Published January 4, 2019 | Version v1
Journal article Restricted

Fat in the Leg: Function of the Expanded Hind Leg in Gasteruptiid Wasps (Hymenoptera: Gasteruptiidae)

  • 1. Frost Entomological Museum, Department of Entomology, The Pennsylvania State University, University Park, PA,
  • 2. Materials Research Institute, Pennsylvania State University, University Park, PA,
  • 3. School of Life Sciences, Arizona State University, Tempe,AZ,
  • 4. Laboratory for Applications of Synchrotron Radiation,Karlsruhe Institute of Technology, Kaiserstr. 12, 76131 Karlsruhe, Germany,
  • 5. Biological Sciences,College of Science and Engineering,Flinders University,Adelaide, SA 5001,Australia,
  • 6. Department of Terrestrial Zoology, Western Australian Museum, Welshpool, Perth, WA 6986, Australia,

Description

Mikó, István, Rahman, Sarthok Rasique, Anzaldo, Salvatore S., Kamp, Thomas van de, Parslow, Ben A., Tatarnic, Nikolai J., Wetherington, Maxwell T., Anderson, Julie, Schilder, Rudolf J., Ulmer, Jonah M., Deans, Andrew R., Hines, Heather M. (2019): Fat in the Leg: Function of the Expanded Hind Leg in Gasteruptiid Wasps (Hymenoptera: Gasteruptiidae). Insect Systematics and Diversity 3 (2019), No. 2: 1-16, DOI: 10.1093/isd/ixy020, URL: http://dx.doi.org/10.1093/isd/ixy020

Files

Restricted

The record is publicly accessible, but files are restricted to users with access.

Linked records

Additional details

Identifiers

LSID
urn:lsid:plazi.org:pub:B808FFF37C750C2BFF87FF958E266755

References

  • van Achterberg, K. 2013. De Nederlandse hongerwespen (Hymenoptera: Evanioidea: Gasteruptiidae). Nederlandse Faunistische Mededelingen. 39: 55-87. Available from http://www.repository.naturalis.nl/record/586890
  • van Achterberg, C., and A. A. Talebi. 2014. Review of Gasteruption Latreille (Hymenoptera, Gasteruptiidae) from Iran and Turkey, with the description of 15 new species. ZooKeys. 458: 1-187.
  • Aguiar, A. P., A. R. Deans, M. S. Engel, M. Forshage, J. T. Huber, J. T. Jennings, N. F. Johnson, A. S. Lelej, J. T. Longino, V. Lohrmann, et al. 2013. Order Hymenoptera. Zootaxa. 3703: 51-62.
  • Amsalem, E., O. Malka, C. Grozinger, and A. Hefetz. 2014. Exploring the role of juvenile hormone and vitellogenin in reproduction and social behavior in bumble bees. BMC Evol. Biol. 14: 45.
  • Amsalem, E., M. Padilla, P. M. Schreiber, N. S. Altman, A. Hefetz, and C. M. Grozinger. 2017. Do bumble bee, Bombus impatiens, queens signal their reproductive and mating status to their workers? J. Chem. Ecol. 43: 563-572.
  • Andrews, S. 2010. FastQC:a quality control tool for high throughput sequence data. Available from http://www.bioinformatics.babraham.ac.uk/projects/ fastqc
  • Arrese, E. L., and J. L. Soulages. 2009. Insect fat body: energy, metabolism, and regulation. Ann. Rev. Entomol. 55: 207-225.
  • Autrum, H., and W. Schneider. 1948. Vergleichende untersuchungen uber den erschutterungssinn der insekten. Zeitschrift fur vergleichende Physiologie. 31: 77-88.
  • Ballan-Dufrancais, C. 2002. Localization of metals in cells of pterygote insects. Microsc. Res. Tech. 56: 403-420.
  • Barth, A. 2007. Infrared spectroscopy of proteins. Biochim. Biophys. Acta. 1767: 1073-1101.
  • Baumann, P., N. A. Moran, and L. C. Baumann. 2013. Bacteriocyte-associated endosymbionts of insects, pp. 465-496. In E. Rosenberg, E. F. DeLong, S. Lory, E. Stackebrandt, and F. Thompson (eds.), The prokaryotes. Springer, Berlin, Germany.
  • Belazi, D., S. Sole-Domenech, B. Johansson, M. Schalling, and P. Sjovall. 2009. Chemical analysis of osmium tetroxide staining in adipose tissue using imaging ToF-SIMS. Histochem. Cell Biol. 132: 105-115.
  • Bolger, A. M., M. Lohse, and B. Usadel. 2014. Trimmomatic: a flexible trimmer for illumina sequence data. Bioinformatics. 30: 2114-20.
  • Bordier, C., H. Dechatre, S. Suchail, M. Peruzzi, S. Soubeyrand, M. Pioz, M. Pelissier, D. Crauser, Y. L. Conte, and C. Alaux. 2017a. Colony adaptive response to simulated heat waves and consequences at the individual level in honeybees (Apis mellifera). Sci. Rep. 7: 3760.
  • Bordier, C., S. Suchail, M. Pioz, J. M. Devaud, C. Collet, M. Charreton, Le Y. Conte, and C. Alaux. 2017b. Stress response in honeybees is associated with changes in task-related physiology and energetic metabolism. J. Insect Physiol. 98: 47-54.
  • Bray, N. L., H. Pimentel, P. Melsted, and L. Pachter. 2016. Near-optimal probabilistic RNA-seq quantification. Nat. Biotechnol. 34: 525-527.
  • Brito, N. F., M. F. Moreira, and A. C. A. Melo. 2016. A look inside odorantbinding proteins in insect chemoreception. J. Insect Physiol. 95: 51-65.
  • Broad, G. R., and D. L. J. Quicke. 2000. The adaptive significance of host location by vibrational sounding in parasitoid wasps. Proc. R. Soc. Lond. B Biol. Sci. 267: 2403-2409.
  • Bruno, D., G. Grossi, R. Salvia, A. Scala, D. Farina, A. Grimaldi, J-J. Zhou, S. A. Bufo, H. Vogel, E. Grosse-Wilde, et al. 2018. Sensilla morphology and complex expression pattern of odorant binding proteins in the vetch aphid Megoura viciae (Hemiptera: Aphididae). Front. Physiol. 9: 777. doi:10.3389/fphys.2018.00777
  • Cecilia, A., A. Rack, P. A. Douissard, T. Martin, dos Santos T. Rolo, P. Vagovi c, E. Hamann, van de T. Kamp, A. Riedel, M. Fiederle, et al. 2010. LPE grown LSO:Tb scintillator films for high-resolution X-ray imaging applications at synchrotron light sources. Nucl. Instrum. Methods Phys. Res. A 648 (Suppl. 1): S321-S323.
  • Clark, M. K., P.A. Dahm. 1973. Phenobarbital-induced, membrane-like scrolls in the oenocytes of Musca domestica Linnaeus. J. Cell Biol. 56: 870-875.
  • C okl, A., and M. Virant-Doberlet. 2003. Communication with substrate-borne signals in small plant-dwelling insects. Ann. Rev. Entomol. 48: 29-50.
  • Combes, S. A., and R. Dudley. 2009. Turbulence-driven instabilities limit insect flight performance. Proc. Natl Acad. Sci. USA. 106: 9105-9108.
  • Corona, M., R. A. Velarde, S. Remolina, A. Moran-Lauter, Y. Wang, K. A. Hughes, and G. E. Robinson. 2007. Vitellogenin, juvenile hormone, insulin signaling, and queen honey bee longevity. Proc. Natl Acad. Sci. USA. 104: 7128-7133.
  • Cousin, M., E. Silva-Zacarin, A. Kretzschmar, M. El Maataoui, J-L. Brunet, and L. P. Belzunces. 2013. Size changes in honey bee larvae oenocytes induced by exposure to paraquat at very low concentrations. PLoS One. 8: 1-7.
  • Crosskey, R. W. 1962. The classification of the Gasteruptiidae (Hymenoptera). Trans. R. Entomol. Soc. Lond. 114: 377-402.
  • 1999. Cloning of a novel cytochrome P450 (CYP4C15) differentially expressed in the steroidogenic glands of an arthropod. Biochem. Biophys. Res. Commun. 264: 413-418.
  • Dean, R. L., M. Locke, and J. V. Collins. 1985. Structure of the fat body, pp. 155-209. In G. A. Kierkut and L. T. Gilbert (eds.), Comparative insect physiology, biochemistry and pharmacology, vol. 3. Pergamon Press, Oxford, United Kingdom.
  • De Biasio, F., L. Riviello, D. Bruno, A. Grimaldi, T. Congiu, Y. F. Sun, and P. Falabella. 2015. Expression pattern analysis of odorant-binding proteins in the pea aphid Acyrthosiphon pisum. Insect Sci. 22: 220-234.
  • Devetak, D., and M. A. Pabst. 1994. Structure of the subgenual organ in the green lacewing, Chrysoperla carnea. Tissue Cell. 26: 249-257.
  • Dippel, S., G. Oberhofer, J. Kahnt, I. Gerischer, L. Opitz, J. Schachtner, M. Stanke, S. Schutz, A. Ernst, E. A. Wimmer, et al. 2014. Tissue-specific transcriptomics, chromosomal localization, and phylogeny of chemosensory and odorant binding proteins from the red flour beetle Tribolium castaneum reveal subgroup specificities for olfaction or more general functions. BMC Genomics. 15: 1141.
  • Dugard, J. J. 1967. Directional change in flying locusts. J. Insect Physiol. 13: 1055-1063.
  • Edgecomb, R. S., D. Robert, M. P. Read, and R. R. Hoy. 1995. The tympanal hearing organ of a fly: phylogenetic analysis of its morphological origins. Cell Tissue Res. 282: 251-268.
  • Fontanetti, C. S., B. Tiritan, and M. I. Camargo-Mathias. 2006. Mineralized bodies in the fat body of Rhinocricus padbergi (Diplopoda). Braz. J. Morphol. Sci. 23: 487-493.
  • Gotz, K. G., B. Hengstenberg, and R. Biesinger. 1979. Optomotor control of wing beat and body posture in Drosophila. Biol. Cyber. 35: 101-112.
  • Gotz, S., J. M. Garcia-Gomez, J. Terol, T. D. Williams, S. H. Nagaraj, M. J. Nueda, M. Robles, M. Talon, J. Dopazo, and A. Conesa. 2008. Highthroughput functional annotation and data mining with the Blast2GO suite. Nucleic Acids Res. 36: 3420-3435.
  • Grabherr, M. G., B. J. Haas, M. Yassour, J. Z. Levin, D. A. Thompson, I. Amit, X. Adiconis, L. Fan, R. Raychowdhury, Q. Zeng, et al. 2011. Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat. Biotechnol. 29: 644-652.
  • Gramates, L. S., S. J. Marygold, G. D. Santos, M. Urbano, G. Antonazzo, B. B. Matthews, A. J. Rey, C. J. Tabone, M. A. Crosby, Emmert, et al. 2017. FlyBase at 25: looking to the future. Nucleic Acids Res. 45: D663-DD671.
  • Grieve, A. C., Barnden, B. L., Howell, R. M., Kanishka, A. M., Stevens, M. I., Schwarz, M. P. and Parslow, B. A. 2018. Reproductive ethology of the Fijian predator-inquiline wasp Pseudofoenus extraneus (Hymenoptera: Gasteruptiidae: Hyptiogastrinae). Trans. R. Soc. S. Aust. 142: 122-129.
  • Gronke, S., A. Mildner, S. Fellert, N. Tennagels, S. Petry, G. Muller, H. Jackle, and R. P. Kuhnlein. 2005. Brummer lipase is an evolutionary conserved fat storage regulator in Drosophila. Cell Metab. 1: 323-330.
  • Gronke, S., G. Muller, J. Hirsch, S. Fellert, A. Andreou, T. Haase, H. Jackle, and R. P. Kuhnlein. 2007. Dual lipolytic control of body fat storage and mobilization in Drosophila. PLOS Biol. 5: e137.
  • Gutierrez, E., D. Wiggins, B. Fielding, and A. P. Gould. 2007. Specialized hepatocyte-like cells regulate Drosophila lipid metabolism. Nature. 445: 275-280.
  • Haunerland, N. H., and P. D. Shirk. 1995. Regional and functional differentiation in the insect fact body. Ann. Rev. Entomol. 40: 121-145.
  • Hepburn, H., R. Bernard, B. Davidson, W. Muller, P. Lloyd, S. Kurstjens, and S. Vincent. 1991. Synthesis and secretion of beeswax in honeybees. Apidologie. 22: 21-36.
  • Huang, D. W., T. B. Sherman, and R. A. Lempicki. 2009. Systematic and integrative analysis of large gene lists using DAVID Bioinformatics Resources. Nat. Protoc. 4: 44-57.
  • Iovinella, I., F. R. Dani, A. Niccolini, S. Sagona, E. Michelucci, A. Gazzano, S. Turillazzi, A. Felicioli, and P. Pelosi. 2011. Differential expression of odorant-binding proteins in the mandibular glands of the honey bee according to caste and age. J. Proteome Res. 10: 3439-3449.
  • Jennings, J. T., and A. D. Austin. 2002. Systematics and distribution of world hyptiogastrine wasps (Hymenoptera:Gasteruptiidae). Invertebr. Syst. 16: 735811.
  • Jennings, J. T., and A. D. Austin. 2004. Biology and host relationships of aulacid and gasteruptiid wasps (Hymenoptera: Evanioidea): a review. Perspect. Biosyst. Biodivers. 2004: 187-215.
  • Jensen, P. V., and L. W. BOrgesen. 2000. Regional and functional differentiation in the fat body of pharaoh's ant queens, Monomorium pharaonis (L.). Arthropod Struct. Dev. 29: 171-184.
  • Jennings, J. T., H. Jourdan, L. Krogmann, and B. A. Parslow. 2015. The gasteruptiid wasp fauna of New Caledonia, with description of three new species of Gasteruption (Hymenoptera: Evanioidea: Gasteruptiidae). Zootaxa. 3947: 397-406.
  • Kilpinen, O., and J. Storm. 1997. Biophysics of the subgenual organ of the honeybee, Apis mellifera. J. Comp. Physiol. A. 181: 309-318.
  • Kim, I. H., V. Pham, W. Jablonka, W. G. Goodman, J. M. C. Ribeiro, and J. F. Andersen. 2017. A mosquito hemolymph odorant-binding protein family member specifically binds juvenile hormone. J. Biol. Chem. 292: 15329-15339.
  • Krupp, J. J., and J. D. Levine. 2010. Dissection of oenocytes from adult Drosophila melanogaster. J. Vis. Exp. JoVE 41: 2242. doi:10.3791/2242
  • Lakes-Harlan, R., T. deVries, H. Stolting, and A. Stumpner. 2014. Useless hearing in male Emblemasoma auditrix (Diptera, Sarcophagidae) - a case of intralocus sexual conflict during evolution of a complex sense organ? PLoS One 9: e87211.
  • Larsen, O. N., G. Gleffe, and J. Tengo. 1986. Vibration and sound communication in solitary bees and wasps. Physiol. Entomol. 11: 287-296.
  • Larter, N. K., J. S. Sun, and J. R. Carlson. 2016. Organization and function of Drosophila odorant binding proteins. eLife. 5: e20242.
  • Li, H., and S. Zhang. 2017. Functions of vitellogenin in eggs. Results Probl Cell Differ. 63: 389-401. doi:10.1007/978-3-319-60855-6_17.
  • Lin, Y., W. Rossler, and K. Kalmring. 1995. Morphology of the tibial organs of acrididae: comparison of subgenual and distal organs in fore-, mid-, and hindlegs of Schistocerca gregaria (Acrididae, Catantopinae) and Locusta migratoria (Acrididae, Oedipodinae). J. Morphol. 226: 351-360.
  • Locke, M. 1969. The ultrastructure of the oenocytes in the molt/intermolt cycle of an insect. Tissue Cell. 1: 103-154.
  • Locke, M. 1988. Lipids of the insect cuticle: origin, composition and function. Comp. Biochem. Physiol. B. 89: 595-645.
  • Lomas, K. F., D. R. Greenwood, J. F. Windmill, J. C. Jackson, J. Corfield, and S. Parsons. 2012. Discovery of a lipid synthesising organ in the auditory system of an insect. PLoS One. 7: e51486.
  • Lorez, M. 1995. Neural control of hindleg steering in flight in the locust. J. Exp. Biol. 198: 869-875.
  • Madden, T. 2002. The BLAST sequence analysis tool. In J. McEntyre and J. Ostell (eds.), The NCBI handbook [Internet]. National Center for Biotechnology Information (US), Bethesda, MD. Chapter 16. Available from http://www.ncbi.nlm.nih.gov/books/NBK21097/
  • Makki, R., E. Cinnamon, and A. P. Gould 2014. The development and functions of oenocytes. Ann. Rev. Entomol. 59: 405-425.
  • Martins, G. F., and J. M. Ramalho-Ortigao. 2012. Oenocytes in insects. Invertebr. Surv. J. 9: 139-152.
  • Matsui, Y., and M. Eguchi. 1991. Purification and relationship of chymotrypsin inhibitors from the fat body and haemolymph of the silkworm, Bombyx mori. Comp. Biochem. Physiol. B. 99: 851-857.
  • McIndoo, N. E. 1922. The auditory sense of the honey-bee. J. Comp. Neurol. 34: 173-199.
  • Miko, I., and Deans, A. R. 2013. What is fluorescing? Hamuli. 4: 19-22.
  • Menzel, J. G., and J. Tautz. 1994. Functional morphology of the subgenual organ of the carpenter ant. Tissue Cell. 26: 735-746.
  • Nishino, H., H. Mukai, and T. Takanashi. 2016. Chordotonal organs in hemipteran insects: unique peripheral structures but conserved central organization revealed by comparative neuroanatomy. Cell Tissue Res. 366: 549-572.
  • Nowel, M., P. Shelton, and R. Stephen. 1995. Functional organisation of the metathoracic femoral chordotonal organ in the cricket Acheta domesticus. J. Exp. Biol. 198: 1977-1988.
  • Oakeshott, J. G., R. M. Johnson, M. R. Berenbaum, H. Ranson, A. S. Cristino, and C. Claudianos. 2010. Metabolic enzymes associated with xenobiotic and chemosensory responses in Nasonia vitripennis. Insect Mol. Biol. 19: 147-163.
  • Park, M. S., P. Park, and M. Takeda. 2013. Roles of fat body trophocytes, mycetocytes and urocytes in the American cockroach, Periplaneta americana under starvation conditions: an ultrastructural study. Arthropod Struct. Dev. 42: 287-295.
  • Parslow, B. A., M. I. Stevens, and M. P. Schwarz. 2018. First record of Gasteruption Latreille (Hymenoptera: Evanioidea: Gasteruptiidae) from Fiji with the description of a new species. Zootaxa. 4407: 111-116.
  • Pelosi, P., J. J. Zhou, L. P. Ban, and M. Calvello. 2006. Soluble proteins in insect chemical communication. Cell. Mol. Life Sci. 63: 1658-1676.
  • Romer, F. 1974. Ultrastructural changes of the oenocytes of Gryllus bimaculatus DEG (Saltatoria, Insecta) during the moulting cycle. Cell Tissue Res. 151: 27-46.
  • dos Santos Rolo, T., A. Ershov, T. van de Kamp, and T. Baumbach. 2014. In vivo X-ray cine-tomography for tracking morphological dynamics. Proc. Natl Acad. Sci. USA. 111: 3921-3926.
  • Saure, C., C. Schmid-Egger, and C. van Achterberg. 2017. Order Hymenoptera, family Gasteruptiidae, pp. 190-224. In A. van Harten (ed.), Arthropod fauna of the UAE, vol. 6. Department of the President's Affairs,Abu Dhabi.
  • Schindelin, J., I. Arganda-Carreras, E. Frise, V. Kaynig, M. Longair, T. Pietzsch, S. Preibisch, C. Rueden, S. Saalfeld, B. Schmid, et al. 2012. Fiji: an open-source platform for biological-image analysis. Nat. Methods. 9: 676-682.
  • Schindelin, J., Rueden, C. T., Hiner, M. C. and Eliceiri, K. W. 2015. The ImageJ ecosystem: an open platform for biomedical image analysis. Mol. Reprod. Dev. 82: 518-529.
  • Scimeca, M., S. Bischetti, H. K. Lamsira, R. Bonfiglio, and E. Bonanno. 2018. Energy Dispersive X-ray (EDX) microanalysis: a powerful tool in biomedical research and diagnosis. Eur. J. Histochem. 62: 2841.
  • Scimeca, M., M. Feola, L. Romano, C. Rao, E. Gasbarra, E. Bonanno, M. L. Brandi, and U. Tarantino. 2017. Heavy metals accumulation affects bone microarchitecture in osteoporotic patients. Environ. Toxicol. 32: 1333-1342.
  • Sekkoum, K., A. Cheriti, S. Taleb, and N. Belboukhari. 2016. FTIR spectroscopic study of human urinary stones from El Bayadh district (Algeria). Arab. J. Chem. 9: 330-334.
  • Shaw, S. R. 1994. Re-evaluation of the absolute threshold and response mode of the most sensitive known "vibration" detector, the cockroach's subgenual organ: a cochlea-like displacement threshold and a direct response to sound. J. Neurobiol. 25: 1167-1185.
  • Snodgrass, R. E. 1910. The anatomy of the honey bee. Cornell University Press, Ithaca, NY. pp. 162.
  • Socrates, G. 1980. Infrared and Raman characteristic group frequencies. John Wiley & Sons, Chichester, United Kingdom. pp. 347.
  • Strauss, J., K. Lomas, and L. H. Field. 2017. The complex tibial organ of the New Zealand ground weta: sensory adaptations for vibrational signal detection. Sci. Rep. 7: 2031.
  • Sun, Y. F., De Biasio, F., H. L. Qiao, I. Iovinella, S. X. Yang, Y. Ling, L. Riviello, D. Battaglia, P. Falabella, X. L. Yang, et al. 2012. Two odorant-binding proteins mediate the behavioral response of aphids to the alarm pheromone (E)-β- farnesene and structural analogues. PLoS One. 7: e32759.
  • Tan, J-L., C. van Achterberg, Q-Q. Tan, X-X. Chen. 2016. Four new species of Gasteruption Latreille from NW China, with an illustrated key to the species from Palaearctic China (Hymenoptera, Gasteruptiidae). ZooKeys. 612: 51-112.
  • Taylor, G. K. 2001. Mechanics and aerodynamics of insect flight control. Biol. Rev. 76: 449-471.
  • Vilhelmsen, L., N. Isidoro, R. Romani, H. H. Basibuyuk, and D. L. J. Quicke. 2001. Host location and oviposition in a basal group of parasitic wasps: the subgenual organ, ovipositor apparatus and associated structures in the Orussidae (Hymenoptera, Insecta). Zoomorphology. 121: 63-84.
  • Vilhelmsen, L., I. Miko, and L. Krogmann. 2010. Beyond the wasp-waist: structural diversity and phylogenetic significance of the mesosoma in apocritan wasps (Insecta: Hymenoptera). Zool. J. Linn. Soc. 159: 22-194.
  • Vilhelmsen, L., G. F. Turrisi, and R. G. Beutel. 2008. Distal leg morphology, subgenual organs and host detection in Stephanidae (Insecta, Hymenoptera). J. Nat. Hist. 42: 1649-1663.
  • Weers, P. M., and R. O. Ryan. 2006. Apolipophorin III: role model apolipoprotein. Insect Biochem. Mol. Biol. 36: 231-240.