Advertisement

The Cyclorrhaphan Larva

  • Graham E. Rotheray
Chapter
Part of the Zoological Monographs book series (ZM, volume 4)

Abstract

The Cyclorrhapha is well-supported, species-rich, biodiverse and includes one of the most explosive of insect radiations. Although the larval stage is considered to be important in the radiation of the Cyclorrhapha, knowledge of larvae is poor, a characteristic of most insect groups with a larval stage. Reasons for such neglect are introduced and include an understandable emphasis on the adult stage in taxonomy, problems of obtaining, rearing and identifying larvae and assumptions that they are inherently similar and poor as a source of data. A brief overview of the literature on cyclorrhaphan larvae is presented. To provide an introduction and to set a context for more detailed assessments that are the subjects of later chapters, the origin of the insect larval stage and its attributes and groundplan states in the Diptera are considered. These attributes and groundplan states include peristalsis, fat storage, dormancy and the puparium, and their influence on cyclorrhaphan larval ecomorphology is introduced. The structure and content of the book is outlined.

References

  1. Anthon H (1988) Larval morphology of Mischoderus (Insecta, Diptera, Nematocera, Tanyderidae) with notes on tanyderid affinities. Zool Scr 17:381–397CrossRefGoogle Scholar
  2. Arias AM (2008) Drosophila melanogaster and the development of biology in the 20th century. In: Dahmann C (ed) Drosophila methods and protocols. Humana, New Jersey, pp 1–25Google Scholar
  3. Arnold SJ (1983) Morphology, performance and fitness. Am Zool 23:347–361CrossRefGoogle Scholar
  4. Arrese EL, Soulages JL (2010) Insect fat body: energy, metabolism, and regulation. Annu Rev Entomol 55:207–225CrossRefGoogle Scholar
  5. Balachowsky A, Mesnil L (1935) Les insectes nuisibles aux plantes cultivées, 2 vols. Busson, ParisGoogle Scholar
  6. Berlese A (1913) Intorno alle metamorfosi degli insetti. Redia 9:121–136Google Scholar
  7. Bernays EA (1971) The vermiform larva of Schistocerca gregaria (Forskaål): form and activity (Insecta, Orthoptera). Z Morph Tiere 70:183–200Google Scholar
  8. Beutel RG, Friedrich F, Hörnschemeyer T, Pohla H, Frank Hünefeld F, Beckmann F, Meier R, Misof B, Whiting MF, Vilhelmsen L (2010) Morphological and molecular evidence converge upon a robust phylogeny of the megadiverse Holometabola. Cladistics 26:1–15CrossRefGoogle Scholar
  9. Brauer F (1863) Monographie der Oestriden. WienGoogle Scholar
  10. Brauns A (1954) Terricole Dipterenlarven. Musterschmidt Wissenschaftlicher Verlag, BerlinGoogle Scholar
  11. Brown BV, Borkent A, Cumming JM, Wood DM, Woodley NE, Zumbado MA (2009, 2010) Manual of Central American Diptera, vols 1–2. National Research Council of Canada, Research Press, OttawaGoogle Scholar
  12. Campos-Ortega JA, Hartenstein V (1997) The embryonic development of Drosophila melanogaster. Springer, BerlinCrossRefGoogle Scholar
  13. Chandler AEF (1968) A preliminary key to the eggs of some of the commoner aphidophagous Syrphidae (Diptera) occurring in Britain. Trans R Ent Soc Lond 120:199–218CrossRefGoogle Scholar
  14. Cook EF (1949) The evolution of the head in the larvae of the Diptera. Microent 14:1–57Google Scholar
  15. Courtney GW, Sinclair BJ, Meier R (2000) Morphology and terminology of Diptera larvae. In: Papp L, Darvas B (eds) Contributions to a manual of Palaearctic Diptera, vol 1. Science Herald, Budapest, pp 85–161Google Scholar
  16. Cumming KP, Sinclair BJ, Wood DM (1995) Homology and phylogenetic implications of male genitalia in Diptera-Eremoneura. Ent Scand 26:120–151CrossRefGoogle Scholar
  17. Dowding VM (1967) The function and ecological significance of the pharyngeal ridges occurring in the larvae of some cyclorrhaphous Diptera. Parasitol (Cam) 57:371–388CrossRefGoogle Scholar
  18. Emden FLV (1957) The taxonomic significance of the characters of immature insects. Annu Rev Entomol 2:91–106CrossRefGoogle Scholar
  19. Ferrar P (1987) A guide to the breeding habits and immature stages of Diptera Cyclorrhapha. Entomonograph 8:1–907Google Scholar
  20. Griffiths GCD (1972) The phylogenetic classification of Diptera Cyclorrhapha, with special reference to the structure of the male postabdomen. Ser Entomol 8:1–340Google Scholar
  21. Grimaldi D, Engel MS (2005) Evolution of the insects. Cambridge University Press, CambridgeGoogle Scholar
  22. Hartley JC (1963) The cephalopharyngeal apparatus of syrphid larvae and its relationship to other Diptera. Proc Zool Soc Lond 141:261–280CrossRefGoogle Scholar
  23. Headrick DH, Goeden RD (1996) The biology of nonfrugivorous tephritid fruit flies. Annu Rev Entomol 43:217–241CrossRefGoogle Scholar
  24. Hennig W (1943) Ein Beitrag zum Problem der “Beziehungen zwischen Larven und Imaginalsystematik”. Arb Morphol Taxon Ent Berlin-Dahlem 10:138–144Google Scholar
  25. Hennig W (1948, 1950, 1952) Die Larvenformen der Dipteren, vols 1–3. Akademie Verlag, BerlinGoogle Scholar
  26. Hinton HE (1948) On the origin and function of the pupal stage. Trans R Ent Soc Lond 99:395–409CrossRefGoogle Scholar
  27. Hennig W (1973) Diptera (Zweiflügler). In: Helmcke JG, Starck D, Wermuth H (eds) Handbuch der Zoologie. De Gruyter, Berlin, Vol IV, 2 Hälfte: Insecta, 2/31, LfgGoogle Scholar
  28. Hinton HE (1977) Enabling mechanisms. In: Proceeding of XV international congress of entomology, Washington, DC, pp 71–83Google Scholar
  29. Hinton HE (1981) Biology of insect eggs, vol 1. Pergamon, OxfordGoogle Scholar
  30. Imms AD (1937) Recent advances in entomology. Blakiston, Philadelphia, PACrossRefGoogle Scholar
  31. Imms AD (1957) A general textbook of entomology. Methuen and Co, LondonGoogle Scholar
  32. Kambysellis MP, Ho KF, Craddock EM, Piano F, Parisi M, Cohen J (1995) Pattern of ecological shifts in the diversification of Hawaiian Drosophila inferred from a molecular phylogeny. Curr Biol 5:1129–1139CrossRefGoogle Scholar
  33. Keilin D (1944) Respiratory systems and respiratory adaptations in larvae and pupae of Diptera. Parasitol (Cam) 36:1–66CrossRefGoogle Scholar
  34. Kingsolver JG, Huey RB (2003) Introduction: the evolution of morphology, performance, and fitness. Integr Comp Biol 43:361–366CrossRefGoogle Scholar
  35. Kirk-Spriggs AH, Sinclair BJ (eds) (2017) Manual of Afrotropical Diptera, vols 1–3. Suricata 4. South African National Biodiversity Institute, PretoriaGoogle Scholar
  36. Kutty SN, Pont AC, Meier R, Pape T (2014) Complete tribal sampling reveals basal split in Muscidae (Diptera), confirms saprophagy as ancestral feeding mode, and reveals an evolutionary correlation between instar numbers and carnivory. Mol Phylogenet Evol 78:349–364CrossRefGoogle Scholar
  37. Labandeira CC (2005) The fossil record of insect extinction: new approaches and future directions. Am Entomol 51:14–29CrossRefGoogle Scholar
  38. Labandeira CC (2011) Evidence for an earliest late carboniferous divergence time and the early larval ecology and diversification of major holometabola lineages. Entomol Am 117:9–21Google Scholar
  39. Lambkin C, Sinclair BJ, Pape T, Courtney GW, Skevington JH, Meier R, Yeates DK, Blagoderov V, Wiegmann BM (2013) The phylogenetic relationships among infraorders and superfamilies of Diptera based on morphological evidence. Syst Entomol 38:164–179CrossRefGoogle Scholar
  40. Levin LA, Bridges TS (1995) Pattern and diversity in reproduction and development. In: McFdward LR (ed) Ecology of marine invertebrate larvae. CRC Press, Boca Raton, FL, pp 1–48Google Scholar
  41. Lundbeck W (1902–1927) Diptera Danica genera and species of flies hitherto found in Denmark, vols 1–7. Copenhagen.Google Scholar
  42. Mamaev BM, Krivosheina NP (1993) The larvae of gall midges (Diptera, Cecidomyiidae): comparative morphology, biology, keys. Balkemia, Rotterdam, NetherlandsGoogle Scholar
  43. Marshall SA (2013) Flies: the natural history and diversity of Diptera. Firefly Books, Richmond HillGoogle Scholar
  44. Martínez-Falcón AP, Marcos-García MA, Moreno CE, Rotheray GE (2011) A critical role for Copestylum larvae (Diptera, Syrphidae) in the decomposition of cactus forests. J Arid Environ 78:41–48CrossRefGoogle Scholar
  45. McAlpine JF, Wood DM (eds) (1989) Manual of Nearctic Diptera, Research Branch. Agriculture Canada. Monograph No. 32, vol 3Google Scholar
  46. McAlpine JF, Peterson BV, Shewell GE, Teskey HJ, Vockeroth JR, Wood DM (eds) (1981) Manual of Nearctic Diptera, Research Branch. Agriculture Canada. Monograph No. 27, vol 1Google Scholar
  47. McAlpine JF, Peterson BV, Shewell GE, Teskey HJ, Vockeroth JR, Wood DM (eds) (1987) Manual of Nearctic Diptera, Research Branch. Agriculture Canada. Monograph No. 28, vol 2Google Scholar
  48. McLean IFG (2000) Beneficial Diptera and their role in decomposition. In: Papp L, Darvas B (eds) Contributions to a manual of Palearctic Diptera, vol 1. Science Herald, Budapest, pp 491–517Google Scholar
  49. Meier R, Hilger S (2000) On the egg morphology and phylogenetic relationships of Diopsidae (Diptera: Schizophora). J Zool Syst Evol Res 38:1–36CrossRefGoogle Scholar
  50. Meier R, Lim GS (2009) Conflict, convergent evolution, and the relative importance of immature and adult characters in endopterygote phylogenetics. Annu Rev Entomol 54:85–104CrossRefGoogle Scholar
  51. Mirth CK, Riddiford LM (2007) Size assessment and growth control: how adult size is determined in insects. Bio Essays 29:344–355Google Scholar
  52. Neugart C, Schneeberg K, Beutel RG (2009) The morphology of the larval head of Tipulidae (Diptera, Insecta) - the dipteran groundplan and evolutionary trends. Zool Anz 248:213–235CrossRefGoogle Scholar
  53. Papp L, Darvas B (eds) (1998–2000) Contributions to a manual of palaearctic diptera, vol 1–3. Science Herald, BudapestGoogle Scholar
  54. Pechenik JA (1999) On the advantages and disadvantages of larval stages in benthic marine invertebrate life cycles. Mar Ecol Prog Ser 177:269–297CrossRefGoogle Scholar
  55. Powell JR (1997) Progress and prospects in evolutionary biology: the Drosophila model. Oxford University Press, New YorkGoogle Scholar
  56. Poyarkoff E (1914) Essai d’une theorie de la nymphe des insectes holometaboles. Arch Zool Exp Gen 54:221–265Google Scholar
  57. Ricarte A, Marcos-García MA, Hancock EG, Rotheray GE (2015) Neotropical Copestylum Macquart (Diptera: Syrphidae) breeding in fruits and flowers, including 7 new species. PLos One 10:1–58.  https://doi.org/10.1371/journal.pone.0142441 CrossRefGoogle Scholar
  58. Roberts MJ (1969) The feeding habits of higher Diptera larvae. Entomologist 102:99–106Google Scholar
  59. Roberts MJ (1971) The structure of the mouthparts of some calypterate dipteran larvae in relation to their feeding habits. Acta Zool 52:171–188CrossRefGoogle Scholar
  60. Rohdendorf BB (1974) The historical development of Diptera. University of Alberta Press, Edmonton, ABGoogle Scholar
  61. Rotheray GE (2016a) Improving knowledge of the cyclorrhaphan larva (Diptera). J Nat Hist 50:2169–2198CrossRefGoogle Scholar
  62. Rotheray GE (2016b) Fieldcraft and closing the knowledge gap between immature and adult stages of Diptera Cyclorrhapha. Dipts Digest 23:85–96Google Scholar
  63. Rotheray GE, Lyszkowski R (2015) Diverse mechanisms of feeding and movement in Cyclorrhaphan larvae (Diptera). J Nat Hist 49:2139–2211CrossRefGoogle Scholar
  64. Schluter D (2000) The ecology of adaptive radiation. Oxford University Press, OxfordGoogle Scholar
  65. Schneeberg K, Beutel RG (2014) The evolution of head structures in lower Diptera. Sci Open Res 2014.  https://doi.org/10.14293/S2199-1006.1.sor-life.altcei1.v2
  66. Schremmer F (1951) Die Mundteile der Brachycerenlarven and der Kopfbau der Larve von Stratiomys chamaeleon. L Osterr Zool Z 3:326–397Google Scholar
  67. Sehnal F, Svacha P, Zrzavy J (1996) Evolution of insect metamorphosis. In: Gilbert LI, Tata JR, Atkinson G (eds) Metamorphosis. Academic, San Diego, CA, pp 3–58CrossRefGoogle Scholar
  68. Shaw MR, Askew RR (2010) Hymenopterous parasitoids of Diptera. In: Chandler P (ed) A dipterist’s handbook, vol 15, 2nd edn. The Amateur Entomologist’s Society, Orpington, pp 347–361Google Scholar
  69. Smith KVG (1989) An introduction to the immature stages of british flies. Handbks Ident Br Insects 10:1–280Google Scholar
  70. Snodgrass RE (1953) The metamorphosis of a fly’s head. Smith Misc Coll 122:1–25Google Scholar
  71. Ståhls G, Hippa H, Rotheray G, Muona J, Gilbert F (2003) Phylogeny of Syrphidae (Diptera) inferred from combined analysis of molecular and morphological characters. Syst Entomol 28:433–450CrossRefGoogle Scholar
  72. Stehr FW (1987) Immature insects, vol 2. Kendall/Hunt, IowaGoogle Scholar
  73. Strathmann RR (1985) Feeding and nonfeeding larval development and life history evolution in marine invertebrates. Annu Rev Ecol Syst 16:339–361CrossRefGoogle Scholar
  74. Swammerdam J (1758) The book of nature; or, the history of insects (translated by T. Floyd in 1758). Seyffert, London, 153pGoogle Scholar
  75. Teskey HJ (1981) Morphology and terminology – larvae. In: McAlpine J, Peterson BV, Shewell GE, Teskey HJ, Vockeroth JR, Wood DM (eds) Manual of Nearctic Diptera, vol 1, pp 65–88Google Scholar
  76. Tkoč M, Tóthová A, Ståhls G, Chandler PJ, Vaňhara J (2016) Molecular phylogeny of flat-footed flies (Diptera: Platypezidae): main clades supported by new morphoogical evidence. Zool Scr 46:429–444CrossRefGoogle Scholar
  77. Trautwein MD, Wiegmann BM, Yeates DK (2010) A multigene phylogeny of the fly superfamily Asiloidea (Insecta): taxon sampling and additional genes reveal the sister-group to all higher flies (Cyclorrhapha). Mol Phylogenet Evol 56:918–930CrossRefGoogle Scholar
  78. Trautwein MD, Wiegmann BM, Beutel R, Kjer KM, David K, Yeates DM (2012) Advances in insect phylogeny at the dawn of the postgenomic era. Annu Rev Entomol 57:449–468CrossRefGoogle Scholar
  79. Truman JW, Riddiford LM (1999) The origins of insect metamorphosis. Nature 410:447–452CrossRefGoogle Scholar
  80. Truman JW, Riddiford LM (2002) Endocrine insights into the evolution of metamorphosis in insects. Annu Rev Entomol 47:467–500CrossRefGoogle Scholar
  81. Wiegmann BM, Trautwein MD, Kim J, Bertone M, Winterton SL, Cassel BK, Yeates DK (2009) Single-copy nuclear genes resolve the phylogeny of the holometabolous insect orders. BMC Biol 7(1):34.  https://doi.org/10.1186/1741-7007-7-34 CrossRefPubMedPubMedCentralGoogle Scholar
  82. Wiegmann BM, Trautwein MD, Winkler IS, Barra NB, Kima J-W, Lambkin C, Berton MA, Cassela BK, Bayless KM, Heimberg AM, Wheeler BM, Petersone KJ, Pape T, Sinclair BJ, Skevington JH, Blagoderov V, Caravask J, Narayanan Kutty SN, Schmidt-Ott U, Kampmeier GE, Thompson FC, Grimaldi DA, Beckenbach AT, Courtney GM, Friedrich M, Meier R, Yeates DK (2011) Episodic radiations in the fly tree of life. Proc Natl Acad Sci U S A 80:5690–5695CrossRefGoogle Scholar
  83. Wigglesworth VB (1954) The physiology of insect metamorphosis. Cambridge University Press, Cambridge, MAGoogle Scholar
  84. Williamson DI (2001) Larval transfer and the origins of larvae. Zool J Linnean Soc 131:111–122CrossRefGoogle Scholar
  85. Williamson DI, Vickers SE (2007) The origins of larvae. Sci Am 95:509–517CrossRefGoogle Scholar
  86. Young AD, Lemmon AR, Skevington JH, Mengua X, Ståhls G, Reemer M, Jordaens K, Kelso S, Lemmon EM, Hauser M, Meyer M, Miso B, Wiegmann BM (2016) Anchored enrichment dataset for true flies (order Diptera) reveals insights into the phylogeny of flower flies (family Syrphidae). Evol Biol 16:143Google Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Graham E. Rotheray
    • 1
  1. 1.National Museums of ScotlandEdinburghUK

Personalised recommendations