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Animal Development, an Open-Ended Segment of Life

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Abstract

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.

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References

  • Alberch P (1991) From genes to phenotype: dynamical systems and evolvability. Genetica 84:5–11

    Article  Google Scholar 

  • Bely AE (2010) Evolutionary loss of animal regeneration: pattern and process. Integr Comp Biol 50:515–527

    Article  Google Scholar 

  • Birnbaum KD, Sánchez Alvarado A (2008) Slicing across kingdoms: regeneration in plants and animals. Cell 132:697–710

    Article  Google Scholar 

  • 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, Paris

    Google Scholar 

  • Boyden A, Shelswell EM (1959) Prophylogeny: some considerations regarding primitive evolution in lower Metazoa. Acta Biotheor 13:115–130

    Article  Google Scholar 

  • Brien P (1973) Les démosponges. Morphologie et reproduction. In: Grassé PP (ed) Traité de Zoologie, vol 3(1). Masson, Paris, pp 133–461

    Google Scholar 

  • 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 136:3485–3494

    Article  Google Scholar 

  • Callebaut W, Rasskin-Gutman D (2005) Modularity: understanding the development and evolution of natural complex systems. MIT Press, Cambridge, MA

    Google Scholar 

  • Cardona A, Hartenstein V, Romero R (2005) The embryonic development of the triclad Schmidtea polychroa. Dev Genes Evol 215:109–131

    Article  Google Scholar 

  • Carter CA, Wourms JP (1993) Naturally occurring diblastodermic eggs in the annual fish Cynolebias: implications for developmental regulation and determination. J Morphol 215:301–312

    Article  Google Scholar 

  • 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 1888:36–46

    Google Scholar 

  • Dawydoff C (1928) Traité d’embryologie comparée des invertébrés. Masson, Paris

    Google Scholar 

  • Dupré J (2010) The polygenomic organism. Sociol Rev 58(s1):19–31

    Article  Google Scholar 

  • Eaves AA, Palmer AR (2003) Widespread cloning in echinoderm larvae. Nature 425:146

    Article  Google Scholar 

  • 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 216:565–577

    Article  Google Scholar 

  • Ellis CH, Fausto-Sterling A (1997) Platyhelminths, the flatworms. In: Gilbert SF, Raunio AM (eds) Embryology: constructing the organism. Sinauer Associates, Sunderland, MA, pp 115–130

    Google Scholar 

  • 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 321–342

    Chapter  Google Scholar 

  • Extavour CG, Akam M (2003) Mechanisms of germ cell specification across the metazoans: epigenesis and preformation. Development 130:5869–5884

    Article  Google Scholar 

  • Fairclough SR, Dayel MJ, King N (2010) Multicellular development in a choanoflagellate. Curr Biol 20:R875–R876

    Article  Google Scholar 

  • Foe VE (1989) Mitotic domains reveal early commitment of cells in Drosophila embryos. Development 107:1–22

    Google Scholar 

  • Folse HJ, Roughgarden J (2010) What is an individual organism? A multilevel selection perspective. Q Rev Biol 85:447–472

    Article  Google Scholar 

  • Franc A (1993) Classe des Scyphozoaires. In: Grassé PP (ed) Traité de zoologie, vol 3(2). Masson, Paris, pp 597–884

    Google Scholar 

  • Fryer G (1961) The developmental history of Mutela bourguignati (Ancey) Bourguignat (Mollusca: Bivalvia). Philos Trans R Soc Lond B 244:259–298

    Article  Google Scholar 

  • Fusco G (2005) Trunk segment numbers and sequential segmentation in myriapods. Evol Dev 7:608–617

    Article  Google Scholar 

  • Fusco G, Minelli A (2010) From polyphenism to complex metazoan life cycles. Philos Trans R Soc B 365:545–690

    Article  Google Scholar 

  • 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, Dordrecht

    Google Scholar 

  • Garcia-Bellido A, Ripoll P, Morata G (1973) Developmental compartmentalisation of the wing disc of Drosophila. Nat New Biol 245:251–253

    Article  Google Scholar 

  • García-Ruiz JM, Checa A, Rivas A (1990) On the origin of ammonite sutures. Paleobiology 16:349–354

    Google Scholar 

  • Gayon J (1992) Darwin et l’après-Darwin: une histoire de l’hypothèse de sélection naturelle. Kimé, Paris

    Google Scholar 

  • Gayon J (1998) Darwinism’s struggle for survival. Cambridge University Press, Cambridge

    Google Scholar 

  • Gerhart JC, Kirschner MW (1997) Cells, embryos and evolution. Blackwell Science, Boston

    Google Scholar 

  • Glenner H, Høeg JT (1995) A new motile, multicellulars stage involved in host invasion by parasitic barnacles (Rhizocephala). Nature 377:147–150

    Article  Google Scholar 

  • Glenny RW, Robertson HT (1990) Fractal properties of pulmonary blood flow: characterization of spatial heterogeneity. J Appl Physiol 69:532–545

    Google Scholar 

  • 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 13:112–116

    Article  Google Scholar 

  • Guthrie S, Prince V, Lumsden A (1993) Selective dispersal of avian rhombomere cells in orthotopic and heterotopic grafts. Development 118:527–538

    Google Scholar 

  • 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 30:121–186

    Google Scholar 

  • Hall BK (1999) The neural crest in development and evolution. Springer, New York

    Google Scholar 

  • Hallez P (1887) Embryogénie des dendrocoeles d’eau douce. Baillière, Paris

    Book  Google Scholar 

  • Hobbs HH Jr (1981) The crayfishes of Georgia. Smithson Contrib Zool 318:1–549

    Article  Google Scholar 

  • Jacobs DK, Hughes NC, Fitz-Gibbon ST, Winchell CJ (2005) Terminal addition, the Cambrian radiation and the Phanerozoic evolution of bilaterian form. Evol Dev 7:498–514

    Article  Google Scholar 

  • Janssen R, Prpic NM, Damen WGM (2004) Gene expression suggests decoupled dorsal and ventral segmentation in the millipede Glomeris marginata (Myriapoda: Diplopoda). Dev Biol 268:89–104

    Article  Google Scholar 

  • Karkach AS (2006) Trajectories and models of individual growth. Demogr Res 15:347–400

    Article  Google Scholar 

  • Keller EF (2000) The century of the gene. Harvard University Press, Cambridge, MA

    Google Scholar 

  • Kupiec J-J (2009) The origins of individuals. World Scientific, Singapore

    Book  Google Scholar 

  • 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

  • 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 249:333–348

    Article  Google Scholar 

  • 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 66:75–114

    Article  Google Scholar 

  • Long CA (2005) Intricate sutures as fractal curves. J Morphol 185:285–295

    Article  Google Scholar 

  • Loughry WJ, Prodohl PA, McDonough CM, Avise JC (1998) Polyembryony in armadillos. Am Sci 86:274–279

    Google Scholar 

  • Manni L, Burighel P (2006) Common and divergent pathways in alternative developmental processes of ascidians. BioEssays 28:902–912

    Article  Google Scholar 

  • 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, Chicago

    Google Scholar 

  • Metzger RJ, Klein OD, Martin GR, Krasnow MA (2008) The branching programme of mouse lung development. Nature 453:745–750

    Article  Google Scholar 

  • 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 2:12

    Article  Google Scholar 

  • Minelli A (2000) Holomeric vs. meromeric segmentation: a tale of centipedes, leeches, and rhombomeres. Evol Dev 2:35–48

    Article  Google Scholar 

  • Minelli A (2001) A three-phase model of arthropod segmentation. Dev Genes Evol 211:509–521

    Article  Google Scholar 

  • Minelli A (2003) The development of animal form. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Minelli A (2009a) Perspectives in animal phylogeny and evolution. Oxford University Press, Oxford

    Google Scholar 

  • Minelli A (2009b) Forms of becoming. Princeton University Press, Princeton

    Google Scholar 

  • 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 116–133

    Google Scholar 

  • Minelli A, Bortoletto S (1988) Myriapod metamerism and arthropod segmentation. Biol J Linn Soc 33:323–343

    Article  Google Scholar 

  • Minelli A, Fusco G (2004) Evo–devo perspectives on segmentation: model organisms, and beyond. Trends Ecol Evol 19:423–429

    Article  Google Scholar 

  • Minelli A, Chagas A Jr, Edgecombe GD (2009) Saltational evolution of trunk segment number in centipedes. Evol Dev 11:318–322

    Article  Google Scholar 

  • Nijhout HF (1990) Metaphors and the role of genes in development. BioEssays 12:441–446

    Article  Google Scholar 

  • Nikolei E (1961) Vergleichende Untersuchungen zur Fortpflanzung der heterogenen Gallmücken unter experimentellen Bedingungen. Z Morphol Okol Tiere 50:281–329

    Article  Google Scholar 

  • 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 39–166

    Google Scholar 

  • Peterson KJ, Cameron RA, Davidson EH (1997) Set-aside cells in maximal indirect development: evolutionary and developmental significance. BioEssays 19:623–631

    Article  Google Scholar 

  • Pigliucci M (2001) Phenotypic plasticity: beyond nature and nurture. The Johns Hopkins University Press, Baltimore

    Google Scholar 

  • Pigliucci M, Müller GB (eds) (2010) Evolution: the extended synthesis. MIT Press, Cambridge

    Google Scholar 

  • 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 40:105–112

    Article  Google Scholar 

  • Pradeu T (2010) What is an organism? An immunological answer. Hist Philos Life Sci 32:247–268

    Google Scholar 

  • 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 135–156

    Google Scholar 

  • 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 122:1395–1407

    Google Scholar 

  • Santelices B (1999) How many kinds of individual are there? Trends Ecol Evol 14:152–155

    Article  Google Scholar 

  • Schlosser G (2002) Modularity and the units of evolution. Theory Biosci 121:1–80

    Article  Google Scholar 

  • Schlosser G, Wagner GP (eds) (2004) Modularity in development and evolution. University of Chicago Press, Chicago

    Google Scholar 

  • Sebens KP (1987) The ecology of indeterminate growth in animals. Ann Rev Ecol Syst 18:371–407

    Article  Google Scholar 

  • Song JL, Wong JL, Wessel GM (2006) Oogenesis: single cell development and differentiation. Dev Biol 300:385–405

    Article  Google Scholar 

  • Soto AM, Sonnenschein C (2004) The somatic mutation theory of cancer: growing problems with the paradigm? BioEssays 26:1097–1107

    Article  Google Scholar 

  • Steenstrup JJS (1845) On the alternation of generation or the propagation and development of animals through alternate generations. Ray Society, London

    Google Scholar 

  • Surhone LM, Timpledon MT, Marseken SF (2010) Paedogenesis. VDM, Saarbrücken

    Google Scholar 

  • 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 35–61

    Google Scholar 

  • Verhoeff KW (1923) Periodomorphose. Zool Anz 56(233–238):241–254

    Google Scholar 

  • Vervoort M (2011) Regeneration and development in animals. Biol Theory 6. doi:10.1007/s13752-011-0005-3

  • West-Eberhard MJ (2003) Developmental plasticity and evolution. Oxford University Press, New York

    Google Scholar 

  • Williamson DJ (2006) Hybridization in the evolution of animal form and life-cycle. Biol J Linn Soc 148:585–602

    Google Scholar 

  • Wolpert L, Jessell T, Lawrence P, Meyerowitz E, Robertson E, Smith J (2007) Principles of development. Oxford University Press, Oxford

    Google Scholar 

  • Wyatt IJ (1961) Pupal paedogenesis in the Cecidomyidae (Diptera) I. Proc R Entomol Soc Lond A 36:133–143

    Google Scholar 

  • Wyatt IJ (1964) Immature stages of Lestremiinae (Diptera: Cecidomyidae) infesting cultivated mushrooms. Trans R Entomol Soc Lond 116:15–27

    Article  Google Scholar 

  • Zamir M (2001) Fractal dimensions and multifractility in vascular branching. J Theor Biol 212:183–190

    Article  Google Scholar 

  • Zattara EE, Bely AE (2011) Evolution of a novel developmental trajectory: fission is distinct from regeneration in the annelid Pristina leidyi. Evol Dev 13:80–95

    Article  Google Scholar 

  • Zhurov V, Terzin T, Grbić M (2007) (In)discrete charm of the polyembryony: evolution of embryo cloning. Cell Mol Life Sci 64:2790–2798

    Article  Google Scholar 

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Acknowledgments

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.

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  1. Department of Biology, University of Padua, Padua, Italy

    Alessandro Minelli

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Minelli, A. Animal Development, an Open-Ended Segment of Life. Biol Theory 6, 4–15 (2011). https://doi.org/10.1007/s13752-011-0002-6

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