Biological Theory

, Volume 6, Issue 1, pp 4–15 | Cite as

Animal Development, an Open-Ended Segment of Life

  • Alessandro Minelli
Original Paper


No comprehensive theory of development is available yet. Traditionally, we regard the development of animals as a sequence of changes through which an adult multicellular animal is produced, starting from a single cell which is usually a fertilized egg, through increasingly complex stages. However, many phenomena that would not qualify as developmental according to these criteria would nevertheless qualify as developmental in that they imply nontrivial (e.g., non degenerative) changes of form, and/or substantial changes in gene expression. A broad, comparative approach is badly needed. In the Cnidaria, for example, even the boundary between generations is problematic. Describing their life cycle in terms of metagenesis (alternation between polyp generation and medusa generation) or in terms of metamorphosis (polyp as larva or juvenile) are matters of semantics more than biology. The life cycle of other metazoans, described in textbooks in terms of larva-to-adult metamorphosis, is hardly different from a typical metagenetic life cycle of cnidarians. This applies to holometabolous insects and to marine invertebrates like sea urchins, where most of the larval cells are discarded at metamorphosis. The uncertain temporal and spatial boundaries of individual development are also shown by the widespread lack of a strict correspondence between adult and mature. A comprehensive theory of development should start with a zero principle of “developmental inertia,” corresponding to an indeterminate local self-perpetuation of cell-level dynamics. Indeterminate growth, scale-invariance, segmentation, and regeneration provide examples of developmental dynamics close to that.


Adult Adultocentrism Larva Metagenesis Metamorphosis Theory of development Zero model of development 



My sincere thanks to Thomas Pradeu for inviting me to contribute to this Thematic Section. To Thomas, as well as to Lucie Laplane and Antonine Nicoglou, I am much indebted for insightful comments on an earlier version of this article. Jean-Jacques Kupiec has kindly shared with me his views on inertial systems.


  1. Alberch P (1991) From genes to phenotype: dynamical systems and evolvability. Genetica 84:5–11CrossRefGoogle Scholar
  2. Bely AE (2010) Evolutionary loss of animal regeneration: pattern and process. Integr Comp Biol 50:515–527CrossRefGoogle Scholar
  3. Birnbaum KD, Sánchez Alvarado A (2008) Slicing across kingdoms: regeneration in plants and animals. Cell 132:697–710CrossRefGoogle Scholar
  4. Bouillon J, Gravili C, Pagès F, Gili JM, Boero F (2006) An introduction to Hydrozoa. Mémoires du Muséum national d’Histoire naturelle, vol 194. Muséum National d’Histoire Naturelle, ParisGoogle Scholar
  5. Boyden A, Shelswell EM (1959) Prophylogeny: some considerations regarding primitive evolution in lower Metazoa. Acta Biotheor 13:115–130CrossRefGoogle Scholar
  6. Brien P (1973) Les démosponges. Morphologie et reproduction. In: Grassé PP (ed) Traité de Zoologie, vol 3(1). Masson, Paris, pp 133–461Google Scholar
  7. Brown FD, Tiozzo S, Roux MM, Ishizuka K, Swalla BJ, De Tomaso AW (2009) Early lineage specification of long-lived germline precursors in the colonial ascidian Botryllus schlosseri. Development 136:3485–3494CrossRefGoogle Scholar
  8. Callebaut W, Rasskin-Gutman D (2005) Modularity: understanding the development and evolution of natural complex systems. MIT Press, Cambridge, MAGoogle Scholar
  9. Cardona A, Hartenstein V, Romero R (2005) The embryonic development of the triclad Schmidtea polychroa. Dev Genes Evol 215:109–131CrossRefGoogle Scholar
  10. Carter CA, Wourms JP (1993) Naturally occurring diblastodermic eggs in the annual fish Cynolebias: implications for developmental regulation and determination. J Morphol 215:301–312CrossRefGoogle Scholar
  11. Chagas A Jr, Edgecombe GD, Minelli A (2008) Variability in trunk segmentation in the centipede order Scolopendromorpha: a remarkable new species of Scolopendropsis Brandt (Chilopoda: Scolopendridae) from Brazil. Zootaxa 1888:36–46Google Scholar
  12. Dawydoff C (1928) Traité d’embryologie comparée des invertébrés. Masson, ParisGoogle Scholar
  13. Dupré J (2010) The polygenomic organism. Sociol Rev 58(s1):19–31CrossRefGoogle Scholar
  14. Eaves AA, Palmer AR (2003) Widespread cloning in echinoderm larvae. Nature 425:146CrossRefGoogle Scholar
  15. Egger B, Ladurner P, Nimeth K, Gschwentner R, Rieger R (2006) The regeneration capacity of the flatworm Macrostomum lignano—on repeated regeneration, rejuvenation, and the minimal size needed for regeneration. Dev Genes Evol 216:565–577CrossRefGoogle Scholar
  16. Ellis CH, Fausto-Sterling A (1997) Platyhelminths, the flatworms. In: Gilbert SF, Raunio AM (eds) Embryology: constructing the organism. Sinauer Associates, Sunderland, MA, pp 115–130Google Scholar
  17. Extavour CGM (2008) Urbisexuality: The evolution of bilaterian germ cell specification and reproductive systems. In: Minelli A, Fusco G (eds) Evolving pathways: key themes in evolutionary developmental biology. Cambridge University Press, Cambridge, pp 321–342CrossRefGoogle Scholar
  18. Extavour CG, Akam M (2003) Mechanisms of germ cell specification across the metazoans: epigenesis and preformation. Development 130:5869–5884CrossRefGoogle Scholar
  19. Fairclough SR, Dayel MJ, King N (2010) Multicellular development in a choanoflagellate. Curr Biol 20:R875–R876CrossRefGoogle Scholar
  20. Foe VE (1989) Mitotic domains reveal early commitment of cells in Drosophila embryos. Development 107:1–22Google Scholar
  21. Folse HJ, Roughgarden J (2010) What is an individual organism? A multilevel selection perspective. Q Rev Biol 85:447–472CrossRefGoogle Scholar
  22. Franc A (1993) Classe des Scyphozoaires. In: Grassé PP (ed) Traité de zoologie, vol 3(2). Masson, Paris, pp 597–884Google Scholar
  23. Fryer G (1961) The developmental history of Mutela bourguignati (Ancey) Bourguignat (Mollusca: Bivalvia). Philos Trans R Soc Lond B 244:259–298CrossRefGoogle Scholar
  24. Fusco G (2005) Trunk segment numbers and sequential segmentation in myriapods. Evol Dev 7:608–617CrossRefGoogle Scholar
  25. Fusco G, Minelli A (2010) From polyphenism to complex metazoan life cycles. Philos Trans R Soc B 365:545–690CrossRefGoogle Scholar
  26. Galaktionov KV, Dobrovolskij AA (2003) The biology and evolution of trematodes. An essay on the biology, morphology, life cycles, and evolution of digenetic trematodes. Kluwer Academic, DordrechtGoogle Scholar
  27. Garcia-Bellido A, Ripoll P, Morata G (1973) Developmental compartmentalisation of the wing disc of Drosophila. Nat New Biol 245:251–253CrossRefGoogle Scholar
  28. García-Ruiz JM, Checa A, Rivas A (1990) On the origin of ammonite sutures. Paleobiology 16:349–354Google Scholar
  29. Gayon J (1992) Darwin et l’après-Darwin: une histoire de l’hypothèse de sélection naturelle. Kimé, ParisGoogle Scholar
  30. Gayon J (1998) Darwinism’s struggle for survival. Cambridge University Press, CambridgeGoogle Scholar
  31. Gerhart JC, Kirschner MW (1997) Cells, embryos and evolution. Blackwell Science, BostonGoogle Scholar
  32. Glenner H, Høeg JT (1995) A new motile, multicellulars stage involved in host invasion by parasitic barnacles (Rhizocephala). Nature 377:147–150CrossRefGoogle Scholar
  33. Glenny RW, Robertson HT (1990) Fractal properties of pulmonary blood flow: characterization of spatial heterogeneity. J Appl Physiol 69:532–545Google Scholar
  34. Grosberg RK, Strathmann RR (1998) One cell, two cell, red cell, blue cell: the persistence of a unicellular stage in multicellular life histories. Trends Ecol Evol 13:112–116CrossRefGoogle Scholar
  35. Guthrie S, Prince V, Lumsden A (1993) Selective dispersal of avian rhombomere cells in orthotopic and heterotopic grafts. Development 118:527–538Google Scholar
  36. Hall BK (1998) Germ layers and the germ-layer theory revisited: primary and secondary germ layers, neural crest as a fourth germ layer, homology, demise of the germ-layer theory. Evol Biol 30:121–186Google Scholar
  37. Hall BK (1999) The neural crest in development and evolution. Springer, New YorkGoogle Scholar
  38. Hallez P (1887) Embryogénie des dendrocoeles d’eau douce. Baillière, ParisCrossRefGoogle Scholar
  39. Hobbs HH Jr (1981) The crayfishes of Georgia. Smithson Contrib Zool 318:1–549CrossRefGoogle Scholar
  40. Jacobs DK, Hughes NC, Fitz-Gibbon ST, Winchell CJ (2005) Terminal addition, the Cambrian radiation and the Phanerozoic evolution of bilaterian form. Evol Dev 7:498–514CrossRefGoogle Scholar
  41. Janssen R, Prpic NM, Damen WGM (2004) Gene expression suggests decoupled dorsal and ventral segmentation in the millipede Glomeris marginata (Myriapoda: Diplopoda). Dev Biol 268:89–104CrossRefGoogle Scholar
  42. Karkach AS (2006) Trajectories and models of individual growth. Demogr Res 15:347–400CrossRefGoogle Scholar
  43. Keller EF (2000) The century of the gene. Harvard University Press, Cambridge, MAGoogle Scholar
  44. Kupiec J-J (2009) The origins of individuals. World Scientific, SingaporeCrossRefGoogle Scholar
  45. Laplane L (2011) Stem cells and the temporal boundaries of development: toward a species-dependent view. Biol Theory 6. doi: 10.1007/s13752-011-0009-z
  46. Lauzon RJ, Ishizuka KJ, Weissman IL (2002) Cyclical generation and degeneration of organs in a colonial urochordate involves crosstalk between old and new: a model for development and regeneration. Dev Biol 249:333–348CrossRefGoogle Scholar
  47. Littlewood DTJ, Rohde K, Clough KA (1999) The interrelationships of all major groups of Platyhelminthes: phylogenetic evidence from morphology and molecules. Biol J Linn Soc 66:75–114CrossRefGoogle Scholar
  48. Long CA (2005) Intricate sutures as fractal curves. J Morphol 185:285–295CrossRefGoogle Scholar
  49. Loughry WJ, Prodohl PA, McDonough CM, Avise JC (1998) Polyembryony in armadillos. Am Sci 86:274–279Google Scholar
  50. Manni L, Burighel P (2006) Common and divergent pathways in alternative developmental processes of ascidians. BioEssays 28:902–912CrossRefGoogle Scholar
  51. McShea DW, Brandon RN (2010) Biology’s first law: the tendency for diversity and complexity to increase in evolutionary systems. The University of Chicago Press, ChicagoGoogle Scholar
  52. Metzger RJ, Klein OD, Martin GR, Krasnow MA (2008) The branching programme of mouse lung development. Nature 453:745–750CrossRefGoogle Scholar
  53. Michalik P, Uhl G (2005) The male genital system of the cellar spider Pholcus phalangioides (Fuesslin, 1775) (Pholcidae, Araneae): development of spermatozoa and seminal secretion. Front Zool 2:12CrossRefGoogle Scholar
  54. Minelli A (2000) Holomeric vs. meromeric segmentation: a tale of centipedes, leeches, and rhombomeres. Evol Dev 2:35–48CrossRefGoogle Scholar
  55. Minelli A (2001) A three-phase model of arthropod segmentation. Dev Genes Evol 211:509–521CrossRefGoogle Scholar
  56. Minelli A (2003) The development of animal form. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  57. Minelli A (2009a) Perspectives in animal phylogeny and evolution. Oxford University Press, OxfordGoogle Scholar
  58. Minelli A (2009b) Forms of becoming. Princeton University Press, PrincetonGoogle Scholar
  59. Minelli A (2011) A principle of developmental inertia. In: Hallgrímsson B, Hall BK (eds) Epigenetics: linking genotype and phenotype in development and evolution. University of California Press, San Francisco, pp 116–133Google Scholar
  60. Minelli A, Bortoletto S (1988) Myriapod metamerism and arthropod segmentation. Biol J Linn Soc 33:323–343CrossRefGoogle Scholar
  61. Minelli A, Fusco G (2004) Evo–devo perspectives on segmentation: model organisms, and beyond. Trends Ecol Evol 19:423–429CrossRefGoogle Scholar
  62. Minelli A, Chagas A Jr, Edgecombe GD (2009) Saltational evolution of trunk segment number in centipedes. Evol Dev 11:318–322CrossRefGoogle Scholar
  63. Nijhout HF (1990) Metaphors and the role of genes in development. BioEssays 12:441–446CrossRefGoogle Scholar
  64. Nikolei E (1961) Vergleichende Untersuchungen zur Fortpflanzung der heterogenen Gallmücken unter experimentellen Bedingungen. Z Morphol Okol Tiere 50:281–329CrossRefGoogle Scholar
  65. Pandian TJ (1994) Arthropoda-Crustacea. In: Adiyodi KG, Adiyodi RG (eds) Reproductive biology of invertebrates, VI(B) Asexual propagation and reproductive strategies. Wiley, Chichester, pp 39–166Google Scholar
  66. Peterson KJ, Cameron RA, Davidson EH (1997) Set-aside cells in maximal indirect development: evolutionary and developmental significance. BioEssays 19:623–631CrossRefGoogle Scholar
  67. Pigliucci M (2001) Phenotypic plasticity: beyond nature and nurture. The Johns Hopkins University Press, BaltimoreGoogle Scholar
  68. Pigliucci M, Müller GB (eds) (2010) Evolution: the extended synthesis. MIT Press, CambridgeGoogle Scholar
  69. Pollock DA, Normark BB (2002) The life cycle of Micromalthus debilis LeConte (1878) (Coleoptera: Archostemata: Micromalthidae): historical review and evolutionary perspective. J Zool Syst Evol Res 40:105–112CrossRefGoogle Scholar
  70. Pradeu T (2010) What is an organism? An immunological answer. Hist Philos Life Sci 32:247–268Google Scholar
  71. Sahli F (1990) On post-adult moults in Julida (Myriapoda, Diplopoda). Why do periodomorphosis and intercalaries occur in males? In: Minelli A (ed) Proceedings of the 7th international congress of myriapodology. Brill, Leiden, pp 135–156Google Scholar
  72. Samakovlis C, Hacohen N, Manning G, Sutherland DC, Guillemin K, Krasnow MA (1996) Development of the Drosophila tracheal system occurs by a series of morphologically distinct but genetically coupled branching events. Development 122:1395–1407Google Scholar
  73. Santelices B (1999) How many kinds of individual are there? Trends Ecol Evol 14:152–155CrossRefGoogle Scholar
  74. Schlosser G (2002) Modularity and the units of evolution. Theory Biosci 121:1–80CrossRefGoogle Scholar
  75. Schlosser G, Wagner GP (eds) (2004) Modularity in development and evolution. University of Chicago Press, ChicagoGoogle Scholar
  76. Sebens KP (1987) The ecology of indeterminate growth in animals. Ann Rev Ecol Syst 18:371–407CrossRefGoogle Scholar
  77. Song JL, Wong JL, Wessel GM (2006) Oogenesis: single cell development and differentiation. Dev Biol 300:385–405CrossRefGoogle Scholar
  78. Soto AM, Sonnenschein C (2004) The somatic mutation theory of cancer: growing problems with the paradigm? BioEssays 26:1097–1107CrossRefGoogle Scholar
  79. Steenstrup JJS (1845) On the alternation of generation or the propagation and development of animals through alternate generations. Ray Society, LondonGoogle Scholar
  80. Surhone LM, Timpledon MT, Marseken SF (2010) Paedogenesis. VDM, SaarbrückenGoogle Scholar
  81. Tattersall WM, Sheppard EM (1934) Observations on the bipinnaria of the asteroid genus Luidia. In: Daniel RJ (ed) James Johnstone memorial volume. University Press of Liverpool, Liverpool, pp 35–61Google Scholar
  82. Verhoeff KW (1923) Periodomorphose. Zool Anz 56(233–238):241–254Google Scholar
  83. Vervoort M (2011) Regeneration and development in animals. Biol Theory 6. doi: 10.1007/s13752-011-0005-3
  84. West-Eberhard MJ (2003) Developmental plasticity and evolution. Oxford University Press, New YorkGoogle Scholar
  85. Williamson DJ (2006) Hybridization in the evolution of animal form and life-cycle. Biol J Linn Soc 148:585–602Google Scholar
  86. Wolpert L, Jessell T, Lawrence P, Meyerowitz E, Robertson E, Smith J (2007) Principles of development. Oxford University Press, OxfordGoogle Scholar
  87. Wyatt IJ (1961) Pupal paedogenesis in the Cecidomyidae (Diptera) I. Proc R Entomol Soc Lond A 36:133–143Google Scholar
  88. Wyatt IJ (1964) Immature stages of Lestremiinae (Diptera: Cecidomyidae) infesting cultivated mushrooms. Trans R Entomol Soc Lond 116:15–27CrossRefGoogle Scholar
  89. Zamir M (2001) Fractal dimensions and multifractility in vascular branching. J Theor Biol 212:183–190CrossRefGoogle Scholar
  90. Zattara EE, Bely AE (2011) Evolution of a novel developmental trajectory: fission is distinct from regeneration in the annelid Pristina leidyi. Evol Dev 13:80–95CrossRefGoogle Scholar
  91. Zhurov V, Terzin T, Grbić M (2007) (In)discrete charm of the polyembryony: evolution of embryo cloning. Cell Mol Life Sci 64:2790–2798CrossRefGoogle Scholar

Copyright information

© Konrad Lorenz Institute 2011

Authors and Affiliations

  1. 1.Department of BiologyUniversity of PaduaPaduaItaly

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