Hostname: page-component-848d4c4894-x24gv Total loading time: 0 Render date: 2024-05-01T13:07:17.729Z Has data issue: false hasContentIssue false

The bug-killer fly Gymnosoma rotundatum (L.) (Diptera: Tachinidae) forms the respiratory funnel independently of the host's immune response

Published online by Cambridge University Press:  17 April 2024

Shin Komagata*
Affiliation:
Graduate School of Integrated Science for Global Society, Kyushu University, 744 Motooka, Nishi-ku, Fukuoka 819-0395, Japan
Kota Ogawa
Affiliation:
Department of Environmental Changes, Faculty of Social and Cultural Studies, Kyushu University, 774 Motooka, Nishi-ku, Fukuoka 819-0395, Japan Insect Sciences and Creative Entomology Centre, Kyushu University, Fukuoka, 819-0395, Japan
Takuji Tachi
Affiliation:
Department of Environmental Changes, Faculty of Social and Cultural Studies, Kyushu University, 774 Motooka, Nishi-ku, Fukuoka 819-0395, Japan
*
Corresponding author: Shin Komagata; Email: komagatashin@gmail.com

Abstract

In internal parasitism, the respiration strategy within the host's body is as essential as evading attack from the host's immune system. Tachinid flies are parasitoids of terrestrial arthropods, mostly insects, during their larval stage. To obtain oxygen while living in the host body, they build a cylindrical structure known as the respiratory funnel at the aperture opened by the tachinid larva on the host integument or trachea. These funnels can be divided morphologically into sheath and cone types. Previous research on sheath-type funnels revealed that they are derived from the encapsulating substance produced by the host's immune system. In contrast, the cone-type funnels cover part of the body of the larval tachinid and may be constructed independently from the host immune system. To determine the mechanisms of cone-type funnel formation, histological observations were carried out on Gymnosoma rotundatum (L.) (Diptera: Tachinidae), which possesses this type of funnel. The respiratory funnel of G. rotundatum was found to be derived from the tube-shaped faeces wrapped with the peritrophic membrane and excreted by the fly larva, not from host tissue or haemocytes. Additionally, secretory glands putatively involved in the funnel formation were discovered around the larval anal plate of G. rotundatum. A comparison of funnel types within Tachinidae revealed that Phasiinae and Dexiinae have cone-type funnels, which may be created by the same mechanism as in G. rotundatum. These new findings suggest that funnel formation that does not use the host immune system is relevant to tachinid phylogeny.

Type
Research Paper
Copyright
Copyright © The Author(s), 2024. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Askew, RR (1971) Protelean parasitic Diptera. In Askew, RR (ed.), Parasitic Insects. London: Heinemann Educational Books Ltd, pp. 185210.Google Scholar
Belshaw, R (1994) Life history characteristics of Tachinidae (Diptera) and their effect on polyphagy. In Hawkins, BA and Sheehan, W (eds), Parasitoid Community Ecology. Oxford: Oxford University Press, pp. 145162.CrossRefGoogle Scholar
Cerretti, P, O'Hara, JE, Wood, DM, Shima, H, Inclan, DJ and Stireman, JO III (2014) Signal through the noise? Phylogeny of the Tachinidae (Diptera) as inferred from morphological evidence. Systematic Entomology 39, 335353.CrossRefGoogle Scholar
Clausen, CP (1940) Entomophagous Insects. New York: Hafner Publication.Google Scholar
Clausen, CP, King, JL and Teranishi, C (1927) The parasites of Popillia japonica in Japan and Chosen (Korea), and their introduction into the United States. Bulletin of the United States Department of Agriculture 1429, 155.Google Scholar
Durham, B and Grodowitz, MJ (2012) The anal plates of larval Hydrellia pakistanae (Diptera/Ephydridae). Florida Entomologist 95, 8288.CrossRefGoogle Scholar
Eggleton, P and Gaston, KJ (1992) Tachinid host ranges: a reappraisal (Diptera: Tachinidae). Entomologist's Gazette 43, 139143.Google Scholar
Eggleton, P and Belshaw, R (1993) Comparisons of dipteran, hymenopteran and coleopteran parasitoids: provisional phylogenetic explanations. Biological Journal of the Linnean Society 48, 213226.CrossRefGoogle Scholar
Feener, DH Jr and Brown, BV (1997) Diptera as parasitoids. Annual Review of Entomology 42, 7397.CrossRefGoogle ScholarPubMed
Gullan, PJ and Cranston, PS (2014) The Insects: An Outline of Entomology, 5th Edn. Chichester: Wiley.Google Scholar
Herting, B (1960) Biologie der westpaläarktischen Raupenfliegen. Dipt., Tachinidae. Monographien zur angewandte Entomologie 16, 1188.Google Scholar
Herting, B (1984) Catalogue of Palearctic Tachinidae (Diptera). Stuttgarter Beiträge zur Naturkunde Serie A Biologie 369, 1228.Google Scholar
Higaki, M (2003) Development of a tachinid parasitoid, Gymnosoma rotundatum (Diptera: Tachinidae) on Plautia crossota stali (Heteroptera: Pentatomidae), and its effects on host reproduction. Applied Entomology and Zoology 38, 215223.CrossRefGoogle Scholar
Higaki, M and Adachi, I (2011) Response of a parasitoid fly, Gymnosoma rotundatum (Linnaeus) (Diptera: Tachinidae) to the aggregation pheromone of Plautia stali Scott (Hemiptera: Pentatomidae) and its parasitism of hosts under field conditions. Biological Control 58, 215221.CrossRefGoogle Scholar
Lackie, AM (1988) Immune mechanisms in insects. Parasitology Today 4, 98105.CrossRefGoogle ScholarPubMed
Lavine, MD and Strand, MR (2002) Insect hemocytes and their role in cellular immune responses. Insect Biochemistry and Molecular Biology 32, 12371242.CrossRefGoogle Scholar
Mellini, E (1990) Sinossi di biologia dei Ditteri Larvavoridi. Bollettino dell'Istituto di Entomologia ‘Guido Grandi’, University of Bologna 45, 138.Google Scholar
Nutting, WL (1953) The biology of Euphasiopteryx brevicornis (Townsend) (Diptera: Tachinidae), parasitic in the cone-headed grasshoppers (Orthoptera, Copiphorinae). Psyche 60, 6981.CrossRefGoogle Scholar
O'Hara, JE and Wood, DM (2004) Catalogue of the Tachinidae (Diptera) of America north of Mexico. Memoirs of Entomology, International 18, 1410.Google Scholar
Pantel, J (1910) Caracteres parasitiques aux points de vue biologique, ethologique et histologique. Recherches sur les dipteres a larves entomobiles. La Cellule 26, 27216.Google Scholar
Prell, H (1915) Zur Biologie der Tachinen Parasetigena segregata Rdi. und Panzeria rudis Fall. Zeitschrift für Angewandte Entomologie 2, 57148.CrossRefGoogle Scholar
Prescott, HW (1961) Respiratory pore construction in the host by the nemestrinid parasite Neorhynchocephalus sackenii (Diptera), with notes on respiratory tube characters. Annals of the Entomological Society of America 54, 557566.CrossRefGoogle Scholar
Salt, G (1968) The resistance of insect parasitoids to the defence reactions of their hosts. Biological Reviews of the Cambridge Philosophical Society 43, 200232.CrossRefGoogle Scholar
Schwantes, PA and Seibold, G (1991) Ion-absorption by specialized epithelial regions in Musca domestica larvae. Journal of Insect Physiology 37, 211221.CrossRefGoogle Scholar
Schwier, N, Zhang, K, Nakamura, S and Furukawa, S (2021) Larvae of the tachinid fly, Drino inconspicuoides (Diptera: Tachinidae), suppress melanization in host lepidopteran insects. Journal of Asia-Pacific Entomology 24, 10501054.CrossRefGoogle Scholar
Stireman, JOIII, Cerretti, P, O'Hara, JE, Blaschke, JD and Moulton, JK (2019) Molecular phylogeny and evolution of world Tachinidae (Diptera). Molecular Phylogenetics and Evolution 139, 106358.CrossRefGoogle ScholarPubMed
Teskey, HJ (1981) Morphology and terminology -larvae 3. In McAlpine, JF, Peterson, BV, Shewell, GE, Teskey, HJ, Vockeroth, JR and Wood, DM (eds), Agriculture Canada Monograph 27. Manual of Nearctic Diptera, vol. 1. Ottawa: Agriculture Canada, pp. 6588.Google Scholar
Thompson, WR (1920) Sur cyrillia angustifrons bond., tachinaire parasite d'un isopode tebrestre. Comptes Rendus de l'Académie des Sciences 170, 16211622.Google Scholar
Thompson, WR (1934) The tachinid parasites of woodlice. Parasitology 26, 378448.CrossRefGoogle Scholar
Thorpe, KW and Harrington, BJ (1979) Observations of seed-bug (Hemiptera: Lygaeidae) parasitism by a species of Catharosia (Diptera: Tachinidae). Psyche 86, 399405.CrossRefGoogle Scholar
Tschorsnig, H-P (2017) Preliminary host catalogue of Palaearctic Tachinidae (Diptera). Version 1. PDF document, 480 pp. Available at http://www.nadsdiptera.org/Tach/WorldTachs/CatPalHosts/Home.htmlGoogle Scholar
Valigurová, A, Michalková, V, Konik, P, Dindo, ML, Gelnar, M and Vanhara, J (2014) Penetration and encapsulation of the larval endoparasitoid Exorista larvarum (Diptera: Tachinidae) in the factitious host Galleria mellonella (Lepidoptera: Pyralidae). Bulletin of Entomological Research 104, 203212.CrossRefGoogle ScholarPubMed
Wood, DM (1987) Rhinophoridae. In McAlpine, JF, Peterson, BV, Shewell, GE, Teskey, HJ, Vockeroth, JR and Wood, DM (eds), Manual of Nearctic Diptera, vol. 2. Agriculture Canada Monograph 28, pp. 11871191.Google Scholar
Yamashita, K, Zhang, K, Ichiki, R, Nakamura, T and Furukawa, S (2019) Novel host immune evasion strategy of the endoparasitoid Drino inconspicuoides. Bulletin of Entomological Research 109, 643648.CrossRefGoogle ScholarPubMed
Supplementary material: File

Komagata et al. supplementary material

Komagata et al. supplementary material
Download Komagata et al. supplementary material(File)
File 4 MB