Advertisement

The Cyclorrhaphan Larva as a Data Source

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

Abstract

In this chapter, the main findings of the book are summarised and discussed with the twin aims of identifying common features within and between contrasts such as taxon, feeding mode and ecomorphology and extending the discussion to consider the role of the larval stage in the diversification of the Cyclorrhapha. Based on examples from earlier chapters, the value of making progress by allowing morphological and movement analyses to inform one another is evaluated. Assessments such as these support the idea that larvae are underestimated as a data source and that they are many times richer in potential than under prevailing hypotheses of similarity and convergence. The origins and roles of trophic and locomotor traits that distinguish the Cyclorrhapha are reassessed and feeding modes compared and contrasted. Switching between feeding modes is a putative contributor to diversification and requires improved assessment and evaluation. Provisional assessment of exemplar lineages with multiple feeding modes has identified change in individual trophic features and these are putative candidates underpinning switches in feeding modes. Against a background of direct and indirect opportunities for phytophagy, saprophagy and zoophagy provided by the diversification of angiosperms and feeding mode switching, adaptive larval features also include component subdivision and recombination, modularity and character lability. The latter in particular seems to be a major contributor to the rapid evolution of the higher Cyclorrhapha. Furthermore, adaptation potential or adaptability appears to increase over phylogenetic distances measured by the number of nodes between taxa. This may be due to conservative evolution in which genetic and developmental mechanisms are accrued and modified rather than becoming redundant or lost. Accrual of adaptability may be another significant contributor to high levels of trophic and locomotor specialisation, ecomorphological variation and diverse life cycles.

References

  1. Alfaro RI, Borden JH (1980) Predation by Lonchaea corticis (Diptera: Lonchaeidae) on the White Pine Weevil, Pissodes strobi (Coleoptera: Curculionidae). Can Entomol 112:1259–1270CrossRefGoogle Scholar
  2. Bauer G (1986) Life-history strategy of Rhagoletis alternata (Diptera: Trypetidae), a fruit fly operating in a ‘non-interactive’ system. J Anim Ecol 55:785–794CrossRefGoogle Scholar
  3. Berrigan D, Pepin DJ (1995) How maggots move: allometry and kinematics of crawling in larval Diptera. J Insect Physiol 41:329–337CrossRefGoogle Scholar
  4. Beutel RG, Friedrichb F, Thomas Hörnschemeyer T, Pohla H, Frank Hünefelda F, Beckmannd F, Meier R, Misof B, Whiting MF, Vilhelmsenh L (2010) Morphological and molecular evidence converge upon a robust phylogeny of the megadiverse Holometabola. Cladistics 26:1–15CrossRefGoogle Scholar
  5. Borkent A, Brown BV, Adler PH, De Souza Amorim D, Barber K, Bickel D, Boucher S, Brooks SE, Burger J, Burington ZL, Capellari RS, Costa DNR, Cumming JM Curler G, Dick CW, Epler JH Fisher E, Gaimari SD, Gelhaus J, Grimaldi DA, Hash J, Hauser M, Hippa H, Ibáñez- Bernal S, Jaschhof M, Kameneva EP, Kerr PH, Korneyev V, Korytkowski CA, Kung G-A, Kvifte GM, Lonsdale O, Marshall SA, Mathis WN, Michelsen V, Naglis S, Norrbom AL, Paiero S, Pape T, Pereira-Colavite A, Pollet M, Rochefort S, Rung A, Runyon JB, Savage J, Silva VC, Sinclair BS, Skevington JH, Stireman JO, Swann J, Vilkamaa P, Wheeler T, Whitworth T, Wong M, Wood DM, Woodley N, Yau T, Zavortink TJ, Zumbado MA (2018) Remarkable fly (Diptera) diversity in a patch of Costa Rican cloud forest: why inventory is a vital science. Zootaxa 4402:53–90PubMedCrossRefPubMedCentralGoogle Scholar
  6. Campos-Ortega JA, Hartenstein V (1997) The embryonic development of Drosophila melanogaster. Springer, BerlinCrossRefGoogle Scholar
  7. Chandler PJ (1991) Attraction of Palloptera usta Meigen (Diptera: Pallopteridae) to recently cut conifer wood and other notes on Pallopteridae. Br J Entomol Nat Hist 4:85–87Google Scholar
  8. Chapman EG, Foote BA, Malukiewicz J, Hoeh WR (2006) Parallel evolution of larval morphology and habitat in the snail-killing fly genus Tetanocera. J Evol Biol 19:1459–1474PubMedCrossRefPubMedCentralGoogle Scholar
  9. Chaudonneret J (1983) Les pieces buccales des Insectes: thème et variations II. Bull Bourgogne 36:116–133Google Scholar
  10. Cheverud JM (1996) Developmental integration and the evolution of pleiotropy. Am Zool 36:44–50CrossRefGoogle Scholar
  11. Cook EF (1949) The evolution of the head in the larvae of the Diptera. Microentomology 14:1–57Google Scholar
  12. 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
  13. Creager DB, Spruijt FJ (1935) The relation of certain fungi to larval development of Eumerus tuberculatus Rond. (Syrphidae, Diptera). Ann Entomol Soc Am 28:425–437CrossRefGoogle Scholar
  14. D’Herculais JK (1875) Recherches sur l’organisation et le development des Volucelles, Paris, p 208Google Scholar
  15. de Meijere JCH (1944) Over de metamorphose van Metopia leucocephala Rossi, Cacoxenus indagator Lw, Palloptera saltuum L., Paranthomyza nitida Mg. en Hydrellia nigripes Zett. (Dipt. ). Tijdsch voor Entomol 86:57–61Google Scholar
  16. de Moor FC (1973) Notes on a syrphid fly, Eumerus obliquus (Fabricius) (Diptera: Syrphidae). Arnoldia 6:1–7Google Scholar
  17. Dowding VM (1967) The function and ecological significance of the pharyngeal ridges occurring in the larvae of some cyclorrhaphous Diptera. Parasitology (Cam) 57:371–388CrossRefGoogle Scholar
  18. Dyte CE (1993) The occurrence of Thrypticus smaragdinus Gest. (Dipt.: Dolichopodidae) in Britain, with remarks on plant host in the genus. Entomologist 112:81–84Google Scholar
  19. Ferrar P (1987) A guide to the breeding habits and immature stages of Diptera Cyclorrhapha. Entomonograph 8:1–907Google Scholar
  20. Friis EM, Pedersen KR, Crane PR (2010) Diversity in obscurity: fossil flowers and the early history of angiosperms. Philos Trans R Soc Lond B Biol Sci 365:369–382PubMedPubMedCentralCrossRefGoogle Scholar
  21. Greve L (1993) Family Pallopteridae (Diptera) in Norway. Fauna Norvegica Ser B 40:37–44Google Scholar
  22. Günther MN, Nettesheim G, Shubeita GT (2016) Quantifying and predicting Drosophila larvae crawling. Sci Rep 6:27972.  https://doi.org/10.1038/srep27972 CrossRefPubMedPubMedCentralGoogle Scholar
  23. Hartley JC (1961) A taxonomic account of the larvae of some British Syrphidae. Proc Zool Soc Lond 136:505–573CrossRefGoogle Scholar
  24. Headrick DH, Goeden RD (1996) The biology of nonfrugivorous Tephritid fruit flies. Ann Rev Entomol 43:217–241CrossRefGoogle Scholar
  25. Heckscher ES, Lockery SR, Doe CQ (2012) Characterization of Drosophila larval crawling at the level of organism, segment, and somatic body wall musculature. J Neurol Sci 32:12460–12471Google Scholar
  26. Hennig W (1943) Ein Beitrag zum Problem der “Beziehungen zwischen Larven und Imaginalsystematik”. Arb Morphol Taxon Ent Berlin-Dahlem 10:138–144Google Scholar
  27. Hennig W (1952) Die larvenformen der Dipteren, vol 3. Akademie-Verlag, BerlinGoogle Scholar
  28. 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
  29. Hering EM (1943) Dipteren-biologien I. Mitteil Deutschen Entomol Gesell 12:16Google Scholar
  30. Hernandez MC (2008) Biology of Thrypticus truncatus and Thrypticus sagittatus (Diptera: Dolichopodidae), petiole miners of water hyacinth, in Argentina, with morphological descriptions of larvae and pupae. Ann Entomol Soc Am 10:1041–1049CrossRefGoogle Scholar
  31. Hodson WEH (1932) The large narcissus fly, Merodon equestris, Fab. (Syrphidae). Bull Entomol Res 23:429–448CrossRefGoogle Scholar
  32. Johannsen OA, Crosby CR (1913) The life history of Thrypticus muhlenbergiae sp. nov. (Diptera). Psyche 20:164–166CrossRefGoogle Scholar
  33. Jürgens G, Lehmann R, Schardin M, Nüsslein-Volhard C (1986) Segmental organisation of the head in the embryo of Drosophila melanogaster. Roux’s Arch Dev Biol 195:359–377CrossRefGoogle Scholar
  34. Kandybinda MN (1961) On the diagnostics of the larvae of fruit-flies (Diptera, Tephritidae). Ent Rev 40:103–110Google Scholar
  35. Krivosheina NP (1969) Ontogeny and evolution of dipterous insects. Nauka, Moscow, p 282Google 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. Lahiri S, Shen K, Klein M, Tang A, Kane E, Gershow M, Garrity P, Samuel ADT (2011) Two alternating motor programs drive navigation in Drosophila larva. PLoS One 6:e23180PubMedPubMedCentralCrossRefGoogle Scholar
  38. 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
  39. Ludwig CE (1949) Embryology and morphology of the larval head of Calliphora erythrocephala Meigen. Microentomology 14:75–111Google Scholar
  40. Martinek V (1977) Species of Genus Palloptera Fallén, 1820 (Dipt., Pallopteridae) in Czechoslovakia. Stud Entomol Forestalia 12:203–220Google Scholar
  41. McAlpine JF (1989) Phylogeny and classification of the Muscomorpha. In: McAlpine JF, Wood DM (eds) Manual Nearctic Diptera 3:1397–1502. Monograph No. 32, Research Branch, Agriculture CanadaGoogle Scholar
  42. Meier R (1995) Cladistic analysis of the Sepsidae (Cyclorrhapha: Diptera) based on a comparative scanning electron microscopic study of larvae. Syst Entomol 20:99–128CrossRefGoogle Scholar
  43. Meier R, Lim GS (2009) Conflict, convergent evolution, and the relative importance of immature and adult characters in endopterygote phylogenetics. Annu Rev Entomol 54:85–104PubMedCrossRefPubMedCentralGoogle Scholar
  44. Mengual X, Stahls G, Rojo S (2008) First phylogeny of predatory flower flies using mitochondrial CO1 and nuclear 28S rRNA genes: conflict and congruence with the current tribal classification. Cladistics 24:543–562CrossRefGoogle Scholar
  45. Misof B et al (2014) Phylogenomics resolves the timing and pattern of insect evolution. Science 346:763–767PubMedCrossRefPubMedCentralGoogle Scholar
  46. Narchuk EP (1985) Adaptions of cyclorrhaphan larvae (Diptera) for the inhabitation of living plants. In: Skarlato OA (ed) Systematics of Diptera (Insecta): ecological and morphological principles. Oxonian Press, New Delhi, pp 97–101Google Scholar
  47. 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
  48. Parmenter L (1951) Notes on the distribution of Pallopteridae in Britain. Ent Rec J Var 63:304–306Google Scholar
  49. Pérez-Bañón C, Marcos-García M-A (1998) Life history and description of the immature stages of Eumerus purpurariae (Díptera: Syrphidae) developing in Opuntia maxima. Eur J Entomol 95:373–382Google Scholar
  50. Persson PI (1963) Studies on the biology and larval morphology of some Trypetidae (Dipt.). Opusc Ent 28:33–69Google Scholar
  51. Ricarte A, Marcos-García MA, Rotheray GE (2008) The early stages and life histories of three Eumerus and two Merodon species (Diptera: Syrphidae) from the Mediterranean region. Ent Fenn 19:129–141Google Scholar
  52. Roberts MJ (1969) Structure of the mouthparts of the larvae of the flies Rhagio and Sargus in relation to feeding habits. J Zool Lond 159:381–398CrossRefGoogle Scholar
  53. Roháček J (2009) A monograph of Palaearctic Anthomyzidae (Diptera), Part 2. Čas Slezsk zem Muzea, Opava (A) 58 (Suppl 1):1–180Google Scholar
  54. Rohdendorf BB (1974) The historical development of Diptera. University of Alberta Press, Edmonton, ABGoogle Scholar
  55. Rotheray GE (1986) Colour, shape and defence in aphidophagous syrphid larvae (Diptera). Zool J Linn Soc 88:201–216CrossRefGoogle Scholar
  56. Rotheray GE (1988) Morphology and feeding behaviour of the leaf-mining larva of Cheilosia semifasciata (Diptera: Syrphidae). J Nat Hist 22:865–873CrossRefGoogle Scholar
  57. Rotheray GE (1993) Colour guide to hoverfly larvae (Diptera, Syrphidae). Dipter Digest 9:1–156Google Scholar
  58. Rotheray GE (1999a) The early stages of Cheilosia illustrata (Harris) (Diptera, Syrphidae). Dipter Digest 6:107–111Google Scholar
  59. Rotheray GE (1999b) Descriptions and a key to the larval and puparial stages of north-west European Volucella (Diptera, Syrphidae). Studia Dipterol 6:103–116Google Scholar
  60. Rotheray GE (2014) Development sites, feeding modes and early stages of seven European Palloptera species (Diptera, Pallopteridae). Zootaxa 3900:50–76PubMedCrossRefGoogle Scholar
  61. Rotheray GE (2016) Improving knowledge of the cyclorrhaphan larva (Diptera). J Nat Hist 50:2169–2198CrossRefGoogle Scholar
  62. Rotheray GE, Gilbert FS (1989) The phylogeny and systematics of European predacious Syrphidae (Diptera) based on larval and puparial stages. Zool J Linn Soc 95:29–70CrossRefGoogle Scholar
  63. Rotheray GE, Gilbert F (1999) Phylogeny of Palaearctic Syrphidae (Diptera): evidence from larval stages. Zool J Linn Soc 127:1–112CrossRefGoogle Scholar
  64. Rotheray GE, Gilbert F (2008) Phylogenetic relationships and the larval head of the lower Cyclorrhapha (Diptera). Zool J Linn Soc 153:287–323CrossRefGoogle Scholar
  65. Rotheray GE, Hewitt S (2015) Development site, feeding mode and early stages of Palloptera scutellata (Macquart) (Diptera, Pallopteridae). Dipter Digest 22:157–170Google Scholar
  66. Rotheray GE, Horsfield D (2013) Development sites and early stages of eleven species of Clusiidae (Diptera) occurring in Europe. Zootaxa 3619:401–427PubMedCrossRefGoogle Scholar
  67. Rotheray GE, Lyszkowski R (2015) Diverse mechanisms of feeding and movement in Cyclorrhaphan larvae (Diptera). J Nat Hist 49:2139–2211CrossRefGoogle Scholar
  68. Rotheray GE, Marcos-Garcia M-A, Hancock EG, Gilbert F (2000) The systematic position of Alipumilio and Nausigaster based on early stages (Diptera, Syrphidae). Studia Dipterol 7:133–144Google Scholar
  69. Rotheray GE, Hancock EG, Marcos-Garcia M (2007) Neotropical Copestylum (Diptera, Syrphidae) breeding in bromeliads (Bromeliaceae) including 22 new species. Zool J Linn Soc 150:267–317CrossRefGoogle Scholar
  70. Rotheray GE, Marcos-Garcia M, Hancock G, Pérez-Bañón C, Maier CT (2009) Neotropical Copestylum (Diptera, Syrphidae) breeding in Agavaceae and Cactaceae including seven new species. Zool J Linn Soc 156:697–749CrossRefGoogle Scholar
  71. Rotheray GE, Bland KP, Hancock G (2014) Paranthomyza nitida (Diptera: Anthomyzidae): life history in Scotland. Entomol Mon Mag 150:7–18Google Scholar
  72. Rupp L (1989) Die mitteleuropäische Arten der Gattung Volucella (Diptera, Syrphidae) als Kommensalen und Parasitoide in den Nestern von Hummeln und sozialen Wespen: Untersuchungen zur Wirtsfindung, Larvalbiologie und Mimikry. Unpublished PhD Thesis, Albert Ludwigs Universität, Freiburg, GermanyGoogle Scholar
  73. Schluter D (2000) The ecology of adaptive radiation. Oxford University Press, OxfordGoogle Scholar
  74. Schremmer F (1956) Funktionsmophologische Srudien an Diprerenlarven. Verh Dt Zool Ges 1956:301–305Google Scholar
  75. Séguy E (1934) Anthomyzidae. In: Diptères (brachycères) (Muscidae Acalyptratae et Scatophagidae). Faune de France 28:301–305Google Scholar
  76. Semelbauer M, Kozánek M (2012) Morphology of preimaginal stages of Lauxania and Calliopum (Diptera: Lauxaniidae). Zootaxa 3346:1–28CrossRefGoogle Scholar
  77. Sinclair BJ (1992) A phylogenetic interpretation of the Brachycera (Diptera) based on the larval mandible and associated mouthpart structures. Syst Entomol 17:233–252CrossRefGoogle Scholar
  78. Sinclair BJ, Cumming JM (2006) The morphology, higher-level phylogeny and classification of the Empidoidea (Diptera). Zootaxa 1180(1):172CrossRefGoogle Scholar
  79. Smith KVG (1989) An introduction to the immature stages of British flies. Handbk Ident Br Insects 10:1–280Google Scholar
  80. Smith SA, Beaulieu JM, Donoghue MJ (2010) An uncorrelated relaxed-clock analysis suggests an earlier origin for flowering plants. Proc Natl Acad Sci USA 107:5897–5902PubMedCrossRefPubMedCentralGoogle Scholar
  81. Snodgrass RE (1953) The metamorphosis of a fly’s head. Smithsonian Misc Colls 122:1–25Google Scholar
  82. Stubbs AE, Drake M (2001) British soldierflies and their allies. British Entomological & Natural History Society, ReadingGoogle Scholar
  83. Stuke J-H (2000) Phylogenetische rekonstruktion der verwandtschaftsbeziehungen innerhalb der gattung Cheilosia Meigen, 1822 anhand der larvenstadien (Diptera: Syrphidae). Stud Dipterol Suppl 8:1–118Google Scholar
  84. Teskey HJ (1981) Morphology and terminology – Larvae. In: McAlpine J, Peterson BV, Shewell GE, Teskey HJ, Vockeroth JR, Wood DM (eds) Manual Nearctic Diptera 1:65–88Google Scholar
  85. Trautwein MD, Wiegmann BM, Beutel R, Kjer KM, Yeates DK (2012) Advances in insect phylogeny at the dawn of the postgenomic era. Annu Rev Entomol 57:449–468PubMedPubMedCentralCrossRefGoogle Scholar
  86. Vijendravarma RK, Narasimha S, Kawecki1 TJ (2013) Predatory cannibalism in Drosophila melanogaster larvae. Nat Commun 4:1789 doi:  https://doi.org/10.1038/ncomms2744
  87. Wang JW, Sylwester AW, Reed D, Wu D-A, Soll DR, Wu X-F (1997) Morphometric description of the wandering behavior in Drosophila larvae: aberrant locomotion in Na+ and K+ channel mutants revealed by computer-assisted motion analysis. J Neurogen 11:231–254CrossRefGoogle Scholar
  88. Wheeler QD (2008) Undisciplined thinking: morphology and Hennig’s unfinished revolution. Syst Entomol 33:2–7CrossRefGoogle Scholar
  89. 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 Nat Acad Sci 108:5690–5695PubMedCrossRefPubMedCentralGoogle Scholar
  90. Wikström N, Savolainen V, Chase MW (2001) Evolution of the angiosperms: calibrating the family tree. Proc R Soc Lond B 268:2211–2220CrossRefGoogle Scholar
  91. Wilkinson G, Rotheray GE (2017) Melanostoma scalare (Meigen) larvae (Diptera, Syrphidae) feed on Diptera larvae in leaf litter. Dipter Digest 24:53–60Google Scholar
  92. Wipfler B, Schneeberg K, Löffler A, Hünefeld F, Meier R, Beutel RG (2013) The skeletomuscular system of the larva of Drosophila melanogaster (Drosophilidae, Diptera) – a contribution to the morphology of a model organism. Arthrop Struct Dev 42:47–68CrossRefGoogle Scholar
  93. Yang AS (2001) Modularity, evolvability, and adaptive radiations: a comparison of the hemi- and holometabolous insects. Evol Develop 3:59–72CrossRefGoogle Scholar
  94. Yeates DK, Wiegmann BM, Courtney GW, Meier R, Lambkin C, Pape T (2007) Phylogeny and systematics of Diptera: two decades of progress and prospects. Zootaxa 1668:565–590Google Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

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

Personalised recommendations