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

  • MING-CHUNG CHIU (a1), CHIN-GI HUANG (a1), WEN-JER WU (a1) and SHIUH-FENG SHIAO (a1)
Summary
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.

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Corresponding author
* Corresponding author: Department of Entomology, National Taiwan University, Taipei 106, Taiwan. E-mail: sfshiao@ntu.edu.tw
References
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Abràmoff M. D., Magalhães P. J. and Ram S. J. (2004). Image processing with ImageJ. Biophotonics International 11, 3642. URL: http://imagej.nih.gov/ij/
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, 245259.
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, 133140.
Baudoin M. (1975). Host castration as a parasitic strategy. Evolution 29, 335352.
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, 133135.
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, 656660.
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, 122.
de Loof A. and Huybrechts R. (1998). ‘Insects do not have sex hormones’: a myth? General and Comparative Endocrinology 111, 245260.
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, 275286.
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, 223229.
Fisher F. M. and Sanborn R. C. (1962). Production of insect juvenile hormone by the microsporidian parasite Nosema . Nature 194, 1193.
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, 295309.
Hanelt B., Grother L. E. and Janovy J. Jr. (2001). Physid snails as sentinels of freshwater nematomorphs. Journal of Parasitology 87, 10491053.
Hanelt B., Thomas F. and Schmidt-Rhaesa A. (2005). Biology of the phylum Nematomorpha. Advances in Parasitology 59, 243305.
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.
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, 307313.
Hurd H. (2001). Host fecundity reduction: a strategy for damage limitation? Trends in Parasitology 17, 363368.
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. 85110.
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, 155166.
Klowden M. J. (2007). Endocrine systems. In Physiological Systems in Insects (ed. Klowden M. J.), pp. 174. Elsevier/Academic Press, Amsterdam.
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, 147152.
Lafferty K. D. and Kuris A. M. (2009). Parasitic castration: the evolution and ecology of body snatchers. Trends in Parasitology 25, 564572.
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, 3134.
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, 554559.
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, 217222.
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. 353374. InTech Press, Slavka Krautzeka.
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, 151156.
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, 561565.
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, 503510.
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
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, 601608.
Rempel J. G. (1940). Intersexuality in Chironomidae induced by nematode parasitism. Journal of Experimental Zoology 84, 261289.
Robinson M. H. and Robinson B. (1979). By dawn's early light: Matutinal mating and sex attractants in a neotropical mantid. Science 205, 825827.
Rowell C. H. F. (2000). Presumptive mermithid-induced intersex individuals in the Neotropical grasshopper genus Drymophilacris Descamps 1976. Journal of Orthoptera Research 9, 3135.
Roy R. (2003). Répartition, biologie et variabilité de Tarachodella monticola Giglio-Tos, 1917 (Dictyoptera, Mantodea, Tarachodidae). Bulletin de la Societe Entomologique de France 108, 447450.
Roy R. (2005). Morphology and taxonomy. In The Praying Mantids (ed. Prete F. R., Wells H., Wells P. H. and Hurd L. E.), pp. 1940. John Hopkins University Press, Baltimore.
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, 353363.
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, 167179.
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, 105116.
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, 356361.
Vance S. A. (1996). Morphological and behavioural sex reversal in mermithid-infected mayflies. Proceedings: Biological Sciences 263, 907912.
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, 6069.
Wülker W. (1964). Parasite-induced changes of internal and external sex characters in insects. Experimental Parasitology 15, 561597.
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Parasitology
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