Skip to main content
SpringerLink
Log in

From Haeckel to event-pairing: the evolution of developmental sequences

  • Published:
Theory in Biosciences Aims and scope Submit manuscript

Summary

Development involves a series of developmental events, separated by transformations, that follow a particular order or developmental sequence. The sequence may in turn be arbitrarily subdivided into contiguous segments (developmental stages). We discuss the properties of developmental sequences. We also examine the differing analytical approaches that have been used to analyse developmental sequences in an evolutionary context. Ernst Haeckel was a pioneer in this field. His approach was evolutionary and he introduced the idea of sequence heterochrony (evolutionary changes in the sequence of developmental events). Despite the availability of detailed developmental data (e.g. Franz Keibel’s ‘Normal Tables’), Haeckel was unable to undertake a quantitative analysis of developmental data. This is now possible through computer-based analytical techniques such as event-pairing, which can extract important biological information from developmental sequences by mapping them onto established phylogenies. It may also yield data that can be used in phylogeny reconstruction, although the inherent ‘non-independence’ of the data may make this invalid. In future, the methods discussed here may be applied to the analysis of patterns of gene expression in embryos, or adapted to studying gene order on chromosomes.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Abraham, K. (1901) Beiträge zur Entwicklungsgeschichte des Wellensittichs (Melopsittacus undulatus). Anat. Hefte 17: 589–669.

    Article  Google Scholar 

  • Alberch, P. (1985) Problems with the interpretation of developmental sequences. Syst. Zool. 34: 46–58.

    Article  Google Scholar 

  • Baker, C. V. H., Bronner-Fraser, M. (2001) Vertebrate cranial placodes. I. Embryonic induction. Dev. Biol. 232: 1–61.

    Article  PubMed  CAS  Google Scholar 

  • Ballard, W. W. (1964) Comparative anatomy and embryology, Ronald Press, New York.

    Google Scholar 

  • Beard, J. (1896) On certain problems of vertebrate embryology. Gustav Fischer. Jena.

    Google Scholar 

  • Bellairs, R., Osmond, M. (1998) The atlas of chick development. Academic Press. San Diego.

    Google Scholar 

  • Chipman, A. D., Haas A., Tchernov E., Khaner O. (2000) Variation in anuran embryogenesis: differences in sequence and timing of early developmental events. J. Exp. Zool. 288: 352–365.

    Article  PubMed  CAS  Google Scholar 

  • Colbert, M. W., Rowe, T. (2001) Ontogenetic sequence analysis: using parsimony to characterize developmental hirearchies. J. Morphol. 248: 218.

    Google Scholar 

  • de Lange, D., Nierstrasz, H. F. (1932) Tabellarische Übersicht der Entwicklung von Tupaia javanica Horsf. Oosthoek Verlag. Utrecht.

    Google Scholar 

  • Dettlaff, T. A., Dettlaff, A. A. (1961) On relative dimensionless characteristics of the development duration in embryology. Arch. Biol. (Liege) 72: 1–16.

    CAS  Google Scholar 

  • Duellman, W. E., Trueb, L. (1994) Biology of amphibians. Johns Hopkins University Press. Baltimore.

    Google Scholar 

  • Eycleshymer, A. C., Wilson, J. A. (1910) Normal plates of the development of Necturus maculosus. Gustav Fischer Verlag. Jena.

    Google Scholar 

  • Ferguson, M. W. J. (1985) Reproductive biology and embryology of crocodilians. In: Gans, C., Billett, F. (eds) Biology of the Reptilia. Wiley. New York. pp. 329–491.

    Google Scholar 

  • Glaesner, L. (1925) Normentafeln zur Entwicklungsgeschichte des gemeinen Wassermolchs (Molge vulgaris). Gustav Fischer Verlag. Jena.

    Google Scholar 

  • Gould, S. J. (1977) Ontogeny and phylogeny. Belknap Press. Cambridge, Massachusetts.

    Google Scholar 

  • Gould, S. J. (1982) Change in developmental timing as a mechanism of macroevolution. In: Bonner, J. T. (ed.) Evolution and development. Springer. Berlin. pp. 333–346.

    Google Scholar 

  • Grandel, H., Merker, S. S. (1998) The development of the paired fins in the zebrafish (Danio rerio). Mech. Devel. 79: 99–120.

    Article  CAS  Google Scholar 

  • Gribnau, A. A. M., Geijsberts, L. G. M. (1981) Developmental stages in the Rhesus monkey (Macaca mulatta). Springer. Berlin.

    Google Scholar 

  • Grosser, O., Tandler, J. (1909) Normentafel zur Entwicklungsgeschichte des Kiebitzes (Vanellus cristatus Meyer). Gustav Fischer. Jena.

    Google Scholar 

  • Haeckel, E. (1910) The evolution of man. Watts & Co. London.

    Google Scholar 

  • Hall, B. K., Miyake, T. (1995) How do embryos measure time? In: McNamara, K. J. (ed.) Evolutionary Change and Heterochrony. Wiley. New York. pp. 3–20.

    Google Scholar 

  • Hamburger, V., Hamilton, H. L. (1951) A series of normal stages in the development of the chick embryo. J. Morphol. 88: 49–92.

    Article  Google Scholar 

  • Henneberg, B. (1937) Normentafeln zur Entwicklungsgeschichte der Wanderratte (Rattus norvegicus Erxleben). Gustav Fischer. Jena.

    Google Scholar 

  • His, W. (1880) Die Anatomie menschlicher Embryonen. Vogel. Leipzig.

    Book  Google Scholar 

  • Hubrecht, A. A., Keibel, F. (1907) Normentafeln zur Entwicklungsgeschichte des Koboldmaki (Tarsius spectrum) und des Plumplori (Nycticebus tardigradus). Gustav Fischer. Jena.

    Google Scholar 

  • Huisman, F. J., de Lange, D. (1937) Tabellarische Übersicht der Entwicklung von Manis javanica Desm. Oosthoek Verlag. Utrecht.

    Google Scholar 

  • Jeffery, J. E., Bininda-Emonds, O. R. P., Coates, M. I., Richardson, M. K. (2002a) Analyzing evolutionary patterns in amniote embryonic development. Evol. Dev.

  • Jeffery, J. E., Richardson, M. K., Coates, M. I., Bininda-Emonds, O. R. P. (2002b). Analyzing developmental sequences within a phylogenetic framework. Syst. Biol.

  • Keibel, F. (1895) Normentafel zur Entwicklungsgeschichte der Wirbeltiere. Anat. Anz. 11: 255–234.

    Google Scholar 

  • Keibel, F. (1897) Normentafel zur Entwicklungsgeschichte des Schweines (Sus scrofa domesticus). Gustav Fischer. Jena.

    Google Scholar 

  • Keibel, F. (1897–1938) Normentafeln zur Entwicklungsgeschichte der Wirbelthiere. Gustav Fischer. Jena.

    Google Scholar 

  • Keibel, F., Abraham, K. (1900) Normentafel zur Entwicklungsgeschichte des Huhnes (Gallus domesticus). Gustav Fischer. Jena.

    Google Scholar 

  • Keibel, F., Elze, C. (1908) Normentafel zur Entwicklungsgeschichte des Menschen. Gustav Fischer. Jena.

    Google Scholar 

  • Kerr, J. G. (1909) Normal plates of the development of Lepidosiren paradoxa and Protopterus annectens. Gustav Fischer. Jena.

    Google Scholar 

  • Kimmel, C. B., Ballard, W. W., Kimmel, S. R., Ullmann, B., Schilling, T. F. (1995) Stages of embryonic development of the zebrafish. Dev. Dynam. 203: 253–310.

    CAS  Google Scholar 

  • Kitching, I. J., Forey, P. L., Humphries, C. J., Williams, D. M. (1998) Cladistics (2e). Oxford University Press. Oxford.

    Google Scholar 

  • Kopsch, F. R. (1952) Die Entwicklung des braunen Grasfrosches Rana fusca Roesel. Georg Thieme Verlag. Stuttgart.

    Google Scholar 

  • Kudô, T. (1938) Normentafeln zur Entwicklungsgeschichte des japanischen Riesensalamanders (Megalobatrachus japonicus Temminck). Gustav Fischer. Jena.

    Google Scholar 

  • Lauder, G. V. (1994) Homology, form, and function. In: Hall, B. K. (ed.) Homology: the hierarchical basis of comparative biology. Academic Press. San Diego. pp. 151–196.

    Google Scholar 

  • Li, Z., Joseph, N. M., Easter, S. S. (2000) The morphogenesis of the zebrafish eye, including a fate map of the optic vesicle. Dev. Dynam. 218: 175–188.

    Article  CAS  Google Scholar 

  • Lovejoy, C. O., Cohn, M. J., White, T. D. (1999) Morphological analysis of the mammalian postcranium: a developmental perspective. Proc. Natl. Acad. Sci. USA 96: 13247–13252.

    Article  PubMed  CAS  Google Scholar 

  • Mabee, P. M., Olmstead, K. L., Cubbage, C. C. (2000) An experimental study of intraspecific variation, developmental timing, and heterochrony in fishes. Evolution 54: 2091–2106.

    PubMed  CAS  Google Scholar 

  • Mabee, P. M., Trendler, T. A. (1996) Development of the cranium and paired fins in Betta splendens (Teleosti: Percomporpha): intraspecific variation and interspecific comparisons. J. Morphol. 227: 249–287.

    Article  Google Scholar 

  • McCrady, E. (1938) Embryology of the opossum. Amer. Anat. Mem. 16: 1–233.

    Google Scholar 

  • McKinney, M. L., McNamara, K. J. (1991) Heterochrony, the evolution of ontogeny. Plenum. New York.

    Google Scholar 

  • Minot, C. S., Taylor, E. (1905) Normal plates of the development of the rabbit (Lepus cuniculus L.). Gustav Fischer. Jena.

    Google Scholar 

  • Nieuwkoop, P. D., Faber, J. (1994) Normal Table of Xenopus laevis (Daudin) (2e). Garland Publishing. London.

    Google Scholar 

  • Nunn, C. L., Smith, K. K. (1998) Statistical analyses of developmental sequences: the craniofacial region in marsupial and placental mammals. Amer. Nat. 152: 82–101.

    Article  CAS  Google Scholar 

  • Oppel, A. (1891) Vergleichung des Entwicklungsgrades der Organe. Fischer. Jena.

    Google Scholar 

  • O’Rahilly, R. (1979) Early human development and the chief sources of information on staged human embryos. Europ. J. Obstet. Gynec. Reprod. Biol. 9: 273–280.

    Article  PubMed  CAS  Google Scholar 

  • O’Rahilly, R., Müller, F. (1987) Developmental stages in human embryos. Carnegie Institution. Washington.

    Google Scholar 

  • O’Rahilly, R., Müller, F. (2000) Prenatal ages and stages — measures and errors. Teratology 61: 382–384.

    Article  PubMed  CAS  Google Scholar 

  • Peter, K. (1904) Normentafel zur Entwicklungsgeschichte der Zauneidechse (Lacerta agilis). Gustav Fischer. Jena.

    Google Scholar 

  • Platnick, N. I., Griswold, C. E., Coddington, J. A. (1991) On missing entries in cladistic analysis. Cladistics 7: 337–343.

    Article  Google Scholar 

  • Richardson, M. K. (1995) Heterochrony and the phylotypic period. Dev. Biol. 172: 412–421.

    Article  PubMed  CAS  Google Scholar 

  • Richardson, M. K. (1999) Vertebrate evolution: the developmental origins of adult variation. BioEssays 21: 604–613.

    Article  PubMed  CAS  Google Scholar 

  • Richardson, M. K., Allen, S. P., Wright, G. M., Raynaud, A., Hanken, J. (1998) Somite number and vertebrate evolution. Development 125: 151–160.

    PubMed  CAS  Google Scholar 

  • Richardson, M. K., Keuck, G. (in press) Haeckel’s ABC of evolution and development. Biol. Rev.

  • Richardson, M. K., Narraway, J. (1999) A treasure house of comparative embryology. Int. J. Dev. Biol. 43: 591–602.

    PubMed  CAS  Google Scholar 

  • Sakurai, T. (1906) Normentafel zur Entwicklungsgeschichte des Rehes (Cervus capreolus). Gustav Fischer. Jena.

    Google Scholar 

  • Scammon, R. E. (1911) Normal plates of the development of Squalus acnathias. Gustav Fischer. Jena.

    Google Scholar 

  • Schlosser, G. (2001) Using heterochrony plots to detect the dissociated coevolution of characters. J. Exp. Zool. (Mol. Dev. Evol.) 291: 282–304.

    Article  CAS  Google Scholar 

  • Scott, J. P. (1937) The embryology of the guinea pig. Amer. J. Anat. 60: 397–432.

    Article  Google Scholar 

  • Semon, R. (1901) Normentafeln zur Entwicklungsgeschichte des Ceratodus forsteri. Gustav Fischer. Jena.

    Google Scholar 

  • Smith, A. B. (1994) Systematics and the fossil record. Blackwell Scientific. London.

    Google Scholar 

  • Smith, K. K. (1996) Integration of craniofacial structures during development in mammals. Amer. Zool. 36: 70–79.

    Google Scholar 

  • Smith, K. K. (1997) Comparative patterns of craniofacial development in eutherian and metatherian mammals. Evolution 51: 1663–1678.

    Article  Google Scholar 

  • Smith, K. K. (2001) Heterochrony revisited: the evolution of developmental sequences. Biol. J. Linn. Soc. 73: 169–186.

    Article  Google Scholar 

  • Streeter, G. L. (1949) Developmental horizons in human embryology (fourth issue). A review of the histogenesis of cartilage and bone. Contrib. Embryol. 33: 149–169.

    PubMed  CAS  Google Scholar 

  • Swofford, D. L. (2001) PAUP*. Phylogenetic analysis using parsimony (*and other methods) (v.4). Sinauer Associates. Sunderland, Massachusetts.

    Google Scholar 

  • Tabin, C. J., Johnson, R. L. (2001) Clocks and Hox. Nature 412: 780–781.

    Article  PubMed  CAS  Google Scholar 

  • Tavolga, W. N. (1949) Embryonic development of the Platyfish (Platpoecilus), the swordtail (Xiphophorus) and their hybrids. Bull. AMNH 94: 165–229.

    Google Scholar 

  • Theiler, K. (1989) The house mouse: atlas of embryonic development. Springer. New York.

    Google Scholar 

  • Townsend, D. S., Stewart, M. M. (1985) Direct development in Eleutherodactylus coqui (Anura: Leptodactylidae): a staging table. Copeia 1985: 423–436.

    Article  Google Scholar 

  • Velhagen, W. A. (1997) Analyzing developmental sequences using sequence units. Syst. Biol. 46: 204–210.

    Article  PubMed  Google Scholar 

  • Velhagen, W. A., Savitzky, A. H. (1998) Evolution of embryonic growth in thamnophiine snakes. Copeia 1998: 549–558.

    Article  Google Scholar 

  • Völker, O. (1922) Normentafel zur Entwicklungsgeschichte des Ziesels (Spermophilus citillus). Gustav Fischer. Jena.

    Google Scholar 

  • Wheeler, Q. D. (1990) Ontogeny and character phylogeny. Cladistics 6: 225–268.

    Article  Google Scholar 

  • Wiens, J. J. (1995) Polymorphic characters in phylogenetic systematics. Syst. Biol. 44: 482–500.

    Article  Google Scholar 

  • Witschi, E. (1956) Development of vertebrates. Saunders. Philadelphia.

    Google Scholar 

  • Wray, G. A., Raff, R. A. (1990) Pattern and process heterochronies in the early development of sea urchins. Semin. Dev. Biol. 1: 245–251.

    Google Scholar 

Download references

Author information

Author notes

  1. Olaf R. P. Bininda-Emonds

    Present address: Lehrstuhl für Tierzucht, Technical University of Munich, Alte Akademie 12, 85354, Freising-Weihenstephan, Germany

Authors and Affiliations

  1. Institute of Evolutionary and Ecological Sciences, Leiden University, Kaiserstraat 63, P.O. Box 9516, 2300 RA, Leiden, The Netherlands

    Olaf R. P. Bininda-Emonds, Jonathan E. Jeffery & Michael K. Richardson

  2. Department of Organismal Biology & Anatomy, University of Chicago, 1027 East 57th Street, 60637-1508, Chicago, Illinois, USA

    Michael I. Coates

Authors
  1. Olaf R. P. Bininda-Emonds
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jonathan E. Jeffery
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Michael I. Coates
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Michael K. Richardson
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Olaf R. P. Bininda-Emonds.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Bininda-Emonds, O.R.P., Jeffery, J.E., Coates, M.I. et al. From Haeckel to event-pairing: the evolution of developmental sequences. Theory Biosci. 121, 297–320 (2002). https://doi.org/10.1007/s12064-002-0016-5

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12064-002-0016-5

Key words

Search

Navigation