Extreme selection in humans against homeotic transformations of cervical vertebrae

Evolution

Volumn 60, Issue 12, 2006, Pages 2643-2654

  Galis, Frietson ^a   Van Dooren, Tom J M ^a   Feuth, Johan D ^b   Metz, Johan A J ^a,c   Witkam, Andrea ^a   Ruinard, Sebastiaan ^a   Steigenga, Marc J ^a,e   Wijnaendts, Liliane C D ^d  

^a LEIDEN UNIVERSITY   (Netherlands)

^b LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^c INTERNATIONAL INSTITUTE FOR APPLIED SYSTEMS ANALYSIS   (Austria)

^d VU UNIVERSITY MEDICAL CENTER   (Netherlands)

^e UNIVERSITY OF BAYREUTH   (Germany)

Author keywords

Developmental constraint; Evolutionary medicine; Hox genes; Left right asymmetry; Modularity; Phylotypic stage; Pleiotropy

Indexed keywords

ABNORMALITY; ASYMMETRY; DEVELOPMENTAL BIOLOGY; DEVELOPMENTAL STABILITY; EVOLUTIONARY BIOLOGY; MAMMAL; NATURAL SELECTION; PLEIOTROPY; VERTEBRATE;

ADULT; ARTICLE; CERVICAL SPINE; CONGENITAL MALFORMATION; FEMALE; FETUS; GENETIC SELECTION; HOMEOBOX; HUMAN; INFANT; MALE; MUSCULOSKELETAL SYSTEM MALFORMATION; PREVALENCE; RADIOGRAPHY; VERTEBRA;

ADULT; CERVICAL VERTEBRAE; FEMALE; FETUS; GENES, HOMEOBOX; HUMANS; INFANT; MALE; MUSCULOSKELETAL ABNORMALITIES; PREVALENCE; SELECTION (GENETICS); THORACIC VERTEBRAE;

MAMMALIA; SLOTHS; TRICHECHIDAE; VERTEBRATA;

EID: 33846869275     PISSN: 00143820     EISSN: 15585646     Source Type: Journal    
DOI: 10.1554/06-064.1     Document Type: Article

References (100)

1. Abbott, M. K., and T. C. Kaufman. 1986. The relationship between the functional complexity and the molecular organization of the Antennapedia locus of Drosophila melanogaster. Genetics 114: 919-942.
2. Adson, A. W., and J. R. Coffey. 1947. Cervical rib. Ann. Surg. 85: 839-857.
3. Agresti, A. 2002. Categorical data analysis. 2nd ed. Wiley, New York.
4. Akaike, H. 1973. Information theory and an extension of the maximum likelihood principle. Pp. 267-281 in B. N. Petrov and F. Csaki, eds. Second international symposium on information theory. Academiai Kiado, Budapest.
5. Amundson, R. 1994. Two concepts of constraint: adaptationism and the challenge from developmental biology. Philos. Sci. 61: 556-578.
6. _. 2005. The changing role of the embryo in evolutionary thought: roots of evo-devo. Cambridge Univ. Press, Cambridge, U.K.
7. Ancel, P., and L. Sencert. 1902. De quelques variations dans la nombre des vertèbres chez l'homme leur interpretation. J. Anat. Physiol. 38:218-257.
8. Arthur, W. 2004. Biased embryos and evolution. Cambridge Univ. Press, Cambridge, U.K.
9. Bardeen, C. R. 1904. Numerical vertebral variation in the human adult and embryo. Anat. Anz. 25:497-519.
10. Bates, A. W., and K. Nale. 2005. Segmentation defects of the human axial skeleton without dysostoses or skeletal dysplasia. Fetal Ped. Pathol. 24:121-127.
11. Bateson, W. 1894. Materials for the study of variation. Macmillan, London.
12. Bel-Vialar, S., N. Itasaki, and R. Krumlauf. 2002. Initiating Hox gene expression: in the early chick neural tube differential sensitivity to FGF and RA signalling subdivides the HoxB genes in two distinct groups. Development 129:5103-5115.
13. Berner, F. 1944. über Rippenanomalien auf Grund von 6 Millionen Reihenbildern. Fortschr. Rontgenstr. 69:202-221.
14. Bianchi, S. 1894. Sulla frequenza della anomalie numeriche vertebrali nello scheletro dei normali e degli alienati. Atti R. Accad. Fisiocrit. Siena 7:21-31.
15. Burke, A. C., C. E. Nelson, B. A. Morgan, and C. Tabin. 1995. Hox genes and the evolution of vertebrate axial morphology. Development 121:333-346.
16. Cartlidge, P. H. T., and J. H. Stewart. 1995. Effect of changing the stillbirth definition on evaluation of perinatal mortality rates. Lancet 346:486-488.
17. Chernoff, N., and J. M. Rogers. 2004. Supernumerary ribs in developmental toxicity bioassays and in human populations: incidence and biological significance. J. Toxicol. Environ. Health B. Crit. Rev. 7:437-449.
18. Cohn, M. J., and C. Tickle. 1999. Developmental basis of limblessness and axial patterning in snakes. Nature 399:474-479.
19. Cordes, R., K. Schuster-Gossler, K. Serth, and A. Gossler. 2004. Specification of vertebral identity is coupled to notch signalling and the segmentation clock. Development 131:1221-1233.
20. Coury, C., and J. Delaporte. 1954. Les anomalies congenitales des ôtes. Sem. Hop. Paris. 42:2656-2673.
21. Crimm, P. D. 1952. Evaluation of a five year minifilm program. Am. J. Roentg. 68:240-246.
22. Cuvier, G. 1835. Leçons d' anatomie comparée. Tome premier. 2nd ed. Crochard, Paris.
23. Davis, D. B., and J. C. King. 1939. Cervical rib in early life. Am. J. Dis. Children 56:744-755.
24. De Galan-Roosen, A. E. M, J. C. Kuijpers, A. P. Meershoek, and D. van Velzen. 1998. Contribution of congenital malformations to perinatal mortality: a 10 years prospective regional study in The Netherlands. Eur. J. Obstet. Gyn. Reprod. Biol. 80:55-61.
25. De Rosa, R., J. K. Grenier, J. Andreeva, C. E. Cook, A. Adoutte, M. Akam, S. B. Carroll, and G. Balavoine. 1999. Hox genes in brachiopods and priapulids and protostome evolution. Nature 399:772-776.
26. Diez del Corral, R., I. Olivera-Martinez, A. Goriely, E. Gale, M. Maden, and K. Storey. 2003. Opposing FGF and retinoid pathways control ventral neural pattern, neuronal differentiation, and segmentation during body axis extension. Neuron 40:65-79.
27. Dubrulle, J., and O. Pourquié. 2004. fgf8 mRNA decay establishes a gradient that couples axial elongation to patterning in the vertebrate embryo. Nature 427:419-422.
28. Dubrulle, J., M. J. McGrew, and O. Pourquié. 2001. FGF signaling controls somite boundary position and regulates segmentation clock control of spatiotemporal Hox gene activation. Cell 106: 219-232.
29. Ensini, M., T. N. Tsuchida, H.-G. Belting, and T. M. Jessell. 1998. The control of rostrocaudal pattern in the developing spinal cord: specification of motor neuron subtype identity is initiated by signals from paraxial mesoderm. Development 125:969-982.
30. Erken, E., H. T. E. Ozer, B. Gulek, and B. Durgun. 2002. The association between cervical rib and sacralization. Spine 27: 1659-1664.
31. Eurocat Report 1997. No. 7. Fifteen years of surveillance of con genital anomalies in Europe 1980-1994. Scientific Institute of Public Health, Brussels.
32. Eurocat Report 1999. Update to Report No. 7. Prevalence of congenital anomalies in Europe 1995-1996. Scientific Institue of Public Health, Brussels.
33. Fishel, A. 1906. Untersuchungen über die Wirbelsäule und den Brustkorb des Menschen. Anat. Hefte 31:462-588.
34. Flower, W. H., and R. Lydekker. 1891. The study of mammals. Adam and Charles Black, London.
35. Galis, F. 1999. Why do almost all mammals have seven cervical vertebrae? Developmental constraints, Hox genes and cancer. J. Exp. Zool. B. (Mol. Dev. Evol.) 285:19-26.
36. Galis, F., and J. A. J. Metz. 2001. Testing the vulnerability of the phylotypic stage. J. Exp. Zool. B. (Mol. Dev. Evol.) 291:195-204.
37. _. 2003. Anti-cancer selection as a source of developmental and evolutionary constraints. BioEssays 25:1035-1039.
38. Galis, F., J. A. J. Metz, and J. J. M. van Alphen. 2002a. Why five fingers? Evolutionary constraints on digit numbers. Trends Ecol. Evol. 16:637-646.
39. Galis, F., T. J. Van Dooren, and J. A. J. Metz. 2002b. Conservation of the segmented germband stage: robustness or pleiotropy? Trends Genet. 18:504-509.
40. Gaunt, S. J. 1994. Conservation in the Hox code during morphological evolution. Int. J. Dev. Biol. 38:549-552.
41. Gladstone, R. J., and C. P. G. Wakeley. 1932. Cervical ribs and rudimentary first thoracic ribs considered from the clinical and etiological standpoints. J. Anat. 66:334-337.
42. Grapin-Botton, A., M.-A. Bonnin, and N. M. LeDouarin. 1997. Hox gene induction in the neural tube depends on three parameters: competence, signal supply and paralogue group. Development 124:849-859.
43. Hall, B. K. 1999. Evolutionary developmental biology. 2nd ed. Kluwer Academic Press, Dordrecht, The Netherlands.
44. Hansen, T. F., and D. Houle. 2004. Evolvability, stabilizing selection, and the problem of stasis. Pp. 130-150 in M. Pigliucci and K. Preston, eds. Phenotypic integration: studying the ecology and evolution of complex phenotypes. Oxford Univ. Press, Oxford, U.K.
45. Henderson, M. S. 1913. Cervical rib: report of thirty-one cases. Am. J. Orthop. Surg. 11:408-430.
46. Kawakami, Y., A. Raya, R. M. Raya, C. Rodriguez-Esteban, and J. C. Belmonte. 2005. Retinoic acid signalling links left-right asymmetric patterning and bilaterally symmetric somitogenesis in the zebrafish embryo. Nature 435:165-171.
47. Keeling, J. W., and I. Kjaer. 1999. Cervical ribs: useful marker of monosomy X in fetal hydrops. Pediat. Dev. Pathol. 2:119-123.
48. Krebs, L. T., N. Iwai, S. Nonaka, I. C. Welsh, Y. Lan, R. Jiang, Y. Saijoy, T. P. O'Brien, H. Hamada, and T. Gridley. 2003. Notch signalling regulates left-right asymmetry determination by inducing Nodal expression. Genes Dev. 17:1207-1212.
49. Kumar, M., N. Jordan, D. Melton, and A. Grapin-Botton. 2003. Signals from lateral plate mesoderm instruct endoderm toward a pancreatic fate. Dev. Biol. 259:109-122.
50. Lancaster, P., and E. Pedisich. 1995. Congenital malformations Australia 1981-1992. Australian Institute of Health and Welfare, National Perinatal Statistics Unit, Sydeney.
51. Lanier, R. R. 1944. Length of first, twelfth, and accessory ribs in American Whites and Negroes; their relationship to certain vertebral variations. Am. J. Physical. Anthropol. 2:137-146.
52. Latimer, A. J., X. Dong, Y. Markov, and B. Appel. 2002. Deltanotch signaling induces hypochord development in zebrafish. Development 129:2555-2563.
53. Leboucq, H. 1898. Recherches sur les variations anatomiques de la première côte chez l'homme. Arch. Biol. 15:9-178.
54. Makhoul, R. G., and H. I. Machleder. 1992. Developmental anomalies at the thoracic outlet: an analysis of 2000 consecutive cases. J. Vasc. Surg. 16:534-545.
55. Mathis, L., P. M. Kulesa, and S. E. Fraser. 2001. FGF receptor signalling is required to maintain neural progenitors during Hensen's node progression. Nat. Cell Biol. 3:559-566.
56. Maynard Smith, J., R. Burian, S. Kauffman, P. Alberch, J. Campbell, B. Goodwin, R. Lande, D. Raup, and L. Wolpert. 1985. Developmental constraints and evolution. Q. Rev. Biol. 60: 265-287.
57. McNally, E., B. Sandin, and R. A. Wilkins. 1990. The ossification of the costal element of the seventh cervical vertebra with particular reference to cervical ribs. J. Anat. 170:125-129.
58. Menárguez Carretero, L., and M. Campo Muňoz. 1967. Estudio radiologico y tipos morfologicos de costillas cervicales en el sexo femenino. Enferm. Torax 16:285-308.
59. Merks, J. H. M., C. D. van Karnebeek, H. N. Caron, and R. C. Hennekam. 2003. Phenotypic abnormalities: terminology and classification. Am. J. Med. Genet. 123A:211-230.
60. Merks, J. H. M., A. M. Smets, R. R. van Rijn, J. Kobes, H. N. Caron, M. Maas, and R. C. Hennekam. 2005. Prevalence of rib anomalies in normal Caucasian children and childhood cancer patients. Eur. J. Med. Genet. 48:113-129.
61. Meyer, D. B. 1978. The appearance of "cervical ribs" during early human fetal development. Anat. Rec. 190:481.
62. Narita, Y., and S. Kuratani. 2005. Evolution of the vertebral formulae in mammals: a perspective on developmental constraints. J. Exp. Zool. B (Mol. Dev. Evol.) 304:91-106.
63. Ninomiya, H., R. P. Elinson, and R. Winklbauer. 2004. Anteroposterior tissue polarity links mesoderm convergent extension to axial patterning. Nature 430:364-367.
64. Noback, C. R., and G. G. Robertson. 1951. Sequences of appearance of ossification centers in the human skeleton during the first five prenatal months. Am. J. Anat. 89:1-28.
65. Nolte, E., A. Brand, I. Koupilova, and M. McKee. 2000. Neonatal and postneonatal mortality in Germany since unification. J. Epidemiol. Commun. Health 54:84-90.
66. Oostra, R. J., R. C. Hennekam, L. de Rooij, and A. F. Moorman. 2005. Malformations of the axial skeleton in Museum Vrolik. I. Homeotic transformations and numerical anomalies. Am. J. Med. Genet. A. 134:268-281.
67. Opitz, J. M., J.M. Fitzgerald, J. F. Reynolds, S. O. Lewin, A. Daniel, L. S. Ekblom, and S. Philips. 1987. The Montana fetal genetic pathology program and a review of prenatal death in humans. Am J. Med. Genet. Suppl. 3:93-112.
68. Paterson, A. M. 1893. The human sacrum. Trans. R. Dub Soc. 5: 123-204.
69. Pionnier, R., and A. Depraz. 1956. Les anomalies costales d'origine congénital (etude statistique d'après 10000 radiographies). Radiol. Clin. 25:170-186.
70. Raff, R. A. 1994. Developmental mechanisms in the evolution of animal form: origins and evolvability of body plans. Pp. 489-500 in S. Bengston, ed. Early life on Earth. Columbia Univ. Press, New York.
71. Raya, A., Y. Kawakami, C. Rodriguez-Esteban, M. Ibanes, D. Rasskin-Gutman, J. Rodriguez-Leon, D. Buscher, J. A. Feijo, and J. C. Izpisua Belmonte. 2004. Notch activity acts as a sensor for extracellular calcium during vertebrate left-right determination. Nature 427:121-128.
72. Richardson, M. K., J. Hanken, M. L. Gooneratne, C. Pieau, A. Raynaud, L. Selwood, and G. M. Wright. 1997. There is no highly conserved embryonic stage in the vertebrates: implications for current theories of evolution and development. Anat. Embryol. 196:91-106.
73. Roos, D. B. 1996. Historical perspectives and anatomic considerations. Semin. Thorac. Cardiovas. Surg. 8:183-189.
74. Rosenberg, E. 1899. Über eine primitive From der Wirbelsäule des Menschen. Morphol. Jahrb. 27:1-118.
75. Regan, L., P. R. Braude, and P. L. Trembath. 1989. Influence of past reproductive performance on risk of spontaneous abortion. Br. Med. J. 299:51-545.
76. Saito, D., S. Yonei-Tamura, Y. Takahashi, and K. Tamura. 2006. Level-specific role of paraxial mesoderm in regulation of Tbx5/Tbx4 expression and limb initiation. Dev. Biol. 292:79-89.
77. Sander, K. 1983. The evolution of patterning mechanisms: gleanings from insect embryogenesis and spermatogenesis. Pp. 137-159 in B. C. Goodwin, N. Holder, and C. C. Wylie, eds. Development and evolution. Cambridge Univ. Press, Cambridge, U.K.
78. Saraiya, M., C. J. Berg, H. Shulman, C. A. Green, and H. K. Atrash. 1999. Estimates of the annual number of clinically recognized pregnancies in the United States, 1981-1991. Am. J. Epidemiol. 149:1025-1029.
79. Schumacher, R., A. Mai, and P. Gutjahr. 1992. Association of rib anomalies and malignancy in childhood. Eur. J. Pediatr. 151:432-434.
80. Schwenk, K., and G. P. Wagner. 2003. Constraint. Pp. 52-60 in B. K. Hall and W. M. Olson, eds. Keywords and concepts in evolutionary developmental biology. Harvard Univ. Press, Cambridge, MA.
81. Sela-Donenfeld, D., and C. Kalcheim. 2000. Inhibition of noggin expression in the dorsal neural tube by somitogenesis: a mechanism for coordinating the timing of neural crest emigration. Development 127:4845-4854.
82. Simpson, E. H. 1951. The interpretation of interaction in contingency tables. J. R. Stat. Soc. B 13:238-241.
83. Slack, J. M., P. M. Holland, and C. F. Graham. 1993. The zootype and the phylotypic stage. Nature 361:490-492.
84. Southam, A. H., and O. B. E. Bythell. 1924. Cervical ribs in children. Br. Med. J. Nov. 8:844-845.
85. Staderini, R. 1894. Ricerche statistische sulla frequenza delle varieta numeriche delle vertebre nell'uomo. Monitore Zool. Ital 5:56-95.
86. Steigenga, M. J., F. M. Helmerhorst, J. de Koning, A. M. I. Tijssen, S. A. T. Ruinard, and F. Galis. 2006. Evolutionary conserved structures as indicators of medical risks: increased incidence of cervical ribs after ovarian hyper stimulation in mice. J. Anim. Biol. 56:63-68.
87. Steinbach 1889. Die zahl den caudalwirbel beim Mensahen. Ph.D. diss. University of Berlin, Berlin.
88. Steiner, H. A. 1943. Roentgenologic manifestations and clinical symptoms of rib abnormalities. Radiology 40:175-178.
89. Stern, C. D., J. Charité, J. Deschamps, D. Duboule, A. J. Durston, M. Kmita, J. F. Nicolas, I. Palmeirim, J. C. Smith, and L. Wolpert. 2006. Head-tail patterning of the vertebrate embryo: one, two or many unresolved problems? Int. J. Dev. Biol. 50:3-15.
90. Sycamore, L. K. 1944. Common congenital anomalies of the bony thorax. Am. J. Roentg. 51:593-599.
91. Topinard, P. 1877. Des anomalies de nombre de la colonne vertébrale chez l'homme. Rev. Anthropol. 6:575-659.
92. Tubbs, R. S., E. G. Salter, and W. J. Oakes. 2006. Klippel-Feil anomaly with associated rudimentary cervical ribs in a human skeleton: case report and review of the literature. Folia (Warsz.) 65:92-94.
93. Van Duin, C. 2002. Hogere zuigelingensterfte in minder welvarende gebieden en onder niet-westerse allochtonen in Nederland. Maandstatistiek van de bevolking, CBS (Central Registry for Statistics, the Netherlands) 50:4-6.
94. Venables, W. N., and B. D. Ripley. 2002. Modern applied statistics with S. 4th ed. Springer-Verlag, New York.
95. Vermot, J., and O. Pourquié 2005. Retinoic acid coordinates somitogenesis and left-right patterning in vertebrate embryos. Nature 435:215-220.
96. Vermot, J., J. Galleo Llamas, V. Fraulob, K. Niederreither, P. Chambon, and P. Dollé. 2005. Retinoic acid controls the bilateral symmetry of somite formation in the mouse embryo. Science 308:563-566.
97. Whittaker, L. R. 1957. The incidence of cervical rib in African patients. East Afr. Med. J. 34:144-147.
98. Yamamoto, M., N. Mine, K. Mochida, Y. Sakai, Y. Saijoh, C. Meno, and H. Hamada. 2003. Nodal signaling induces the midline barrier by activating NodalI expression in the lateral plate. Development 130:1794-1804.
99. Yang, X., D. Dormann, A. E. Muensterberg, and C. J. Weijer. 2002. Cell movement patterns during gastrulation in the chick are controlled by positive and negative chemotaxis mediated by FGF4 and FGF8. Dev. Cell 3:425-437.
100. Zakany, J., M. Kmita, P. Alarcon, J. L. de la Pompa, and D. Duboule. 2001. Localized and transient transcription of Hox genes suggests a link between patterning and the segmentation clock. Cell 106:207-217.