Inverting the hourglass: Quantitative evidence against the phylotypic stage in vertebrate development

Proceedings of the Royal Society B: Biological Sciences

Volumn 270, Issue 1513, 2003, Pages 341-346

  Bininda Emonds, Olaf R P ^a,b   Jeffery, Jonathan E ^a   Richardson, Michael K ^a  

^a LEIDEN UNIVERSITY   (Netherlands)

^b TECHNICAL UNIVERSITY OF MUNICH   (Germany)

Author keywords

Development; Developmental modules; Heterochrony; Phenotypic variation; Phylotypic stage; Vertebrates

Indexed keywords

DEVELOPMENTAL BIOLOGY; HETEROCHRONY (ONTOGENY); PHENOTYPIC PLASTICITY; VERTEBRATE;

ARTICLE; BIODIVERSITY; CONTROLLED STUDY; DEVELOPMENTAL BIOLOGY; DEVELOPMENTAL STAGE; EVOLUTION; MAMMAL; NONHUMAN; PHENOTYPIC VARIATION; PREDICTION; PRIORITY JOURNAL; VERTEBRATE;

MAMMALIA; VERTEBRATA;

EID: 0037460684     PISSN: 09628452     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rspb.2002.2242     Document Type: Article

References (30)

1. Abouheif, E., Akam, M., Dickinson, W. J., Holland, P. W., Meyer, A., Patel, N. H., Raff, R. A., Roth, V. L. & Wray, G. A. 1997 Homology and developmental genes. Trends Genet. 13, 432-433.
2. Anderson, D. T. 1973 Embryology and phylogeny in annelids and arthropods. International series of monographs in pure and applied biology. Division: Zoology. Oxford: Pergamon.
3. Ballard, W. W. 1981 Morphogenetic movements and fate maps of vertebrates. Am. Zool. 21, 391-399.
4. Bininda-Emonds, O. R. P., Jeffery, J. E., Coates, M. I. & Richardson, M. K. 2002 From Haeckel to event-pairing: the evolution of developmental sequences. Theory Biosci. 121, 297-320.
5. Cohen, J. 1967 Living embryos: an introduction to the study of animal development. Oxford: Pergamon.
6. Cohen, J. 1993 Development of the zootype. Nature 363, 307.
7. Collazo, A. 2000 Developmental variation, homology, and the pharyngula stage. Syst. Biol. 49, 3-18.
8. de Beer, G. 1971 Homology: an unsolved problem. Oxford biology readers. Oxford University Press.
9. Duboule, D. 1994 Temporal colinearity and the phylotypic progression: a basis for the stability of a vertebrate Bauplan and the evolution of morphologies through heterochrony. Development (Suppl.), 135-142.
10. Galis, F. & Metz, J. A. J. 2001 Testing the vulnerability of the phylotypic stage: on modularity and evolutionary conservation. J. Exp. Zool. 291, 195-204.
11. Galis, F., van Alphen, J. J. M. & Metz, J. A. J. 2001 Why five fingers? Evolutionary constraints on digit numbers. Trends Ecol. Evol. 16, 637-646.
12. Gould, S. J. 1977 Ontogeny and phylogeny. Cambridge, MA: Belknap.
13. Gould, S. J. 1982 Change in developmental timing as a mechanism of macroevolution. In Evolution and development (ed. J. T. Bonner), pp. 333-346. New York: Springer.
14. Hall, B. K. 1996 Baupläne, phylotypic stages, and constraint - why are there so few types of animals? Evol. Biol. 29, 251-261.
15. Hall, B. K. 1997 Phylotypic stage or phantom: is there a highly conserved embryonic stage in vertebrates? Trends Ecol. Evol. 12, 461-463.
16. Jeffery, J. E., Bininda-Emonds, O. R. P., Coates, M. I. & Richardson, M. K. 2002 Analyzing evolutionary patterns in vertebrate embryonic development. Evol. Dev. 4, 292-302.
17. Kimmel, C. B., Ballard, W. W., Kimmel, S. R., Ullmann, B. & Schilling, T. F. 1995 Stages of embryonic development of the zebrafish. Devl Dynam. 203, 253-310.
18. Needham, J. 1950 Biochemistry and morphogenesis. Cambridge University Press.
19. Raff, R. A. 1996 The shape of life: genes, development, and the evolution of animal form. University of Chicago Press.
20. Richardson, M. K. 1995 Heterochrony and the phylotypic period. Devl Biol. 172, 412-421.
21. Richardson, M. K. 1999 Vertebrate evolution: the developmental origins of adult variation. BioEssays 21, 604-613.
22. Richardson, M. K. & Keuck, G. 2002 Haeckel's ABC of evolution and development. Biol. Rev. 77, 495-528.
23. Richardson, M. K., Hanken, J., Gooneratne, M. L., Pieau, C., Raynaud, A., Selwood, L. & Wright, G. M. 1997 There is no highly conserved embryonic stage in the vertebrates: implications for current theories of evolution and development. Anat. Embryol. 196, 91-106.
24. Rougvie, A. E. 2001 Control of developmental timing in animals. Nature Rev. Genet. 2, 690-701.
25. Sander, K. 1983 The evolution of patterning mechanisms: gleanings from insect embryogenesis and spermatogenesis. In Development and evolution (ed. B. C. Goodwin, N. Holder & C. C. Wylie), pp. 137-159. Cambridge University Press.
26. Seidel, F. 1960 Körpergrundgestalt und Keimstruktur eine Erörterung über die Grundlagen der vergleichenden und experimentellen Embryologie und deren Gültigkeit bei phylogenetischen Überlegungen. Zool. Anz. 164, 245-305.
27. Slack, J. M., Holland, P. W. & Graham, C. F. 1993 The zootype and the phylotypic stage. Nature 361, 490-492.
28. Wagner, G. P. 1996 Homologues, natural kinds and the evolution of modularity. Am. Zool. 36, 36-43.
29. Wagner, G. P. & Misof, B. Y. 1993 How can a character be developmentally constrained despite variation in developmental pathways? J. Evol. Biol. 6, 449-455.
30. Yost, H. J. 1999 Diverse initiation in a conserved left-right pathway? Curr. Opin. Genet. Dev. 9, 422-426.