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First-male sperm precedence and precopulatory and postcopulatory rituals in the parasitoid wasp Ooencyrtus kuvanae (Hymenoptera: Encyrtidae)

Published online by Cambridge University Press:  28 March 2014

K.M. Ablard
Affiliation:
Department of Biological Sciences, Simon Fraser University, 8888 University Drive., Burnaby, British Columbia, Canada V5A 1S6
K. Simonetto
Affiliation:
Department of Biological Sciences, Simon Fraser University, 8888 University Drive., Burnaby, British Columbia, Canada V5A 1S6
L.K. Weir
Affiliation:
Department of Biological Sciences, Simon Fraser University, 8888 University Drive., Burnaby, British Columbia, Canada V5A 1S6
B.J. Crespi
Affiliation:
Department of Biological Sciences, Simon Fraser University, 8888 University Drive., Burnaby, British Columbia, Canada V5A 1S6
P.W. Schaefer
Affiliation:
4 Dare Drive, Elkton, Maryland 21921, United States of America
G. Gries*
Affiliation:
Department of Biological Sciences, Simon Fraser University, 8888 University Drive., Burnaby, British Columbia, Canada V5A 1S6
*
1Corresponding author (email: gries@sfu.ca)

Abstract

Sperm competition generates selection for male traits to prevent it. These traits remain unclear in species where males compete for a virgin who is briefly receptive. Males of the parasitoid wasp Ooencyrtus kuvanae Howard (Hymenoptera: Encyrtidae) compete over females following emergence from host egg masses. Males engage virgins in a precopulatory ritual, mate, and then immediately perform a postcopulatory ritual after which the female becomes unreceptive. Often, sneaker (M2) males copulate with a female while she is engaged in the postcopulatory ritual, and they also perform the postcopulatory ritual. We investigated (i) paternity of M1 and M2 males using DNA microsatellite analysis, (ii) copulation and postcopulatory behaviour of both males, and (iii) morphological adaptations of the aedeagus for sperm removal. Eighty-eight percent of M1 males sired all daughters when they were first to perform the precopulatory and postcopulatory ritual, suggesting a linked effect of both rituals on paternity. The number and length of copulations by both males did not affect paternity, and the shape of the aedeagus does not seem to facilitate sperm removal. Our results are consistent with the hypothesis that postcopulatory rituals represent forms of mate guarding that function to increase paternity in the context of sperm competition.

Type
Behaviour & Ecology
Copyright
© Entomological Society of Canada 2014 

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Footnotes

Subject editor:Heather Proctor

References

Ablard, K., Fairhurst, S., Andersen, G., Schaefer, P.W., and Gries, G. 2011. Mechanisms, functions and fitness consequences of pre- and post-copulatory rituals of the parasitoid wasp Ooencyrtus kuvanae . Entomologia Experimentalis et Applicata, 140: 103111.Google Scholar
Ablard, K., Gries, R., Khaskin, G., Schaefer, P.W., and Gries, G. 2012. Does the stereochemistry of methylated cuticular hydrocarbons contribute to mate recognition in the egg parasitoid wasp Ooencyrtus kuvanae? Journal of Chemical Ecology, 38: 13061317.Google Scholar
Ablard, K.M., Schaefer, P.W., and Gries, G. 2013. A parasitoid wasp gathers and guards a harem by pheromone-tagging virgins. Behavioural Processes, 94: 3240.Google Scholar
Alcock, J. 1994. Postinsemination associations between males and females in insects: the mate-guarding hypothesis. Annual Review of Entomology, 39: 121.CrossRefGoogle Scholar
Allen, G.R., Kazmer, D.J., and Luck, R.F. 1994. Postcopulatory male behavior, sperm precedence and multiple mating in a solitary parasitoid wasp. Animal Behaviour, 48: 635644.CrossRefGoogle Scholar
Benelli, G., Bonsignori, G., Stefanini, C., Dario, P., and Canale, A. 2013. Male wing fanning performance during successful and unsuccessful mating in the parasitic wasp Lariophagus distinguendus Förster (Hymenoptera: Pteromalidae). Journal of Insect Behavior, 26: 228237.Google Scholar
Boorman, E. and Parker, G.A. 1976. Sperm (ejaculate) competition in Drosophila melanogaster, and reproductive value of females to males in relation to female age and mating status. Animal Behaviour, 48: 635644.Google Scholar
Brown, M.W. 1984. Literature review of Ooencyrtus kuvanae [Hym: Encyrtidae] an egg parasite of Lymantria dispar [Lep: Lymantriidae]. Entomophaga, 29: 249265.Google Scholar
Brown, W.D., Crespi, B.J., and Choe, J.C. 1997. Sexual conflict and the evolution of mating systems. In The evolution of mating systems in insects and arachnids. Edited by J.C. Choe and B.J. Crespi. Cambridge University Press, Cambridge, United Kingdom. Pp. 352377.Google Scholar
Damiens, D. and Boivin, G. 2006. Why do sperm-depleted males continue to mate? Behavioral Ecology, 17: 138143.Google Scholar
Eberhard, W.G. 1996. Female control: sexual selection by cryptic female choice. Princeton University Press, Princeton, New Jersey, United States of America.Google Scholar
Eberhard, W.G. 2009. Postcopulatory sexual selection: Darwin’s omission and its consequences. Proceedings of the National Academy of Sciences of the United States of America, 106: 1002510032.Google Scholar
Field, S.A. and Keller, M.A. 1993. Alternative mating tactics and female mimicry as post-copulatory mate-guarding behaviour in the parasitic wasp Cotesia rubecula . Animal Behaviour, 46: 11831189.Google Scholar
Gordh, G. and DeBach, P. 1978. Courtship behavior in the Aphytis lingnanensis group, its potential usefulness in taxonomy and a review of sexual behavior in the parasitic Hymenoptera (Chalcidoidea: Aphelinidae). Hilgardia, 46: 3775.Google Scholar
Gromko, M.H., Gilbert, D.G., and Richmond, R.C. 1984. Sperm transfer and use in the multiple mating system of Drosophila . In Sperm competition and the evolution of animal mating systems. Edited by R.L. Smith. Academic Press, Florida, United States of America. Pp. 372420.Google Scholar
Gwynne, D.T. 1984. Male mating effort, confidence of paternity, and insect sperm competition. In Sperm competition and the evolution of animal mating systems. Edited by R.L. Smith. Academic Press, Florida, United States of America. Pp. 117144.Google Scholar
Hofstetter, R.W. and Raffa, K.F. 1997. New host record for Ooencyrtus kuvanae (Hymenoptera: Encyrtidae). Entomological News, 108: 6365.Google Scholar
Holmes, H.B. 1974. Patterns of sperm competition in Nasonia vitripennis . Canadian Journal of Genetics and Cytology, 16: 789795.CrossRefGoogle ScholarPubMed
Jones, K.C., Levine, K.F., and Banks, J.D. 2002. Characterization of 11 polymorphic tetranucleotide microsatellites for forensic applications in California elk. Cervus elaphus canadensis. Molecular Ecology Notes, 4: 425427.Google Scholar
Jones, O.R. and Wang, J. 2010. COLONY: a program for parentage and sibship inference from multilocus genotype data. Molecular Ecology Resources, 10: 551555.Google Scholar
King, B.H. and Fischer, C.R. 2005. Males mate guard in absentia through extended effects of postcopulatory courtship in the parasitoid wasp Spalangia endius (Hymenoptera: Pteromalidae). Journal of Insect Physiology, 5: 13401345.Google Scholar
Knowlton, N. and Greenwell, S.R. 1984. Male sperm competition avoidance mechanisms: the influence of female interests. In Sperm competition and the evolution of animal mating systems. Edited by R.L. Smith. Academic Press, Florida, United States of America. Pp. 6283.Google Scholar
Kock, D. and Sauer, K.P. 2007. High variation in sperm precedence and last male advantage in the scorpionfly Panorpa germanica L. (Mecoptera, Panorpidae): possible causes and consequences. Journal of Insect Physiology, 53: 11451150.Google Scholar
Kuhbandner, S., Sperling, S., Mori, K., and Ruther, J. 2012. Deciphering the signature of cuticular lipids with contact sex pheromone function in a parasitic wasp. The Journal of Experimental Biology, 215: 24712478.Google Scholar
Mackauer, M. 1969. Sexual behaviour of, and hybridization between three species of Aphidius Nees parasitic on the pea aphid. Proceedings of the Entomological Society of Washington, 71: 339351.Google Scholar
Martel, V., Damiens, D., and Boivin, G. 2008. Strategic ejaculation in the egg parasitoid Trichogramma turkestanica (Hymenoptera: Trichogrammatidae). Ecological Entomology, 33: 357361.CrossRefGoogle Scholar
Martinez-Martinez, L., Leyva-Vazquez, J.L., and Mojica, H.B. 1993. Sperm competition in the female Diachasmimorpha longicaudata (Hymenoptera: Braconidae). Southwestern Entomologist, 18: 293299.Google Scholar
Otronen, M. 1994. Repeated copulations as a strategy to maximize fertilization in the fly Dryomyza anilis (Dryomyzidae). Behavioural Ecology, 5: 5156.Google Scholar
Parker, G.A. 1970. Sperm competition and its evolutionary consequences in insects. Biological Reviews of the Cambridge Philosophical Society, 45: 525567.CrossRefGoogle Scholar
Parker, G.A. 1974. Courtship persistence and female guarding as male time investment strategies. Behaviour, 48: 157184.Google Scholar
Ridley, M. 1993. Clutch size and mating frequency in parasitic Hymenoptera. American Naturalist, 142: 893910.Google Scholar
Shuster, S.M. and Wade, M.J. 2003. Mating systems and strategies. Princeton University Press, Princeton, New Jersey, United States of America.Google Scholar
Simmons, L.W. 1990. Nuptial feeding in tettigoniids: male costs and the rates of fecundity increase. Behavioral Ecology and Sociobiology, 27: 4347.CrossRefGoogle Scholar
Simmons, L.W. 2001. Sperm competition and its evolutionary consequences in the insects. Princeton University Press, Princeton, New Jersey, United States of America.Google Scholar
Somjee, U., Ablard, K., Crespi, B.J., Schaefer, P.W., and Gries, G. 2011. Local mate competition in the solitary parasitoid wasp Ooencyrtus kuvanae . Behavioral Ecology and Sociobiology, 65: 10711077.Google Scholar
Thornhill, R. 1984. Alternative hypotheses for traits believed to have evolved by sperm competition. In Sperm competition and the evolution of animal mating systems. Edited by R.L. Smith. Academic Press, Florida, United States of America. Pp. 151176.Google Scholar
Thornhill, R. and Alcock, J. 1983. The evolution of insect mating systems. Cambridge University Press, Cambridge, United Kingdom.Google Scholar
van den Assem, J. 1986. Mating behaviour in parasitic wasps. In Insect parasitoids. Edited by J. Waage and D. Greathead. Academic Press, London, United Kingdom. Pp. 137167.Google Scholar
van den Assem, J. 1996. Mating behaviour. In Insect natural enemies: practical approaches to their study and evaluation. Edited by M.A. Jervis and N.A.C. Kidd. Springer, Dordrecht, The Netherlands. Pp. 163221.Google Scholar
van den Assem, J., Gijswijt, M.J., and Nubel, B.K. 1980. Observations on courtship and mating strategies in a few species of parasitic wasps (Chalcidoidea). Netherlands Journal of Zoology, 30: 208227.Google Scholar
van den Assem, J., van Lersel, J.J.A., and Los-den Hartogh, R.L. 1989. Is being large more important for female than for male parasitic wasps? Behavior, 108: 160195.Google Scholar
Viggiani, B. and Battaglia, D. 1983. Courtship and mating behaviour in a few Aphelinidae (Hym. Chalcidoidea). Bollettino del Laboratorio di Entomologia Agraria ‘Filippo Silvestri’, 40: 9091.Google Scholar
Waage, J.K. 1984. Alternative hypotheses for traits believed to have evolved by sperm competition. In Sperm competition and the evolution of animal mating systems. Edited by R.L. Smith. Academic Press, Florida, United States of America. Pp. 251290.Google Scholar