Abstract
The traditional framework for the description of arthropod development takes the molt-to-molt interval as the fundamental unit of periodization, which is similar to the morphological picture of the main body axis as a series of segments. Developmental time is described as the subdivision into a few major stages of one or more instars each, which is similar to the subdivision of the main body axis into regions of one to many segments each. Parallel to recent criticisms to the segment as the fundamental building block of arthropod anatomy, we argue that, while a firm subdivision of development in stages is useful for describing arthropod ontogeny, this is limiting as a starting point for studying its evolution. Evolutionary change affects the association between different developmental processes, some of which are continuous in time whereas others are linked to the molting cycle. Events occurring but once in life (hatching; first achieving sexual maturity) are traditionally used to establish boundaries between major units of arthropod developmental time, but these boundaries are quite labile. The presence of embryonic molts, the ‘gray zone’ of development accompanying hatching (with the frequent delivery of an immature whose qualification as ‘free-embryo’ or ordinary postembryonic stage is arbitrary), and the frequent decoupling of growth and molting suggest a different view. Beyond the simple comparison of developmental schedules in terms of heterochrony, the flexible canvas we suggest for the analysis of arthropod development opens new vistas into its evolution. Examples are provided as to the origin of holometaboly and hypermetaboly within the insects.
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References
Andersson G (1979) On the use of larval characters in the classification of lithobiomorph centipedes (Chilopoda Lithobiomorpha). In: Camatini M (ed) Myriapod biology. Academic, London, pp 73–81
André HM (1988) Age-dependent evolution: from theory to practice. In: Humphries CJ (ed) Ontogeny and systematics. Columbia University Press, New York, pp 137–187
André HM (1989) The concept of stase. In: André HM, Lions J-C (eds) L’ontogenèse et le concept de stase chez les arthropodes. AGAR Publishers, Warre, pp 3–16
Bain BA (2003) Larval types and a summary of postembryonic development within the pycnogonids. Invertebr Reprod Dev 43:193–222
Beck SD (1971) Growth and retrogression in larvae of Trogoderma glabrum (Coleoptera: Dermestidae). 1. Characteristics under feeding and starvation conditions. Ann Entomol Soc Am 64:149–155
Berlese A (1913) Intorno alle metamorfosi degli insetti. Redia 9:121–136
Budd GE (2001) Why are arthropods segmented? Evol Dev 3:332–342
Caussanel C (1966) Étude du développement larvaire de Labidura riparia (Derm. Labiduridae). Ann Soc Entomol Fr NS 2:469–498
Chatterton BDE, Speyer SE (1997) Ontogeny. In: Kaesler RL (ed) Treatise on invertebrate paleontology, part O, Arthropoda 1, Trilobita, revised. Volume 1: introduction, Order Agnostida, Order Redlichiida. Geol Soc Amer, Boulder, CO; University of Kansas, Lawrence, KS, pp 173–247
Edgecombe GD, Giribet G (2004) Adding mitochondrial sequence data (16S rRNA and cytochrome c oxidase subunit I) to the phylogeny of centipedes (Myriapoda: Chilopoda): an analysis of morphology and four molecular loci. J Zoolog Syst Evol Res 42:89–134
Enghoff H, Dohle W, Blower JG (1993) Anamorphosis in millipedes (Diplopoda). The present state of knowledge and phylogenetic considerations. Zool J Linn Soc 109:103–234
Ferrari FD, Grygier MJ (2003) Comparative morphology among trunk limbs of Caenestheriella gifuensis and of Leptestheria kawachiensis (Crustacea: Branchiopoda: Spinicaudata). Zool J Linn Soc 139:547–564
Fusco G (2005) Trunk segment numbers and sequential segmentation in myriapods. Evol Dev 7:608–617
Gore RH (1985) Molting and growth in decapod larvae. In: Wenner AM (ed) Larval growth (Crustacean Issues 2). Balkema, Rotterdam Boston, pp 1–65
Goudeau M (1977) Contribution à la biologie d’un crustacé parasite: Hemioniscus balani Buchholz, isopode épicaride. Nutrition, mues et croissance de la femelle et des embryons. Cah Biol Mar 18:201–242
Grandjean F (1938) Sur l’ontogénie des acariens. CR Acad Sci Paris 206D:146–150
Grimaldi D, Engel MS (2005) Evolution of the insects. Cambridge University Press, Cambridge, New York
Hassall M, Grayson FWL (1987) The occurrence of an additional instar in the development of Chorthippus brunneus (Orthoptera: Gomphocerinae). J Nat Hist 21:329–337
Heming BS (2003) Insect development and evolution. Comstock Publ Associates, Ithaca London
Hobbs HH Jr (1981) The crayfishes of Georgia. Smithson Contrib Zool 318:1–549
Hughes NC (2003) Trilobite body patterning and the evolution of arthropod tagmosis. Bioessays 25:386–395
Ivanenko VN, Ferrari FD, Smurov AV (2001) Nauplii and copepodids of Scottomyzon gibberum (Copepoda: Siphonostomatoida: Scottomyzontidae, new family), a symbiont of Asterias rubens (Asteroidea). Proc Biol Soc Wash 114:237–261
Kabata Z (1979) Parasitic copepoda of British fishes. Ray Society, London
Klausnitzer B (2003) Unterordnung Polyphaga. In: Dathe HH (ed) 5. Teil: Insecta. In: Gruner H-E (ed) Band I. Wirbellose Tiere. In: Kaestner A (founder) Lehrbuch der Speziellen Zoologie. Gustav Fischer, Jena Stuttgart New York, pp 452–526
Konopová B, Zrzavý J (2005) Ultrastructure, development, and homology of insect embryonic cuticles. J Morphol 264:339–362
Krool S, Bauer T (1987) Reproduction, development and pheromone secretion in Heteromurus nitidus Templeton, 1835 (Collembola, Entomobryidae). Rec Ecol Biol Sol 24:187–195
Langton PH, Cranston PS, Armitage P (1988) The parthenogenetic midge of water supply systems, Paratanytarsus grimmi (Schneider) (Diptera: Chironomidae). Bull Entomol Res 78:317–328
Lawrence JF, Nielsen ES, Mackerras IM (1991) Skeletal anatomy and key to orders. In: CSIRO (ed) Insects of Australia. I. Melbourne University Press, Carlton, pp 3–32
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
Minelli A (1996) Segments, body regions and the control of development through time. Mem Calif Acad Sci 20:55–61
Minelli A (2003) The development of animal form. Cambridge University Press, Cambridge
Minelli A (2004) Bits and pieces. Science 306:1693–1694
Minelli A, Fusco G (2004) Evo-devo perspectives on segmentation: model organisms and beyond. Trends Ecol Evol 19:423–429
Minelli A, Negrisolo E, Fusco G (2006) Reconstructing animal phylogeny in the light of evolutionary developmental biology. In: Hodkinson TR, Parnell JAN, Waldren S (eds) Systematics of species reach taxa: building and using the tree of life. CRC Press, Boca Raton, FL
Moritz M (1993) Unterstamm Arachnata. In: Gruner EE, Moritz M, Dunger W (eds) 4. Teil: Arthropoda (ohne Insecta). In: Gruner H-E (ed) Band I. Wirbellose Tiere. In: Kaestner A (founder) Lehrbuch der Speziellen Zoologie. Gustav Fischer, Jena Stuttgart New York, pp 64–442
Murakami Y (1963) Postembryonic development of the common Myriapoda of Japan. XIII. Life history of Bazillozonium nodulosum Verhoeff (Colobognatha, Platydesmidae) 3. Zool Mag Tokyo 71:245–249
Nigon V (1965) Développment et reproduction des Nématodes. In: Grassé PP (ed) Traité de Zoologie, Tome IV, fascicule II. Masson, Paris, pp 218–386
Nielsen C (2001) Animal evolution: interrelationships of the living phyla, 2nd edn. Oxford University Press, Oxford
Nijhout F (1994) Insect hormones. Princeton University Press, Princeton, NJ
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 New York København Köln, pp 135–156
Scholtz G (2000) Evolution of the nauplius stage in malacostracan crustaceans. J Zool Syst Evol Res 38:175–187
Scholtz G (2004) Baupläne versus ground patterns, phyla versus monophyla: aspects of patterns and processes in evolutionary developmental biology. In: Scholtz G (ed) Evolutionary developmental biology of Crustacea (Crustacean Issues 15). Balkema, Lisse, pp 3–16
Sehnal F (1985) Growth and life cycles. In: Kerkut GA, Gilbert LI (eds) Comprehensive insect physiology biochemistry and pharmacology, 2. Postembryonic development. Pergamon, New York, pp 1–86
Smith KK (2001) Heterochrony revisited: the evolution of developmental sequences. Biol J Linn Soc 73:169–186
Thorens P (1991) Développement et morphologie comparés de Chorthippus mollis (Charp.) (Orthoptera, Acrididae). Mitt Schweiz Entomol Ges 64:9–25
Truman JW, Riddiford LM (1999) The origins of insect metamorphosis. Nature 401:447–452
Uvarov B (1966) Grasshoppers and locusts. A handbook of general acridology, vol 1. Anatomy, physiology, development, phase polymorphism, introduction to taxonomy. Cambridge University Press, Cambridge, UK
Whiting MF (2004) Phylogeny of the holometabolous insects: the most successful group of terrestrial organisms. In: Cracraft J, Donoghue MJ (eds) Assembling the tree of life. Oxford University Press, New York, pp 345–361
Acknowledgements
Special thanks are due to Jean Deutsch for inviting AM to the Paris meeting on “Development and Phylogeny of Arthropods” (23–24 September 2005), thus stimulating our thoughts on the topic on the present contribution, and to Marta Chiodin for sharing with us her results on Lithobius neural development. Authors are also very grateful to Frank Ferrari, Bruce Heming, H. Frederick Nijhout, Peter Weygoldt, and two anonymous referees for their very useful comments on a draft of this paper. Ronald Jenner and Ariel Chipman kindly read our text at the Paris meeting, while the senior author was unable to attend for last-minute health problems. This research was sponsored by the Italian MIUR and the University of Padova.
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Minelli, A., Brena, C., Deflorian, G. et al. From embryo to adult—beyond the conventional periodization of arthropod development. Dev Genes Evol 216, 373–383 (2006). https://doi.org/10.1007/s00427-006-0075-6
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DOI: https://doi.org/10.1007/s00427-006-0075-6