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Morphological allometry and intersexuality in horsehair-worm-infected mantids, Hierodula formosana (Mantodea: Mantidae)

Published online by Cambridge University Press:  20 April 2015

MING-CHUNG CHIU ,
CHIN-GI HUANG ,
WEN-JER WU  and
SHIUH-FENG SHIAO
MING-CHUNG CHIU
Affiliation:
Department of Entomology, National Taiwan University, Taipei 106, Taiwan
CHIN-GI HUANG
Affiliation:
Department of Entomology, National Taiwan University, Taipei 106, Taiwan
WEN-JER WU
Affiliation:
Department of Entomology, National Taiwan University, Taipei 106, Taiwan
SHIUH-FENG SHIAO*
Affiliation:
Department of Entomology, National Taiwan University, Taipei 106, Taiwan
*
* Corresponding author: Department of Entomology, National Taiwan University, Taipei 106, Taiwan. E-mail: sfshiao@ntu.edu.tw
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Summary

Parasitic castration is a strategy used by parasites to minimize damage to the host by consuming its reproductive system, which results in the morphological alteration of the host. We determined that the forewing shape and density of the antennal sensilla of field-collected adult male mantids (Hierodula formosana), infected by horsehair worms (Chordodes formosanus) was partially feminized (intersexuality), and both male and female mantids infected by horsehair worms exhibited allometric changes in their wings and walking legs. In addition, the testes of most infected male adults disappeared or reduced in size, whereas the number of ovarioles in infected female adults was unaffected. The infection mainly influenced the structures related to host reproduction and locomotion, suggesting unbalanced energy exploitation and the reduction of parasitic virulence. In addition, the intersexuality of infected male adults indicated that sexual differentiation in insects, which researchers have considered to be an autonomous process, was influenced by the infection. The similarity of the antennae of infected male adults with those of last-instar female nymphs suggested that parasitic juvenilization may cause such feminization, but the mechanism of parasitic influence on insect sex characteristics should be studied further.

Keywords

allometryintersexualityparasitic castrationmantidshorsehair worms

Information

Type
Research Article
Information
Parasitology , Volume 142 , Issue 8 , July 2015 , pp. 1130 - 1142
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Copyright
Copyright © Cambridge University Press 2015 

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References

REFERENCES

Abràmoff, M. D., Magalhães, P. J. and Ram, S. J. (2004). Image processing with ImageJ. Biophotonics International 11, 36–42. URL: http://imagej.nih.gov/ij/ Google Scholar
Alizon, S., Hurford, A., Mideo, N. and van Baalen, M. (2009). Virulence evolution and the trade-off hypothesis: history, current state of affairs and the future. Journal of Evolutionary Biology 22, 245–259.Google Scholar
Allen, L. E., Barry, K. L. and Holwell, G. I. (2012). Mate location and antennal morphology in the praying mantid Hierodula majuscula . Australian Journal of Entomology 51, 133–140.Google Scholar
Baudoin, M. (1975). Host castration as a parasitic strategy. Evolution 29, 335–352.CrossRefGoogle ScholarPubMed
Béthoux, O. (2010). Alteration of sex-related developmental modules: a case of ‘feminized’ male wing morphology in Creobroter gemmatus (Mantodea: Hymenopodidae). European Journal of Entomology 107, 133–135.Google Scholar
Biron, D. G., Ponton, F., Joly, C., Menigoz, A., Hanelt, B. and Thomas, F. (2005). Water-seeking behavior in insects harboring hairworms: should the host collaborate? Behavioral Ecology 16, 656–660.Google Scholar
Chiu, M. C., Huang, C. G., Wu, W. J. and Shiao, S. F. (2011). A new horsehair worm, Chordodes formosanus sp. n. (Nematomorpha, Gordiida) from Hierodula mantids of Taiwan and Japan with redescription of a closely related species, Chordodes japonensis . ZooKeys 160, 1–22.Google Scholar
de Loof, A. and Huybrechts, R. (1998). ‘Insects do not have sex hormones’: a myth? General and Comparative Endocrinology 111, 245–260.Google Scholar
DeFalco, T., Camara, N., Le Bras, S. and Van Doren, M. (2008). Non-autonomous sex determination controls sexually dimorphic development of the Drosophila gonad. Developmental Cell 14, 275–286.CrossRefGoogle Scholar
Down, R. E., Bell, H. A., Bryning, G., Kirkbride-Smith, A. E., Edwards, P. J. and Weaver, R. J. (2008). Infection by the microsporidium Vairimorpha necatrix (Microspora: Microsporidia) elevates juvenile hormone titers in larvae of the tomato moth, Lacanobia oleracea (Lepidoptera: Noctuidae). Journal of Invertebrate Pathology 97, 223–229.Google Scholar
Fisher, F. M. and Sanborn, R. C. (1962). Production of insect juvenile hormone by the microsporidian parasite Nosema . Nature 194, 1193.Google Scholar
Hall, S. R., Becker, C. and Ca'ceres, C. E. (2007). Parasitic castration: a perspective from a model of dynamic energy budgets. Integrative and Comparative Biology 47, 295–309.Google Scholar
Hanelt, B., Grother, L. E. and Janovy, J. Jr. (2001). Physid snails as sentinels of freshwater nematomorphs. Journal of Parasitology 87, 1049–1053.CrossRefGoogle ScholarPubMed
Hanelt, B., Thomas, F. and Schmidt-Rhaesa, A. (2005). Biology of the phylum Nematomorpha. Advances in Parasitology 59, 243–305.Google Scholar
Harron, A. L. and Yager, D. D. (1996). Juvenile hormone reduces auditory sensitively in the praying mantis Taumantis ehomanni . Society of Neuroscience Abstract 22, 1144.Google Scholar
Holwell, G. I., Barry, K. L. and Herberstein, M. E. (2007). Mate location, antennal morphology, and ecology in two praying mantids (Insecta: Mantodea). Biological Journal of the Linnaean Society 91, 307–313.CrossRefGoogle Scholar
Hurd, H. (2001). Host fecundity reduction: a strategy for damage limitation? Trends in Parasitology 17, 363–368.Google Scholar
Hurd, H. (2009). Evolutionary drivers of parasite-induced changes in insect life-history traits: from theory to underlying mechanisms. In Advances in Parasitology, Vol 68, Natural History of Host–Parasite Interactions (ed. Webster, J. P.), pp. 85–110.Google Scholar
Hurd, L. E., Prete, F. R., Jones, T. H., Singh, T. B., Co, J. E. and Portman, R. T. (2004). First identification of a putative sex pheromone in a praying mantid. Journal of Chemical Ecology 30, 155–166.CrossRefGoogle Scholar
Klowden, M. J. (2007). Endocrine systems. In Physiological Systems in Insects (ed. Klowden, M. J.), pp. 1–74. Elsevier/Academic Press, Amsterdam.Google Scholar
Kotaki, T., Shinada, T., Kaihara, K., Ohfune, Y. and Numata, H. (2011). Biological activities of juvenile hormone III skipped bisepoxide in last instar nymphs and adults of a stink bug, Plautia stali . Journal of Insect Physiology 57, 147–152.Google Scholar
Lafferty, K. D. and Kuris, A. M. (2009). Parasitic castration: the evolution and ecology of body snatchers. Trends in Parasitology 25, 564–572.Google Scholar
Lombardo, F. and Umbriaco, R. (2011). Taxonomic re-evaluation of Parastagmatoptera abnormis Beier, 1963 (Dictyoptera, Mantidae: Stagmatopterinae): an unusual case of ‘parasite-induced’ synonymy. Zootaxa 2735, 31–34.Google Scholar
Looney, C., Hanelt, B. and Zack, R. S. (2012). New records of nematomorph parasites (Nematomorpha: Gordiida) of ground beetles (Coleoptera: Carabidae) and camel crickets (Orthoptera: Rhaphidophoridae) in Washington state. Journal of Parasitology 98, 554–559.Google Scholar
McKeever, S., Brickle, D. S. and Hagan, D. V. (1997). Mouthparts, antennae and genitalia of intersex Culicoides stellifer parasitized by mermithid nematodes. Medical and Veterinary Entomology 11, 217–222.Google Scholar
Negri, I. and Pellecchia, M. (2012). Sex steroids in insects and the role of the endosymbiont Wolbachia: a new perspective. In Sex Hormones (ed. Dubey, R.), pp. 353–374. InTech Press, Slavka Krautzeka.Google Scholar
Ohba, S. Y., Tatsuta, H. and Sasaki, M. (2006). Raptorial legs and claws are not influenced by food condition in nymphal stages of Lethocerus deyrolli (Heteroptera: Belostomatidae). Annals of the Entomological Society of America 99, 151–156.CrossRefGoogle Scholar
Prete, F. R., Klimek, C. A. and Grossman, S. P. (1990). The predatory strike of the praying mantis, Tenodera aridifolia sinensis . Journal of Insect Physiology 36, 561–565.Google Scholar
Prete, F. R., Hurd, L. E., Branstrator, D. and Johnson, A. (2002). Responses to computer-generated visual stimuli by the male praying mantis, Sphodromantis lineola (Burmeister). Animal Behaviour 63, 503–510.Google Scholar
R Development Core Team (2014). R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. URL: http://www.R-project.org Google Scholar
Ramaswamy, S. B. and Gupta, A. P. (1981). Effects of juvenile hormone on sense organs involved in mating behaviour of Blattella germanica (L.) (Dictyoptera: Blattellidae). Journal of Insect Physiology 27, 601–608.CrossRefGoogle Scholar
Rempel, J. G. (1940). Intersexuality in Chironomidae induced by nematode parasitism. Journal of Experimental Zoology 84, 261–289.Google Scholar
Robinson, M. H. and Robinson, B. (1979). By dawn's early light: Matutinal mating and sex attractants in a neotropical mantid. Science 205, 825–827.Google Scholar
Rowell, C. H. F. (2000). Presumptive mermithid-induced intersex individuals in the Neotropical grasshopper genus Drymophilacris Descamps 1976. Journal of Orthoptera Research 9, 31–35.Google Scholar
Roy, R. (2003). Répartition, biologie et variabilité de Tarachodella monticola Giglio-Tos, 1917 (Dictyoptera, Mantodea, Tarachodidae). Bulletin de la Societe Entomologique de France 108, 447–450.Google Scholar
Roy, R. (2005). Morphology and taxonomy. In The Praying Mantids (ed. Prete, F. R., Wells, H., Wells, P. H. and Hurd, L. E.), pp. 19–40. John Hopkins University Press, Baltimore.Google Scholar
Schafer, R. (2005). Postembryonic development in the antenna of the cockroach, Leucophaea maderae: growth, regeneration, and the development of the adult pattern of sense organs. Journal of Experimental Zoology 183, 353–363.Google Scholar
Schmidt-Rhaesa, A. and Ehrmann, R. (2001). Horsehair worms (Nematomorpha) as parasites of praying mantids with a discussion of their life cycle. Zoologischer Anzeiger 240, 167–179.Google Scholar
Slifer, E. H. (1968). Sense organs on the antenna1 flagellum of a praying mantis, Tenodera angustipennis, and of two related species (Mantodea). Journal of Morphology 124, 105–116.Google Scholar
Thomas, F., Schmidt-Rhaesa, A., Martin, G., Manu, C., Durand, P. and Renaud, F. (2002). Do hairworms (Nematomorpha) manipulate the water seeking behaviour of their terrestrial hosts? Journal of Evolutionary Biology 15, 356–361.Google Scholar
Vance, S. A. (1996). Morphological and behavioural sex reversal in mermithid-infected mayflies. Proceedings: Biological Sciences 263, 907–912.Google Scholar
Winnick, C. G., Holwell, G. I. and Herberstein, M. E. (2009). Internal reproductive anatomy of the praying mantid Ciulfina klassi (Mantodea: Liturgusidae). Arthropod Structure and Development 38, 60–69.Google Scholar
Wülker, W. (1964). Parasite-induced changes of internal and external sex characters in insects. Experimental Parasitology 15, 561–597.Google Scholar