The evolutionary geometry of human anatomy: Discovering our inner fly

Evolutionary Anthropology

Volumn 19, Issue 6, 2010, Pages 227-235

  Held, Lewis I ^a  

^a TEXAS TECH UNIVERSITY   (United States)

Author keywords

Asymmetry; Atavism; Bilateria; Epiphanies; Evo devo; Hair patterning; Heterochrony; Homeobox; Morphogens; Origami

Indexed keywords

ANIMALIA; BILATERIA;

EID: 78651296355     PISSN: 10601538     EISSN: 15206505     Source Type: Journal    
DOI: 10.1002/evan.20287     Document Type: Article

References (100)

1. Cantore E. 1977. Scientific man: the humanistic significance of science. New York: Institute of Scientific Humanism Publications.
2. Bronowski J. 1956. Science and human values. New York: Harper & Row.
3. Darwin C. 1871. The descent of man, and selection in relation to sex. London: John Murray.
4. Weiss KM, Buchanan AV. 2004. Genetics and the logic of evolution. Hoboken, NJ: John Wiley & Sons.
5. Mackay TFC, Anholt RRH. 2006. Of flies and man: Drosophila as a model for human complex traits. Annu Rev Genomics Hum Genet 7: 339-367.
6. Müller GB. 2008. Evo-devo as a discipline. In: Minelli A, Fusco G, editors. Evolving pathways: key themes in evolutionary developmental biology. New York: Cambridge University Press: 5-30.
7. Raff RA. 2000. Evo-devo: the evolution of a new discipline. Nature Rev Genet 1: 74-79.
8. Sander K, Schmidt-Ott U. 2004. Evo-devo aspects of classical and molecular data in a historical perspective. J Exp Zool (Mol Dev Evol) 302B: 69-91.
9. Wagner GP, Chiu C-H, Laubichler M. 2000. Developmental evolution as a mechanistic science: the inference from developmental mechanisms to evolutionary processes. Amer Zool 40: 819-831.
10. Wolpert L. 1969. Positional information and the spatial pattern of cellular differentiation. J Theor Biol 25: 1-47.
11. Briscoe J, Lawrence PA, Vincent J-P, editors. 2010. Generation and interpretation of morphogen gradients. Woodbury, NY: Cold Spring Harbor Laboratory Press.
12. Gerhart J, Kirschner M. 1997. Cells, embryos, and evolution. Malden, MA: Blackwell Science.
13. Driever W. 2004. The bicoid morphogen papers (II): account from Wolfgang Driever. Cell S116: S7-S9.
14. Zeitlinger J, Stark A. 2010. Developmental gene regulation in the era of genomics. Dev Biol 339: 230-239.
15. El-Hawrani A, Sohn M, Noga M, El-Hakim H. 2006. The face does predict the brain: midline facial and forebrain defects uncovered during the investigation of nasal obstruction and rhinorrhea. Case report and a review of holoprosencephaly and its classifications. Int J Pediatr Otorhinolaryngol 70: 935-940.
16. Ingham PW, Placzek M. 2006. Orchestrating ontogenesis: variations on a theme by sonic hedgehog. Nat Rev Genet 7: 841-850.
17. Tabin CJ, McMahon AP. 2008. Grasping limb patterning. Science 321: 350-352.
18. Cohen MM, Jr. 2006. Holoprosencephaly: clinical, anatomic, and molecular dimensions. Birth Defects Res (Pt. A): Clin Mol Teratol 76: 658-673.
19. Litingtung Y, Dahn RD, Li Y, Fallon JF, Chiang C. 2002. Shh and Gli3 are dispensable for limb skeleton formation but regulate digit number and identity. Nature 418: 979-983.
20. Pettigrew JD. 1991. Evolution of binocular vision. In: Cronly-Dillon JR, Gregory RL, editors. Evolution of the eye and visual system. Boston, Mass.: CRC Press. p 271-283.
21. 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 (Mol Dev Evol) 310B: 240-258.
22. Gurnett CA, Bowcock AM, Dietz FR, Morcuende JA, Murray JC, Dobbs MB. 2007. Two novel point mutations in the long-range SHH enhancer in three families with triphalangeal thumb and preaxial polydactyly. Am J Med Genet 143A: 27-32.
23. Hu D, Helms JA. 1999. The role of sonic hedgehog in normal and abnormal craniofacial morphogenesis. Development 126: 4873-4884.
24. Carroll SB. 2005. Endless forms most beautiful: the new science of evo devo and the making of the animal kingdom. New York: Norton.
25. McGinnis W. 1994. A century of homeosis, a decade of homeoboxes. Genetics 137: 607-611.
26. McGinnis W, Krumlauf R. 1992. Homeobox genes and axial patterning. Cell 68: 283-302.
27. de Santa Barbara P, Roberts DJ. 2002. Tail gut endoderm and gut/genitourinary/tail development: a new tissue-specific role for Hoxa13. Development 129: 551-561.
28. Held LI, Jr. 2009. Quirks of human anatomy: an evo-devo look at the human body. New York: Cambridge University Press.
29. Indrebo A, Langeland M, Juul HM, Skogmo HK, Rengmark AH, Lingaas F. 2008. A study of inherited short tail and taillessness in Pembroke Welsh corgi. J Small Anim Pract 49: 220-224.
30. Deforest ME, Basrur PK. 1979. Malformations and the manx syndrome in cats. Can Vet J 20: 304-314.
31. Whitcome KK, Shapiro LJ, Lieberman DE. 2007. Fetal load and the evolution of lumbar lordosis in bipedal hominins. Nature 450: 1075-1078.
32. Woltering JM, Duboule D. 2010. The origin of digits: expression patterns versus regulatory mechanisms. Cell 18: 526-532.
33. Heiss H. 1957. Beiderseitige kongenitale daumenlose Fünffingerhand bei Mutter und Kind. Z Anat Entw-Gesch 120: 226-231.
34. Vargas AO, Fallon JF. 2005. The digits of the wing of birds are 1, 2, and 3: a review. J Exp Zool (Mol Dev Evol) 304B: 206-219.
35. Hallgrímsson B, Jamniczky H, Young NM, Rolian C, Parsons TE, Boughner JC, Marcucio RS. 2009. Deciphering the palimpsest: studying the relationship between morphological integration and phenotypic covariation. Evol Biol 36: 355-376.
36. Nübler-Jung K, Arendt D. 1994. Is ventral in insects dorsal in vertebrates? A history of embryological arguments favouring axis inversion in chordate ancestors. Roux's Arch Dev Biol 203: 357-366.
37. Niehrs C. 2010. On growth and form: a Cartesian coordinate system of Wnt and BMP signaling specifies bilaterian body axes. Development 137: 845-857.
38. Gerhart J. 2000. Inversion of the chordate body axis: are there alternatives? Proc Natl Acad Sci USA 97: 4445-4448.
39. Lapraz F, Besnardeau L, Lepage T. 2009. Patterning of the dorsal-ventral axis in echinoderms: insights into the evolution of the BMP-chordin signaling network. PLoS Biol 7: e1000248.
40. Lowe CJ, Terasaki M, Wu M, Freeman RM, Jr, Runft L, Kwan K, Haigo S, Aronowicz J, Lander E, Gruber C, Smith M, Kirschner M, Gerhart J. 2006. Dorsoventral patterning in hemichordates: insights into early chordate evolution. PLoS Biol 4: 1603-1619.
41. Grande C, Patel NH. 2009. Nodal signalling is involved in left-right asymmetry in snails. Nature 457: 1007-1011.
42. Weiss K. 2002. Is the medium the message? Biological traits and their regulation. Evol Anthropol 11: 88-93.
43. Ashburner M. 2006. Won for all: How the Drosophila genome was sequenced. Plainview, NY: Cold Spring Harbor Laboratory Press.
44. Held LI, Jr. 2002. Imaginal discs: the genetic and cellular logic of pattern formation. New York: Cambridge University Press.
45. Morris D. 1967. The naked ape: a zoologist's study of the human animal. New York: Random House.
46. Jablonski NG. 2010. The naked truth. Sci Am 302: 42-49.
47. Held LI, Jr. 2010. The evo-devo puzzle of human hair patterning. Evol Biol 37: 113-122.
48. Borok MJ, Tran DA, Ho MCW, Drewell RA. 2010. Dissecting the regulatory switches of development: lessons from enhancer evolution in Drosophila. Development 137: 5-13.
49. Närhi K, Järvinen E, Birchmeier W, Taketo MM, Mikkola ML, Thesleff I. 2008. Sustained epithelial β-catenin activity induces precocious hair development but disrupts hair follicle down-growth and hair shaft formation. Development 135: 1019-1028.
50. Zhang Y, Andl T, Yang SH, Teta M, Liu F, Seykora JT, Tobias JW, Piccolo S, Schmidt-Ullrich R, Nagy A, Taketo MM, Dlugosz AA, Millar SE. 2008. Activation of β-catenin signaling programs embryonic epidermis to hair follicle fate. Development 135: 2161-2172.
51. Lo Celso C, Prowse DM, Watt FM. 2004. Transient activation of β-catenin signalling in adult mouse epidermis is sufficient to induce new hair follicles but continuous activation is required to maintain hair follicle tumours. Development 131: 1787-1799.
52. Huelsken J, Vogel R, Erdmann B, Cotsarelis G, Birchmeier W. 2001. β-Catenin controls hair follicle morphogenesis and stem cell differentiation in the skin. Cell 105: 533-545.
53. Rogers GE. 2004. Hair follicle differentiation and regulation. Int J Dev Biol 48: 163-170.
54. van Amerongen R, Nusse R. 2009. Towards an integrated view of Wnt signaling in development. Development 136: 3205-3214.
55. Baer MM, Chanut-Delalande H, Affolter M. 2009. Cellular and molecular mechanisms underlying the formation of biological tubes. Curr Topics Dev Biol 89: 137-162.
56. Gilbert SF. 2010. Developmental biology. Sunderland, MA: Sinauer.
57. Moore KL, Persaud TVN. 2008. The developing human: clinically oriented embryology. Philadelphia: Saunders.
58. Weiss K, Aldridge K. 2003. What stamps the wrinkle deep on the brow? Evol Anthropol 12: 205-210.
59. Schoenwolf GC, Bleyl SB, Brauer PR, Francis-West PH. 2009. Larsen's human embryology. Philadelphia: Churchill Livingstone.
60. Shubin N. 2008. Your inner fish: a journey into the 3.5-billion-year history of the human body. New York: Pantheon Books.
61. Hendrikse JL, Parsons TE, Hallgrímsson B. 2007. Evolvability as the proper focus of evolutionary developmental biology. Evol Dev 9: 393-401.
62. Konkel MK, Walker JA, Batzer MA. 2010. Lines and sines of primate evolution. Ev Anth 19(6): pp 236-249.
63. Rister J, Desplan C. 2010. Deciphering the genome's regulatory code: the many languages of DNA. BioEssays 32: 381-384.
64. Willmore KE. 2010. Development influences evolution. Am Sci 98: 220-227.
65. Suzanne M, Petzoldt AG, Spéder P, Coutelis J-B, Steller H, Noselli S. 2010. Coupling of apoptosis and L/R patterning controls stepwise organ looping. Curr Biol 20: 1773-1778.
66. Werner T, Koshikawa S, Williams TM, Carroll SB. 2010. Generation of a novel wing colour pattern by the Wingless morphogen. Nature 464: 1143-1148.
67. Kohlsdorf T, Wagner GP. 2006. Evidence for the reversibility of digit loss: a phylogenetic study of limb evolution in Bachia (Gymnophthalmidae: Squamata). Evolution 60: 1896-1912.
68. Porter ML, Crandall KA. 2003. Lost along the way: the significance of evolution in reverse. Trends Ecol Evol 18: 541-547.
69. Weiss K, Sholtis S. 2003. Dinner at baby's: werewolves, dinosaur jaws, hen's teeth, and horse toes. Evol Anthropol 12: 247-251.
70. Verhulst J. 1996. Atavisms in Homo sapiens: a Bolkian heterodoxy revisited. Acta Biotheor 44: 59-73.
71. Brandley MC, Huelsenbeck JP, Wiens JJ. 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 of intermediate body forms. Evolution 62: 2042-2064.
72. Wendelin DS, Pope DN, Mallory SB. 2003. Hypertrichosis. J Am Acad Dermatol 48: 161-179.
73. Sun M, Li N, Dong W, Chen Z, Liu Q, Xu Y, He G, Shi Y, Li X, Hao J, Luo Y, Shang D, Lv D, Ma F, Zhang D, Hua R, Lu C, Wen Y, Cao L, Irvine AD, McLean WHI, Dong Q, Wang M-R, Yu J, He L, Lo WHY, Zhang X. 2009. Copy-number mutations on chromosome 17q24.2-q24.3 in congenital generalized hypertrichosis terminalis with or without gingival hyperplasia. Am J Hum Genet 84: 807-813.
74. Bolk L. 1926. Das problem der menschwerdung. Jena: Gustav Fischer.
75. Gould SJ. 1977. Ontogeny and phylogeny. Cambridge, MA: Harvard University Press.
76. Shea BT. 1989. Heterochrony in human evolution: the case for neoteny reconsidered. Yearbk Phys Anthropol 32: 69-101.
77. Smith KK. 2003. Time's arrow: heterochrony and the evolution of development. Int J Dev Biol 47: 613-621.
78. Wilson GN. 1988. Heterochrony and human malformation. Am J Med Genet 29: 311-321.
79. Alba DM. 2002. Shape and stage in heterochronic models. In: Minugh-Purvis N, McNamara K, editors. Human evolution through developmental change. Baltimore: Johns Hopkins University Press: 28-50.
80. Weirauch MT, Hughes TR. 2010. Conserved expression without conserved regulatory sequence: the more things change, the more they stay the same. Trends Genet 26: 66-74.
81. Vinagre T, Moncaut N, Carapuço M, Nóvoa A, Bom J, Mallo M. 2010. Evidence for a myotomal Hox/Myf cascade governing nonautonomous control of rib specification within global vertebral domains. Dev Cell 18: 655-661.
82. 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 USA. In press.
83. Montero JA, Hurlé JM. 2007. Deconstructing digit chondrogenesis. BioEssays 29: 725-737.
84. Panman L, Galli A, Lagarde N, Michos O, Soete G, Zuniga A, Zeller R. 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.
85. Robert B, Lallemand Y. 2006. Anteroposterior patterning in the limb and digit specification: contributions of mouse genetics. Dev Dynamics 235: 2337-2352.
86. Dessaud E, Yang LL, Hill K, Cox B, Ulloa F, Ribeiro A, Mynett A, Novitch BG, Briscoe J. 2007. Interpretation of the sonic hedgehog morphogen gradient by a temporal adaptation mechanism. Nature 450: 717-720.
87. Niswander L. 2003. Pattern formation: old models out on a limb. Nature Rev Genet 4: 133-143.
88. Kmita M, Fraudeau N, Hérault Y, Duboule D. 2002. Serial deletions and duplications suggest a mechanism for the collinearity of Hoxd genes in limbs. Nature 420: 145-150.
89. Marzke MW, Marzke RF. 2000. Evolution of the human hand: approaches to acquiring, analysing and interpreting the anatomical evidence. J Anat 197: 121-140.
90. Knezevic V, De Santo R, Schughart K, Huffstadt U, Chiang C, Mahon KA, Mackem S. 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.
91. Bier E, McGinnis W. 2004. Model organisms in the study of development and disease. In: Epstein CJ, Erickson RP, Wynshaw-Boris A, editors. Inborn errors of development: the molecular basis of clinical disorders of morphogenesis. New York: Oxford University Press. pp. 25-45.
92. De Robertis EM, Sasai Y. 1996. A common plan for dorsoventral patterning in Bilateria. Nature 380: 37-40.
93. Gould SJ. 1997. As the worm turns. Nat Hist 106: 24-27, 68-73.
94. Telford MJ. 2007. A single origin of the central nervous system? Cell 129: 237-239.
95. Hirokawa N, Tanaka Y, Okada Y, Takeda S. 2006. Nodal flow and the generation of left-right asymmetry. Cell 125: 33-45.
96. Zacchetti G, Duboule D, Zakany J. 2007. Hox gene function in vertebrate gut morphogenesis: the case of the caecum. Development 134: 3967-3973.
97. Chivers DJ. 1992. Diet and guts. In: Bunney S, Jones S, Martin R, Pilbeam D editors. The cambridge encyclopedia of human evolution. New York: Cambridge University Press. pp. 60-64.
98. Schier AF. 2009. Nodal morphogens. Cold Spring Harbor Perspect Biol 1: a003459.
99. Massagué J, Chen Y-G. 2000. Controlling TGF-β signaling. Genes Dev 14: 627-644.
100. Martini FH, Ober WC, Garrison CW, Welch K, Hutchings RT, Ireland K. 2004. Fundamentals of anatomy and physiology. San Francisco: Benjamin Cummings.