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Parasitic castration by Xenos vesparum depends on host gender

Published online by Cambridge University Press:  28 April 2014

FEDERICO CAPPA ,
FABIO MANFREDINI ,
ROMANO DALLAI ,
MARCO GOTTARDO  and
LAURA BEANI
FEDERICO CAPPA*
Affiliation:
Dipartimento di Biologia, Università degli Studi di Firenze, Via Madonna del piano 6, 50019, Sesto Fiorentino (Firenze), Italy
FABIO MANFREDINI
Affiliation:
School of Biological Sciences, Royal Holloway University of London, Egham TW20 0EX, UK
ROMANO DALLAI
Affiliation:
Dipartimento di Biologia Evolutiva, Università degli Studi di Siena, Via Aldo Moro, 53100, Siena, Italy
MARCO GOTTARDO
Affiliation:
Dipartimento di Biologia Evolutiva, Università degli Studi di Siena, Via Aldo Moro, 53100, Siena, Italy
LAURA BEANI
Affiliation:
Dipartimento di Biologia, Università degli Studi di Firenze, Via Madonna del piano 6, 50019, Sesto Fiorentino (Firenze), Italy
*
* Corresponding author: Dipartimento di Biologia, Università degli Studi di Firenze, Via Madonna del piano 6, 50019, Sesto Fiorentino (Firenze), Italy. E-mail: [email protected]
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Summary

Host castration represents a mechanism used by parasites to exploit energy resources from their hosts by interfering with their reproductive development or to extend host lifespan by removing risks associated with reproductive activity. One of the most intriguing groups of parasitic castrators is represented by the insects belonging to the order Strepsiptera. The macroparasite Xenos vesparum can produce dramatic phenotypic alterations in its host, the paper wasp Polistes dominula. Parasitized female wasps have undeveloped ovaries and desert the colony without performing any social task. However, very little attention has been given to the parasitic impact of X. vesparum on the male phenotype. Here, we investigated the effects of this parasite on the sexual behaviour and the morpho-physiology of P. dominula males. We found that, differently from female wasps, parasitized males are not heavily affected by Xenos: they maintain their sexual behaviour and ability to discriminate between female castes. Furthermore, the structure of their reproductive apparatus is not compromised by the parasite. We think that our results, demonstrating that the definition of X. vesparum as a parasitoid does not apply to infected males of P. dominula, provide a new perspective to discuss and maybe reconsider the traditional view of strepsipteran parasites.

Keywords

parasitic castrationhost gendermale sexual preferencepaper waspPolistesStrepsiptera
Type
Research Article
Information
Parasitology , Volume 141 , Issue 8 , July 2014 , pp. 1080 - 1087
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Copyright
Copyright © Cambridge University Press 2014 

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References

REFERENCES

Baudin, M. (1975). Host castration as a parasitic strategy. Evolution 29, 335–352.Google Scholar
Beani, L. (1996). Lek-like courtship in paper wasps: “a prolonged, delicate, and troublesome affair”. In The Natural History and Evolution of Paper-Wasps (ed. Turillazzi, S. and West-Eberhard, M. J.), pp. 113–125. Oxford University Press, Oxford, UK.Google Scholar
Beani, L. (2006). Crazy wasps: when parasites manipulate the Polistes phenotype. Annales Zoologici Fennici 43, 564–574.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-emerging phase. Redia 90, 161–164.Google Scholar
Beani, L. and Turillazzi, S. (1988). Alternative mating tactics in males of Polistes dominulus (Hymenoptera: Vespidae). Behavioral Ecology and Sociobiology 22, 257–264.Google Scholar
Beani, L., Giusti, F., Mercati, D., Lupetti, P., Paccagnini, E., Turillazzi, S. and Dallai, R. (2005). Mating of Xenos vesparum (Rossi) (Strepsiptera, Insecta) revisited. Journal of Morphology 265, 291–303.Google Scholar
Beani, L., Dallai, R., Mercati, D., Cappa, F., Giusti, F. and Manfredini, F. (2011). When a parasite breaks all the rules of a colony: morphology and fate of wasps infected by a strepsipteran endoparasite. Animal Behaviour 82, 1305–1312.CrossRefGoogle Scholar
Beckage, N. E. (1997). New insights: how parasites and pathogens alter the endocrine physiology and development of insect hosts. In Parasites and Pathogens: Effects on Host Hormones and Behavior (ed. Beckage, N. E.), pp. 3–36. Chapman & Hall, New York, NY, USA.CrossRefGoogle Scholar
Brown, J. J. and Reed, D. A. (1997). Host embryonic and larval castration as a strategy for the individual castrator and the species. In Parasites and Pathogens: Effects on Host Hormones and Behavior (ed. Beckage, N. E.), pp. 156–178. Chapman & Hall, New York, NY, USA.Google Scholar
Cappa, F., Bruschini, C., Cervo, R., Turillazzi, S. and Beani, L. (2013). Males do not like the working class: male sexual preference and recognition of functional castes in a primitively eusocial wasp. Animal Behaviour 86, 801–810.Google Scholar
Cervo, R., Dapporto, L., Beani, L., Strassmann, J. E. and Turillazzi, S. (2008). On status badges and quality signals in the paper wasp Polistes dominulus: body size, facial colour patterns and hierarchical rank. Proceedings of the Royal Society London B 269, 1423–1428.Google Scholar
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, 545–552.Google Scholar
Dawkins, R. (1982). The Extended Phenotype. Oxford University Press, Oxford, UK.Google Scholar
Dawkins, R. (2012). Preface. In Host Manipulation by Parasites (ed. Hughes, D. P., Brodeur, J. and Thomas, F.), pp. xi–xiii. Oxford University Press, Oxford, UK.Google Scholar
Duneau, D. and Ebert, D. (2012). Host sexual dimorphism and parasite adaptation. PloS Biology 10, e1001271.Google Scholar
Duneau, D., Luijckx, P., Ruder, L. F. and Ebert, D. (2012). Sex-specific effects of a parasite evolving in a female-biased host population. BMC Biology 10, 104.Google Scholar
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, 327–336.Google Scholar
Eickwort, K. (1969). Separation of the caste of Polistes exclamans and notes on its biology (Hymenoptera: Vespidae). Insectes Sociaux 16, 67–72.Google Scholar
Hartikainen, H. and Okamura, B. (2012). Castrating parasites and colonial hosts. Parasitology 139, 547–556.Google Scholar
Hechinger, R. F., Lafferty, K. D., Mancini, F. T., Warner, R. R., Kuris, A. M. (2009). How large is the hand in the puppet? Ecological and evolutionary factors affecting body mass of 15 trematode parasitic castrators in their snail host. Evolutionary Ecology 23, 651–667.Google Scholar
Huelsenbeck, J. P. (1998). Systematic bias in phylogenetic analysis: is the Strepsiptera problem solved? Systematic Biology 47, 519–537.Google Scholar
Hughes, D. P., Beani, L., Turillazzi, S. and Kathirithamby, J. (2003). Prevalence of the parasite Strepsiptera in Polistes as detected by dissection of immatures. Insectes Sociaux 50, 62–68.Google Scholar
Hughes, D. P., Kathirithamby, J., Turillazzi, S. and Beani, L. (2004 a). Social wasps desert the colony and aggregate outside if parasitized: parasite manipulation? Behavioral Ecology 15, 1037–1043.CrossRefGoogle Scholar
Hughes, D. P., Kathirithamby, J. and Beani, L. (2004 b). Prevalence of the parasite Strepsiptera in adult Polistes wasps: field collections and literature overview. Ethology, Ecology and Evolution 16, 363–375.Google Scholar
Hughes, D. P., Kronauer, D. J. C. and Boomsma, J. J. (2008). Extended phenotype: nematodes turn ants into bird-dispersed fruits. Current Biology 18, R294–R295.Google Scholar
Hughes, D. P., Andersen, S. B., Hywel-Jones, N. L., Himaman, W., Billen, J. and Boomsma, J. J. (2011). Behavioral mechanisms and morphological symptoms of zombie ants dying from fungal infection. BMC Ecology 11, 13.Google Scholar
Hurd, H. (1990). Physiological and behavioural interactions between parasites and invertebrate-hosts. Advances in Parasitology 29, 271–317.Google Scholar
Kathirithamby, J. (1989). Review of the order Strepsiptera. Systematic Entomology 14, 41–92.Google Scholar
Kathirithamby, J. (2009). Host-parasitoid associations in Strepsiptera. Annual Review of Entomology 54, 227–249.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
Lefèvre, T., Lebarbenchon, C., Gauthier-Clerc, M., Missé, D., Poulin, R. and Thomas, F. (2009 a). The ecological significance of manipulative parasites. Trends in Ecology and Evolution 24, 41–48.Google Scholar
Lefèvre, T., Adamo, S. A., Biron, D. G., Missé, D., Hughes, D. and Thomas, F. (2009 b). Invasion of the body snatchers: the diversity and evolution of manipulative strategies in host-parasite interactions. Advances in Parasitology 68, 45–83.Google Scholar
Liebert, A., Wilson-Rich, N., Johnson, C. E. and Starks, P. T. (2010). Sexual interactions and nestmate recognition in invasive populations of Polistes dominulus wasps. Insectes Sociaux 57, 457–463.Google 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, 588–601.Google Scholar
Manfredini, F., Massolo, A. and Beani, L. (2010 a). Hard to choose for tiny pests: host-seeking behaviour in Xenos vesparum triungulins. Ethology, Ecology and Evolution 22, 1–10.Google Scholar
Manfredini, F., Beani, L., Taormina, M. and Vannini, L. (2010 b). Parasitic infection protects wasp larvae against a bacterial challenge. Microbes and Infections 12, 727–735.Google Scholar
Manfredini, F., Benati, D. and Beani, L. (2010 c). The strepsipteran endoparasite Xenos vesparum alters the immunocompetence of its host, the paper wasp Polistes dominulus . Journal of Insect Physiology 56, 253–259.Google Scholar
Manfredini, F., Grozinger, C. M. and Beani, L. (2013). Examining the “evolution of increased competitive ability” hypothesis in response to parasites and pathogens in the invasive paper wasp Polistes dominula . Naturwissenschaften 100, 219–228.Google Scholar
McMahon, D. P., Hayward, A. and Kathirithamby, J. (2011). Strepsiptera. Current Biology 21, R271–R272.Google Scholar
Moore, J. (2002). Parasites and the Behavior of Animals. Oxford University Press, Oxford, UK.Google Scholar
Pohl, H. and Beutel, R. G. (2008). The evolution of Strepsiptera (Hexapoda). Zoology 111, 318–338.Google Scholar
Polak, M. (1993). Competition for landmark territories among male Polistes canadensis (L.) (Hymenoptera: Vespidae): large-size advantage and alternative mate-acquisition tactics. Behavioural Ecology 4, 325–331.Google Scholar
Poulin, R. and Thomas, F. (1999). Phenotypic variability induced by parasites: extent and evolutionary implications. Parasitology Today 15, 28–32.Google Scholar
Proffitt, F. (2005). Twisted parasites from outer space perplex biologists. Science 307, 343.Google Scholar
Retschnig, G., Williams, G. R., Mehmann, M. M., Yañez, O., de Miranda, J. R. and Neumann, P. (2014). Sex-specific differences in pathogen susceptibility in honey bees (Apis mellifera). PLOS One 9, e85261.Google Scholar
Schmid-Hempel, P. (2011). Parasites, immunity and sexual selection. In Evolutionary Parasitology: the Integrated Study of Infections, Immunology, Ecology, and Genetics (ed. Schmid-Hempel, P.), pp. 141–163. Oxford University Press, Oxford, UK.Google Scholar
Sen, R., Samudre, S., Shilpa, M. C., Chitra Tarak, R. and Gadagkar, R. (2010). Middle aged wasps mate through most of the year, without regard to body size, ovarian development and nestmateship: a laboratory study of the primitively eusocial wasp Ropalidia marginata . Insectes Sociaux 57, 95–103.Google Scholar
Strambi, C. and Strambi, A. (1973). Influence du développement du parasite Xenos vesparum Rossi (Insecte, Strepsiptère) sur le système neuro-endocrinien des femelles de Polistes (Hyménoptère, Vespide) au début de leur vie imaginale. Archives d Anatomie Microscopique et de Morphologie Experimentale 62, 39–54.Google Scholar
Strambi, C., Strambi, A. and Augier, A. (1982). Protein levels in the haemolymph of the wasp Polistes gallicus L. at the beginning of imaginal life and during overwintering. Action of the strepsipteran parasite Xenos vesparum Rossi. Experientia 38, 1189–1191.Google Scholar
Strassmann, J. E. (1981). Evolutionary implications of early male and satellite nest production in Polistes exclamans colony cycles. Behavioral Ecology and Sociobiology 8, 55–64.Google Scholar
Thomas, F., Adamo, S. and Moore, J. (2005). Parasitic manipulation: where are we and where should we go? Behavioural Processes 68, 185–199.Google Scholar
Tibbetts, E. A., Skaldina, O., Zhao, V., Toth, A. L., Skaldin, M., Beani, L. and Dale, J. (2011). Geographic variation in the status signals of Polistes dominulus paper wasps. PLoS One 6, e28173.Google Scholar
Toth, A. L., Bilof, K. B. J., Henshaw, M. T., Hunt, J. H. and Robinson, G. E. (2009). Lipid stores, ovary development, and brain gene expression in Polistes metricus females. Insectes Sociaux 56, 77–84.Google Scholar
Tsuji, K. (1996). Queen-male conflict over sperm use in social insects. Trends in Ecology and Evolution 11, 490–491.Google Scholar
Whiting, M. F., Carpenter, J. C., Wheeler, Q. D. and Wheeler, W. C. (1997). The Strepsiptera problem: phylogeny of the holometabolous insect orders inferred from 18S and 28S ribosomal DNA sequences and morphology. Systematic Biology 46, 1–68.Google Scholar
Zuk, M. (1990). Reproductive strategies and disease susceptibility: an evolutionary viewpoint. Parasitology Today 6, 231–233.Google Scholar
Zuk, M. (2009). The sicker sex. PLoS Pathogens 5, e1000267.Google Scholar