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Non-sibling parasites (Strepsiptera) develop together in the same paper wasp

Published online by Cambridge University Press:  23 May 2008

L. VANNINI*
Affiliation:
Department of Evolutionary Biology, University of Siena, via A. Moro 2, 53100 Siena, Italy
A. CARAPELLI
Affiliation:
Department of Evolutionary Biology, University of Siena, via A. Moro 2, 53100 Siena, Italy
F. FRATI
Affiliation:
Department of Evolutionary Biology, University of Siena, via A. Moro 2, 53100 Siena, Italy
L. BEANI
Affiliation:
Department of Evolutionary Biology ‘Leo Pardi’, University of Florence, via Romana 17, 50125 Firenze, Italy
*
*Corresponding author: Department of Evolutionary Biology, University of Siena, via A. Moro 2, 53100 Siena, Italy. Tel: +39 0577 234410. Fax: +39 0577 234476. E-mail: [email protected]

Summary

Host discrimination by immature host-seeking endoparasites is a complex and somewhat unexplored topic. In the case of multiple infections, conflicts among conspecifics may occur to monopolize space and resources in the same host. Two or more 1st instar larvae of Xenos vesparum (Strepsiptera, Stylopidae) may enter into a Polistes dominulus (Hymenoptera, Vespidae) larva and develop together until the adult stage of both parasite and host. We carried out a screening of mitochondrial haplotypes in X. vesparum individuals extracted from superparasitized wasps taken in 5 naturally infected nests from different areas of Tuscany (Italy), to assess whether non-sibling parasites may infect the same colony and host. In total, we obtained 12 different haplotypes out of 122 genotyped individuals of both sexes: 17 of 34 superparasitized wasps hosted parasites that originated from females differing in their haplotypes. To date, this is the first described case of superparasitism with non-sibling host-seeking larvae infecting a single individual hymenopteran host. In addition, at least in heavily infected colonies, there is evidence of a male-biased sex-ratio and synchronous development of the parasites, regardless of their haplotypes. Finally, the distribution of haplotypes per nest is consistent with either phoretic infection or larvipositing on nests by means of superparasitized wasps.

Type
Original Articles
Copyright
Copyright © 2008 Cambridge University Press

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References

REFERENCES

Beani, L. (2006). Crazy wasps: when a parasite manipulates Polistes phenotype. Annales Zoologici Fennici Special Issue 43, 564574.Google Scholar
Beani, L. and Massolo, A. (2007). Polistes dominulus wasps (Hymenoptera Vespidae), if parasitized by Xenos Vesparum (Strepsiptera Stylopidae), wander among nests during the pre-emergence phase. Redia XC, 161164.Google Scholar
Beani, L., Giusti, F., Mercati, D., Lupetti, P., Paccagnini, E., Turilazzi, S. and Dallai, R. (2005 a). Mating of Xenos vesparum (Rossi) (Strepsiptera, Insecta) revisited. Journal of Morphology 265, 291303.CrossRefGoogle ScholarPubMed
Beani, L., Theodora, R., Dallai, R. and Turillazzi, S. (2005 b). Epicuticular hydrocarbons of Xenos vesparum (Strepsiptera, Stylopidae), parasite of Polistes dominulus (Hymenoptera, Vespidae): preliminary data. Redia 87, 167169.Google Scholar
Brodeur, J. and Boivin, G. (2004). Functional ecology of immature parasitoids. Annual Review of Entomology 49, 2749.CrossRefGoogle ScholarPubMed
Carapelli, A., Vannini, L., Nardi, F., Boore, J. L., Beani, L., Dallai, R. and Frati, F. (2006). The mitochondrial genome of the entomophagous endoparasite Xenos vesparum (Insecta: Strepsiptera). Gene 376, 248259.CrossRefGoogle ScholarPubMed
Cervo, R. and Dani, F. R. (1996). Social parasitism and its evolution in Polistes. In Natural History and Evolution of Paper-Wasps (ed. Turillazzi, S. and West-Eberhard, M. J.), pp. 98112. Oxford University Press, Oxford.CrossRefGoogle Scholar
Clement, M., Posada, D. and Crandall, K. A. (2000). TCS: a computer program to estimate gene genealogies. Molecular Ecology 9, 16571660.CrossRefGoogle ScholarPubMed
Dapporto, L., Cini, A., Palagi, E., Morelli, M., Simonti, A. and Turillazzi, S. (2007). Behaviour and chemical signature of pre-hibernating females of Polistes dominulus infected by the strepsipteran Xenos vesparum. Parasitology 134, 545552.CrossRefGoogle ScholarPubMed
Dunkle, S. W. (1979). Sexual competition for space of the parasite Xenos pallidus Brues in male Polistes annularis (L.) (Strepsiptera, Stylopidae, and Hymenoptera, Vespidae). Psyche 86, 327336.CrossRefGoogle Scholar
Excoffier, L., Laval, G. and Schneider, S. (2005). Arlequin ver. 3.0: An integrated software package for population genetics data analysis. Evolutionary Bioinformatics Ondine 1, 4750.Google Scholar
Giusti, F., Dallai, L., Beani, L., Manfredini, F. and Dallai, R. (2007). The midgut ultrastructure of the endoparasite Xenos vesparum (Rossi) (Insecta, Strepsiptera) during post-embryonic development and stable carbon isotopic analyses of the nutrient uptake. Arthropod Structure and Development 36, 183197.CrossRefGoogle ScholarPubMed
Godfray, H. C. J. (1994). Parasitoids: Behavioral and Evolutionary Ecology. Princeton University Press, Princeton, New Jersey.CrossRefGoogle Scholar
Good, P. (2000). Permutation Tests: a Practical Guide to Resampling Methods for Testing Hypotheses, 2nd Edn.Springer Verlag, New York.CrossRefGoogle Scholar
Grimaldi, D. J., Kathirithamby, J. and Schawaroch, V. (2005). Strepsiptera and triungula in Cretaceous amber. Insect Systematics and Evolution 36, 120.Google Scholar
Hughes, D. P. (2003). The behavioural ecology of strepsipteran parasites of Polistes wasps. Ph.D. thesis, Oxford University.Google Scholar
Hughes, D. P. (2005). Parasitic manipulation: a social context. Behavioral Processes 68, 263266.CrossRefGoogle ScholarPubMed
Hughes, D. P. and Kathirithamby, J. (2005). Cost of strepsipteran macroparasitism for immature wasps: does sociality modulate virulence? Oikos 110, 428434.CrossRefGoogle Scholar
Hughes, D. P., Beani, L., Turilazzi, S. and Kathirithamby, J. (2003). Prevalence of the parasite Strepsiptera in Polistes as detected by dissection of immatures. Insectes Sociaux 50, 6269.CrossRefGoogle Scholar
Hughes, D. P., Kathirithamby, J. and Beani, L. (2004 a). Prevalence of the parasite Strepsiptera in adult Polistes wasps: field collections and literature overview. Ethology Ecology and Evolution 16, 363375.CrossRefGoogle Scholar
Hughes, D. P., Kathirithamby, J., Turilazzi, S. and Beani, L. (2004 b). Social wasps desert the colony and aggregate outside if parasitized: parasite manipulation? Behavioral Ecology 15, 10371043.CrossRefGoogle Scholar
Kathirithamby, J. (1989). Review of the order Strepsiptera. Systematic Entomology 14, 4192.CrossRefGoogle Scholar
Koskella, B., Giraud, T. and Hood, M. E. (2006). Pathogen relatedness affects the prevalence of within-host competition. The American Naturalist 168, 121126.CrossRefGoogle ScholarPubMed
Linsley, E. G. and McSwain, J. W. (1957). Observations on the habits of Stylops pacifica Bohart. University of California Publications in Entomology 11, 395430.Google Scholar
Maeta, Y., Goukon, K., Kitamura, K. and Miyanga, R. (2001). Factors that determine the position where Pseudoxenos iwatai Esaki (Strepsiptera: Stylopidae) extrudes from the host cuticle. Tijdschrift voor Entomologie 144, 203215.CrossRefGoogle Scholar
Manfredini, F., Giusti, F., Beani, L. and Dallai, R. (2007). Developmental strategy of the endoparasite Xenos vesparum (Strepsiptera, Insecta): host invasion and elusion of its defense reactions. Journal of Morphology 268, 588601.CrossRefGoogle ScholarPubMed
Marris, G. C. and Casperd, J. (1996). The relationship between conspecific superparasitism and the outcome of in vitro contests staged between different larval instars of the solitary endoparasitoid Venturia canescens. Behavioral Ecology and Sociobiology 39, 6169.CrossRefGoogle Scholar
Mehta, C. and Patel, N. (1996). LogXact for Windows: User Manual. Cytel Software Corp., Cambridge, MA. USA.Google Scholar
Outreman, Y. and Pierre, J. S. (2005). Adaptive value of host discrimination in parasitoids: when host defences are very costly. Behavioural Processes 70, 93103.CrossRefGoogle ScholarPubMed
Pardi, L. (1946). Ricerche sui Polistini. VI. La ‘dominazione’ e il ciclo ovarico annuale in Polistes gallicus (L.). Bollettino dell'Istituto di Entomologia dell' Università di Bologna 15, 2584.Google Scholar
Royer, L., Fournet, S., Brunel, E. and Boivin, G. (1999). Intra- and interspecific host discrimination by host-seeking larvae of coleopteran parasitoids. Oecologia 118, 5968.CrossRefGoogle ScholarPubMed
Salt, G. (1961). Competition among insect parasitoids. Symposia of the Society for Experimental Biology 15, 96119.Google Scholar
Schmid-Hempel, P. (1998). Parasites in Social Insects. Princeton University Press, Princeton, New Jersey.Google Scholar
Schmid-Hempel, R. and Schmid-Hempel, P. (1989). Superparasitism and larval competition in conopid flies (Diptera, Conopidae), parasitizing bumblebees (Hymenoptera, Apidae). Mitteilungen der schweizerische entomologische Gesellschaft 62, 279289.Google Scholar
Schofield, P., Chaplain, M. and Hubbard, S. (2005). Evolution of searching and life history characteristics in individual-based models of host-parasitoid-microbe associations. Journal of Theoretical Biology 237, 116.CrossRefGoogle ScholarPubMed
Starks, P. T. (1998). A novel ‘sit and wait’ reproductive strategy in social wasps. Proceedings of the Royal Society of London, B 265, 14071410.CrossRefGoogle Scholar
Thompson, J. D., Gibson, T. J., Plewniak, F., Jeanmougin, F. and Higgins, D. G. (1997). The CLUSTAL_X windows interface flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research 25, 48764882.CrossRefGoogle ScholarPubMed
van Alphen, J. J. M. and Visser, M. E. (1990). Superparasitism as an adaptative strategy for insect parasitoids. Annual Review of Entomology 35, 5979.CrossRefGoogle ScholarPubMed
van Lenteren, J. C., Bakker, K. and van Alphen, J. J. M. (1978). How to analyse host discrimination. Ecological Entomology 3, 7175.CrossRefGoogle Scholar