Metapodial or phalanx? An evolutionary and developmental perspective on the homology of the first ray's proximal segment

Journal of Experimental Zoology Part B: Molecular and Developmental Evolution

Volumn 320, Issue 5, 2013, Pages 276-285

  Reno, Philip L ^a   Horton, Walter E ^b,c   Lovejoy, C Owen ^c  

^a PENNSYLVANIA STATE UNIVERSITY   (United States)

^b Northeast Ohio Medical University   (United States)

^c KENT STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL; BONE DEVELOPMENT; EPIPHYSIS; EVOLUTION; FINGER PHALANX; GROWTH PLATE; HISTOLOGY; NOTE; PHYLOGENY;

ANIMALS; BIOLOGICAL EVOLUTION; EPIPHYSES; FINGER PHALANGES; GROWTH PLATE; OSTEOGENESIS; PHYLOGENY;

MAMMALIA; TETRAPODA; THERIA;

EID: 84879064213     PISSN: 15525007     EISSN: 15525015     Source Type: Journal    
DOI: 10.1002/jez.b.22506     Document Type: Note

References (83)

1. Allin EF. 1975. Evolution of the mammalian middle ear. J Morphol 147:403-437.
2. Boulet AM, Capecchi MR. 2002. Duplication of the Hoxd11 gene causes alterations in the axial and appendicular skeleton of the mouse. Dev Biol 249:96-107.
3. Broom R. 1906. On the arrangement of the epiphyses of the mammalian metacarpals and metatarsals. Anatomischer Amzeiger 28:106-112.
4. Buchholtz EA, Stepien CC. 2009. Anatomical transformation in mammals: Developmental origin of aberrant cervical anatomy in tree sloths. Evol Dev 11:69-79.
5. Burstein AH, Wright TM. 1994. Fundamentals of orthopaedic biomechanics. Baltimore: Williams & Wilkins.
6. Carroll RL. 1988. Vertebrate paleontology and evolution. New York: W.H. Freeman and Company.
7. Carroll SB. 2008. Evo-devo and an expanding evolutionary synthesis: A genetic theory of morphological evolution. Cell 134:25-36.
8. Cubo J. 2000. Process heterochonies in endochondral ossification. J Theor Biol 205:343-353.
9. de Bruffrénil V, Ineich I, Böhme W. 2005. Comparative data on epiphyseal development in the family Varanidae. J Herpetol 37:238-335.
10. Diogo R, Abdala V. 2010. Muscles of vertebrates. Boca Raton, FL: CRC Press.
11. Furniss D, Lettice LA, Taylor IB, et al. 2008. A variant in the sonic hedgehog regulatory sequence (ZRS) is associated with triphalangeal thumb and deregulates expression in the developing limb. Hum Mol Genet 17:2417-2423.
12. Galis F, van Alphen JJM, Metz JAJ. 2001. Why five fingers? Evolutionary constraints on digit numbers. Trends Ecol Evol 16:637-646.
13. Gonzalez F, Duboule D, Spitz F. 2007. Transgenic analysis of Hoxd gene regulation during digit development. Dev Biol 306:847-859.
14. Guillem P, Demondion X, Drizenko A, Fontaine C. 1999. La biophalange du pouce. Revue génénrale de la littérature. Morphologie 83:27-31.
15. Haines RW. 1969. Epiphyses and sesamoids. In: Gans C, editor. Biology of reptilia. New York: Academic Press. p 81-115.
16. Haines RW. 1974. The pseudoepiphysis of the first metacarpal of man. J Anat 117:145-158.
17. Hamrick MW. 1999. A chondral modeling theory revisited. J Theor Biol 201:201-298.
18. Hamrick MW. 2001. Primate origins: Evolutionary change in digital ray patterning and segmentation. J Hum Evol 40:339-351.
19. Harfe BD, Scherz PJ, Nissim S, et al. 2004. Evidence for an expansion-based temporal Shh gradient in specifying vertebrate digit identities. Cell 118:517-528.
20. Hartmann C, Tabin CJ. 2001. Wnt-14 plays a pivotal role in inducing synovial joint formation in the developing appendicular skeleton. Cell 104:341-351.
21. Hautier L, Weisbecker V, Sánchez-Villagra MR, Goswami A, Asher RJ. 2010. Skeletal development in sloths and the evolution of mammalian vertebral patterning. Proc Natl Acad Sci U S A 107:18903-18908.
22. Heiss H. 1957. Beiderseitige kongenitale daumenlose Fünffingerhand bei Mutter und Kind. Z Anat Entwicklungsgesch 120:226-231.
23. Hendrikse JL, Parsons TE, Hallgrimsson B. 2007. Evolvability as the proper focus of evolutionary developmental biology. Evol Dev 9:393-401.
24. Hopson JA. 1995. Patterns of evolution in the manus and pes of non-mammalian therapsids. J Vertebr Paleontol 15:615-639.
25. Jenkins FA. 1971. The postcranial skeleton of African cynodonts. New Haven: Peabody Museum of Natural History.
26. Jenkins FA Jr, Parrington FR. 1976. The postcranial skeletons of the Triassic mammals Eozostrodon, Megazostrodon and Erythrotherium. Philos Trans R Soc Lond B Biol Sci 273:387-431.
27. Ji Q, Luo ZX, Yuan CX, et al. 2002. The earliest known eutherian mammal. Nature 416:816-822.
28. Kember NF, Kirkwood JK, Duignan PJ, Godfrey D, Spratt DJ. 1990. Comparative cell kinetics of avian growth plates. Res Vet Sci 49:283-288.
29. Kemp TS. 1982. Mammal-like reptiles and the origin of mammals. London: Academic Press.
30. Kielan-Jaworowska Z, Hurum JH. 2006. Limb posture in early mammals: Sprawling or parasagittal. Acta Palaeontol Pol 51:393-406.
31. Knezevic V, De Santo R, Schughart K, et al. 1997. Hoxd-12 differentially affects preaxial and postaxial chondrogenic branches in the limb and regulates Sonic hedgehog in a positive feedback loop. Development 124:4523-4536.
32. Lacroix L. 1951. The organization of bones. Philadelphia: The Blakiston Company.
33. Latimer B, Lovejoy CO. 1990. Hallucal tarsometatarsal joint in Australopithecus afarensis. Am J Phys Anthropol 82:125-133.
34. Li Y, Qiu Q, Watson SS, Schweitzer R, Johnson RL. 2010. Uncoupling skeletal and connective tissue patterning: Conditional deletion in cartilage progenitors reveals cell-autonomous requirements for Lmx1b in dorsal-ventral limb patterning. Development 137:1181-1188.
35. Limb D, Loughenbury PR. 2012. The prevalence of pseudoepiphyses in the metacarpals of the growing hand. J Hand Surg Eur 37:678-681.
36. Lovejoy CO, Cohn MJ, White TD. 1999. Morphological analysis of the mammalian postcranium: A developmental perspective. Proc Nat Acad Sci USA 96:13247-13252.
37. Luo ZX, Ji Q, Yuan CX. 2007. Convergent dental adaptations in pseudo-tribosphenic and tribosphenic mammals. Nature 450:93-97.
38. Luo ZX, Yuan CX, Meng QJ, Ji Q. 2011. A Jurassic eutherian mammal and divergence of marsupials and placentals. Nature 476:442-445.
39. Maisano JA. 2002a. Postnatal skeletal ontogeny in Callisaurus draconoides and Uta stansburiana (Iguania: Phrynosomatidae). J Morphol 251:114-139.
40. Maisano JA. 2002b. Postnatal skeletal ontogeny in five Xantusiids. J Morphol 254:1-38.
41. McCollum MA, Rosenman BA, Suwa G, Meindl RS, Lovejoy CO. 2010. The vertebral formula of the last common ancestor of African apes and humans. J Exp Zool B Mol Dev Evol 314:123-134.
42. Mitgutsch C, Richardson MK, Jiménez R, Martin JE, Kondrashov P, de Bakker MA, Sánchez-Villagra MR. 2012. Circumventing the polydactyly "constraint": The mole's "thumb." Biol Lett 8:74-77.
43. Montavon T, Le Garrec JF, Kerszberg M, Duboule D. 2008. Modeling Hox gene regulation in digits: Reverse collinearity and the molecular origin of thumbness. Genes Dev 22:346-359.
44. Montavon T, Soshnikova N, Mascrez B, et al. 2011. A regulatory archipelago controls Hox genes transcription in digits. Cell 147:1132-1145.
45. Moodie RL. 1908. Reptilian epiphyses. Am J Anat 7:443-467.
46. Morgan BA, Izpisuabelmonte JC, Duboule D, Tabin CJ. 1992. Targeted misexpression of Hox-4.6 in the avian limb bud causes apparent homeotic transformations. Nature 358:236-239.
47. Müller GB, 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.
48. Müller J, Scheyer TM, Head JJ, Barrett PM, Werneburg I, Ericson PG, Pol D, Sánchez-Villagra MR. 2010. Homeotic effects, somitogenesis and the evolution of vertebral numbers in recent and fossil amniotes. Proc Natl Acad Sci U S A 107:2118-2123.
49. Napier JR, Napier PH. 1985. The natural history of primates. Cambridge, MA: The MIT Press.
50. Nelson CE, Morgan BA, Burke AC, Laufer E, et al. 1996. Analysis of Hox gene expression in the chick limb bud. Development 122:1449-1466.
51. Ogden JA, Ganey TM, Light TR, Belsole RJ, Greene TL. 1994. Ossification and pseudoepiphysis formation in the "nonepiphyseal" end of bones of the hand and feet. Skeletal Radiol 23:3-13.
52. Pilbeam D. 2004. The anthropoid postcranial axial skeleton: Comments on development, variation, and evolution. J Exp Zool B Mol Dev Evol 302:241-267.
53. Prabhakar S, Visel A, Akiyama JA, et al. 2008. Human-specific gain of function in a developmental enhancer. Science 321:1346-1350.
54. Qazi Q, Kassner EG. 1988. Triphalangeal thumb. J Med Genet 25:505-520.
55. Reno PL, McCollum MA, Lovejoy CO, Meindl RS. 2000. Adaptationism and the anthropoid postcranium: Selection does not govern the length of the radial neck. J Morphol 246:59-67.
56. Reno PL, DeGusta D, Serrat MA, et al. 2005. Plio-pleistocene hominid limb proportions-Evolutionary reversals or estimation errors? Cur Anthropol 46:575-588.
57. Reno PL, McBurney DL, Lovejoy CO, Horton WE. 2006. Ossification of the mouse metatarsal: Differentiation and proliferation in the presence/absence of a defined growth plate. Anat Rec A288A:104-118.
58. Reno PL, Horton WE, Elsey RM, Lovejoy CO. 2007. Growth plate formation and development in alligator and mouse metapodials: Evolutionary and functional implications. J Exp Zool B Mol Dev Evol 308B:283-296.
59. Reno PL, McCollum MA, Cohn MJ, Meindl RS, Hamrick M, Lovejoy CO. 2008. Patterns of correlation and covariation of anthropoid distal forelimb segments correspond to Hoxd expression territories. J Exp Zool B Mol Dev Evol 310B:240-258.
60. Rieppel O. 1992. Studies on skeleton formation in reptiles 1. The postembryonic development of the skeleton in Cyrtodactylus pubisulcus (Reptilia, Gekkonidae). J Zool 227:87-100.
61. Rieppel O. 1994. Homology, topology, and typology: The history of modern debates. In: Hall BK, editor. Homology: The hierarchical basis of comparative biology. San Diego: Academic Press. p 63-100.
62. Sánchez-Villagra MR, Gemballa S, Nummela S, Smith KK, Maier W. 2002. Ontogenetic and phylogenetic transformations of the ear ossicles in marsupial mammals. J Morphol 251:219-238.
63. Sarrafian SK. 1993. Anatomy of the foot and ankle: Descriptive, topagraphical, functional. Philadelphia: J.B. Lippincott Company.
64. Sereno PC. 2006. Shoulder girdle and forelimb in multituberculates: Evolution of parasagittal forelimb posture in mammals. In: Carrano MT, Gaudin TJ, Blob RW, Wible JR, editors. Amniote paleobiology: Perspectives on the evolution of mammals, birds, and reptiles. Chicago: The University of Chicago Press. p 325-366.
65. Shively MJ. 1978. First metacarpal bone or proximal phalanx? Vet Radiol Ultrasound 19:50-52.
66. Standring S. 2005. Gray's anatomy. Edinburgh: Elsevier.
67. Storm EE, Kingsley DM. 1999. GDF5 coordinates bone and joint formation during digit development. Dev Biol 209:11-27.
68. Struthers J. 1863. On variation in the number of finters and toes, and the number of phalanges in man. Edinb New Philisophical J 18:83-111.
69. Suzuki T, Hasso SM, Fallon JF. 2008. Unique SMAD1/5/8 activity at the phalanx-forming region determines digit identity. Proc Natl Acad Sci U S A 105:4185-4190.
70. Szalay FS. 1994. Evolutionary history of the marsupials and an analysis of osteological characters. Cambridge: Cambridge University Press.
71. Thomson A. 1869. On the differences in the mode of ossification of the first and other metacarpal and metatarsal bones. J Anat 3:131-146.
72. Valenzuela CY, Berríos-Loyola R, Canals A. 2009. The first metacarpal in the thumb first phalange. EvoDevo implications. Int J Morphol 27:985-988.
73. Vargas AO, Fallon JF. 2005. Birds have dinosaur wings: The molecular evidence. J Exp Zoo B Mol Dev Evol 304B:86-90.
74. Vargas AO, Kohlsdorf T, Fallon JF, VandenBrooks J, Wagner GP. 2008. The Evolution of HoxD-11 Expression in the Bird Wing: Insights from Alligator mississippiensis. PLoS ONE 3:e3325. DOI: 10.1371/journal.pone.0003325
75. Vesalius A. 1998. On the fabric of the human Body. W.F. Richarson, translator. San Francisco: Norman Publishing.
76. Wagner GP. 2005. The developmental evolution of avian digit homology: An update. Theory Biosci 124:165-183.
77. Wagner GP. 2007. The developmental genetics of homology. Nat Rev Genet 8:473-479.
78. Wagner GP, Altenberg L. 1996. Complex adaptations and the evolution of evolvability. Evolution 50:967-976.
79. Wagner GP, Gauthier JA. 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.
80. Wagner GP, Vargas AO. 2008. On the nature of thumbs. Genome Biol 9:213.
81. Wang Z, Young RL, Xue H, Wagner GP. 2011. Transcriptomic analysis of avian digits reveals conserved and derived digit identities in birds. Nature 477:583-586.
82. Woltering JM, Duboule D. 2010. The origin of digits: Expression patterns versus regulatory mechanisms. Dev Cell 18:526-532.
83. Zuidam JM, Dees EE, Lequin MH, Hovius SE. 2006. The effect of the epiphyseal growth plate on the length of the first metacarpal in triphalangeal thumb. J Hand Surg 31:1183-1188.