kmita M, Sharpe J, Ros MA. Hox genes regulate digit patterning by controlling the wavelength of a turing-type mechanism. Science 2012, 338:1478-1480.
40. Thulborn RA. Theropod dinosaurs, progenesis and birds: homology of digits in the manus. Neues Jb Geol Paläontol Abh 2006, 242:205-241.
41. Fernández-Terán MA, Hinchliffe JR, Ros MA. Birth and death of cells in limb development: a mapping study. Dev Dyn 2006, 235:2521-2537. 10.1002/dvdy.20916, 16881063.
42. Wake D, Wake MH, Specht C. Homoplasy: From Detecting Pattern to Determining Process and Mechanism of Evolution. Science 2011, 331:1032-1035. 10.1126/science.1188545, 21350170.
43. Davidson EH. Emerging properties of animal gene regulatory networks. Nature 2010, 468:911-920. 10.1038/nature09645, 3967874, 21164479.
44. Montavon T, Garrec JFL, Kerzberg M, Duboule D. Modelling HOX genes regulation in digits: reverse collinearity and the molecular origin of thumbness. Genes Dev 2008, 22:236-259.
45. Tarchini B, Duboule D. Control of HoxD collinearity during early limb development. Dev Cell 2006, 10:93-103. 10.1016/j.devcel.2005.11.014, 16399081.
46. Acloque H, Wilkinson DG, Nieto MA. In situ hybridization analysis of chick embryos in whole-Mount and tissue sections. Methods Cell Biol 2008, 87:169-185.
47. Hamburger V, Hamilton HL. A series of normal stages in the development of the chick embryo. Dev Dyn 1992, 195:231-272. 10.1002/aja.1001950404, 1304821.
48. Li S, Muneoka K. Cell migration and chick limb development: chemotactic action of FGF-4 and the AER. Dev Biol 1999, 211:335-347. 10.1006/dbio.1999.9317, 10395792.
49. Sato K, Koizumi Y, Takahashi M, Kuroiwa A, Tamura K. Specification of cell fate along the proximal-distal axis in the developing chick limb bud. Development 2007, 134:1397-1406. 10.1242/dev.02822, 17329359.
50. Hama H, Kurokawa H, Kawano H, Ando R, Shimogori T, Noda H, Fukami K, Sakaue-Sawano A, Miyawaki A. Scale: a chemical approach for fluorescence imaging and reconstruction of transparent mouse brain. Nat Neurosci 2011, 14:1481-1488. 10.1038/nn.2928, 21878933.