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Sexual activity diminishes male virility in two Coccinella species: consequences for female fertility and progeny development

Published online by Cambridge University Press:  17 April 2013

J.P. Michaud ,
Mahadev Bista ,
Geetanjali Mishra  and
Omkar Singh
J.P. Michaud*
Affiliation:
Department of Entomology, Kansas State University, Agricultural Research Station-Hays, Hays, KS, USA
Mahadev Bista
Affiliation:
Ladybird Research Laboratory, Department of Zoology, University of Lucknow, Lucknow, India
Geetanjali Mishra
Affiliation:
Ladybird Research Laboratory, Department of Zoology, University of Lucknow, Lucknow, India
Omkar Singh
Affiliation:
Ladybird Research Laboratory, Department of Zoology, University of Lucknow, Lucknow, India
*
*Author for correspondence Phone: 785-625-3425 Fax: 785-625-4369 E-mail: [email protected]
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Abstract

Male contributions, both chemical and behavioural, can influence female sperm usage and reproductive success. To determine whether such male factors are subject to depletion in Coccinella septempunctata and Coccinella transversalis, we tested the effects of male mating history on male virility, as estimated by measures of mating behaviour, female reproductive success and progeny fitness, with parental age held constant. Overt measures of male mating effort (wriggling duration, number of shaking bouts and total copula duration) all diminished from virgin to 5 × mated males and were mirrored by concurrent declines in female fecundity and fertility (measured over 20 days). Paternal effects were also observed which diminished as a function of mating history, suggesting that transgenerational signals of male origin are also subject to depletion. Progeny of virgin fathers had higher rates of survival (C. transversalis) and faster development (both species) than progeny of 5 × mated fathers. Seminal fluid proteins are known to have allohormonal properties and can stimulate female fecundity and fertility in a number of insects, making them strong candidates for depletion as a function of mating activity. However, it is also possible that sperm limitation and/or reduced tactile stimulation of females by multiple-mated males may have contributed to some of the observed effects.

Keywords

developmental timefecundityfertilitypaternal effectsseminal fluid proteins
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 103 , Issue 5 , October 2013 , pp. 570 - 577
Copyright
Copyright © Cambridge University Press 2013 

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References

Alexander, R.D., Marshall, D.C. & Cooley, J.R. (1997) Evolutionary perspectives on insect mating. pp. 4–31in Choe, J.C. & Crespi, B.J. (Eds) The Evolution of Mating Systems in Insects and Arachnids. Cambridge, UK, Cambridge University Press.Google Scholar
Alonzo, S. & Pizzari, T. (2010) Male fecundity stimulation: conflict and cooperation within and between the sexes: model analyses and coevolutionary dynamics. American Naturalist 175, 174–185.Google Scholar
Avila, F.W., Sirot, L.K., LaFlamme, B.A., Rubinstein, C.D. & Wolfner, M.F. (2011) Insect seminal fluid proteins: identification and function. Annual Review of Entomology 56, 21–40.Google Scholar
Bind, R.B. (2007) Reproductive behaviour of a generalist aphidophagous ladybird beetle Cheilomenes sexmaculata (Coleoptera: Coccinellidae). International Journal of Tropical Insect Science 27, 77–84.Google Scholar
Bista, M. & Omkar, (2012) Impact of multiple mating on behavioural patterns and reproductive attributes of seven spotted ladybird beetle, Coccinella septempunctata (L.). Journal of Applied Bioscience 38, 159–164.Google Scholar
Bonduriansky, R. (2001) The evolution of male mate choice in insects: a synthesis of ideas and evidence. Biological Reviews 76, 305–339.Google Scholar
Bonduriansky, R. & Head, M. (2007) Maternal and paternal condition effects on offspring phenotype in Telostylinus ngusticollis (Diptera: Neriidae). Journal of Evolutionary Biology 20, 2379–2388.Google Scholar
Camarano, S., Andres, G. & Carmen, R. (2009) Biparental endowment of endogenous defensive alkaloids in Epilachna paenulata. Journal of Chemical Ecology 35, 1–7.Google Scholar
Cameron, E., Day, T. & Rowe, L. (2007) Sperm competition and the evolution of ejaculate composition. American Naturalist 169, E158–E172.Google Scholar
Chen, P.S. (1984) The functional morphology and biochemistry of insect male accessory glands and their secretions. Annual Review of Entomology 29, 233–255.Google Scholar
Chen, P.S., Strumm-Zollinger, E., Aigaki, T., Balmer, J., Bienz, M. & Bohlen, P. (1988) A male accessory gland peptide that regulates reproductive behavior of female Drosophila melanogaster. Cell 54, 291–298.Google Scholar
de Jong, P.W., Brakefield, P.M., Geerinck, B.P. (1998) The effect of female mating history on sperm precedence in the two-spot ladybird, Adalia bipunctata (Coleoptera: Coccinellidae). Behavorial Ecology 9, 559–565.Google Scholar
Dobzhansky, T. (1935) Maternal effect as a cause of the difference between the reciprocal crosses in Drosophila pseudoobscura. Proceedings of the National Academy of Sciences of the United States of America 21, 443–446.Google Scholar
Eberhard, W.G. (1996) Female Control: Sexual Selection by Cryptic Female Choice. Princeton, NJ, Princeton University Press.Google Scholar
Eberhard, W.G. (1997) Sexual selection by cryptic female choice in insects and arachnids. pp. 32–57in Choe, J.C. & Crespi, B.J. (Eds) The Evolution of Mating Systems in Insects and Arachnids. Cambridge, UK, Cambridge University Press.Google Scholar
Fisher, D.O., Double, M.C., Blomberg, S.P., Jennions, M.D. & Cockburn, A. (2006) Post-mating sexual selection increases lifetime fitness of polyandrous females in the wild. Nature 444, 89–92.Google Scholar
Fisher, T.W. (1959) Occurrence of spermatophore in certain species of Chilocorus. Pan-Pacific Entomologist 35, 205–208.Google Scholar
Fox, C.W. & Mousseau, T.A. (1998) Maternal effects as adaptations for transgenerational phenotypic plasticity in insects. pp. 159–177in Mousseau, T. & Fox, C. (Eds), Maternal Effects as Adaptations. Oxford, UK, Oxford University Press.Google Scholar
Gillott, C. (2003) Male accessory gland secretions: modulators of female reproductive physiology and behavior. Annual Review of Entomology 48, 163–184.Google Scholar
Haddrill, P.R., Shuker, D.M., Mayes, S. & Majerus, M.E.N. (2007) Temporal effects of multiple mating on components of fitness in the two-spot ladybird, Adalia bipunctata (Coleoptera: Coccinellidae). European Journal of Entomology 104, 393–398.Google Scholar
Haddrill, P.R., Shuker, D.M., Amos, W., Majerus, M.E.N. & Mayes, S. (2008) Female multiple mating in wild and laboratory populations of the two-spot ladybird, Adalia bipunctata. Molecular Ecology 17, 3189–3197.Google Scholar
Hanin, O., Azrielli, A., Applebaum, S.W. & Rafaeli, A. (2012) Functional impact of silencing the Helicoverpa armigera sex-peptide receptor on female reproductive behaviour. Insect Molecular Biology 21, 161–167.CrossRefGoogle ScholarPubMed
Heifetz, Y. & Wolfner, M.F. (2004) Mating, seminal fluid components, and sperm cause changes in vesicle release in the Drosophila female reproductive tract. Proceedings of the National Academy of Sciences Series B 101, 6261–6266.Google Scholar
Heifetz, Y., Tram, U. & Wolfner, M.F. (2001) Male contributions to egg production: the role of accessory gland products and sperm in Drosophila melanogaster. Proceedings of the Royal Society of London. Series B. Biological Sciences 268, 175–180.Google Scholar
Herman, W.S. (1993) Endocrinology of the monarch butterfly. Natural History Museum of Los Angeles County Science Series 38, 143–146.Google Scholar
Hodek, I. (1996) Food relationships. pp. 143–238in Hodek, I & Honek, A. (Eds) Ecology of Coccinellidae. Dordrecht, Netherlands, Kluwer Academic Publishers.Google Scholar
Hodek, I. & Michaud, J.P. (2008) Why is Coccinella septempunctata so successful? European Journal of Entomology 105, 1–12.CrossRefGoogle Scholar
Katakura, H., Nakano, S., Hosogai, T. & Kahono, S. (1994) Female internal reproductive organs, modes of sperm transfer, and phylogeny of Asian Epilachninae (Coleoptera: Coccinellidae). Journal of Natural History 28, 577–583.Google Scholar
Kaufmann, T. (1996) Dynamics of sperm transfer, mixing, and fertilization in Cryptolaemus montrouzieri (Coleoptera: Coccinellidae) in Kenya. Annals of the Entomological Society of America 89, 238–242.Google Scholar
Kindlmann, P. & Dixon, A.F.G. (1993) Optimal foraging in ladybird beetles (Coleoptera: Coccinelidae) and its consequences in their use in biological control. European Journal of Entomology 90, 443–450.Google Scholar
LaFlamme, B.A., Ram, K.R. & Wolfner, M.F. (2012) The Drosophila melanogaster seminal fluid protease ‘seminase’ regulates proteolytic and post-mating reproductive processes. Public Library of Science Genetics 8, e10002435.Google Scholar
Lupold, S., Manier, M.K., Ala-Honkola, O., Belote, J.M. & Pitnick, S. (2010) Male Drosophila melanogaster adjust ejaculate size based on female mating status, fecundity, and age. Behavioral Ecology 22, 184–191.Google Scholar
Majerus, M.E.N. (1994) Female promiscuity maintains high fertility in ladybirds (Col., Coccinellidae). Entomologist's Monthly Magazine 130, 1564–1567.Google Scholar
Mousseau, T.A. & Fox, C.W. (Eds) (1998) Maternal Effects as Adaptations. Oxford, UK, Oxford University Press.Google Scholar
Mousseau, T.A., Uller, T., Wapstra, E. & Badyaev, A.V. (2009) Evolution of maternal effects: past and present. Philosophical Transactions of the Royal Society of London Series B, Biological Sciences 364, 1035–1038.Google Scholar
Obata, S. (1987) Mating behaviour and sperm transfer in the ladybird beetle, Harmonia axyridis Pallas (Coleoptera: Coccinellidae). Applied Entomological Zoology 22, 434–442.Google Scholar
O'Donald, P. & Majerus, M.E.N. (1984) Polymorphism of melanic ladybirds maintained by frequency-dependent sexual selection. Biological Journal of the Linnean Society 23, 101–111.Google Scholar
Omkar, & James, B.E. (2005) Reproductive behaviour of an aphidophagous ladybeetle Coccinella transversalis (Coleoptera: Coccinellidae). International Journal of Tropical Insect Science 25, 96–102.Google Scholar
Omkar, & Mishra, G. (2005 a) Evolutionary significance of promiscuity in an aphidophagous ladybird, Propylea dissecta (Coleoptera: Coccinellidae). Bulletin of Entomological Research 95, 527–533.Google Scholar
Omkar, & Mishra, G. (2005 b) Mating in aphidophagous ladybirds: costs and benefits. Journal of Applied Entomology 129, 432–436.Google Scholar
Omkar, & Pervez, A. (2005) Mating behavior of an aphidophagous ladybird beetle, Propylea dissecta (Mulsant). Journal of Insect Science 12, 37–44.Google Scholar
Omkar, & Srivastava, S. (2002) The reproductive behaviour of an aphidophagous ladybeetle, Coccinella septempunctata (Coleoptera: Coccinellidae). European Journal of Entomology 99, 465–470.Google Scholar
Omkar, , Singh, S.K. & Pervez, A. (2006) Influence of mating duration on fecundity and fertility in two aphidophagous ladybirds. Journal of Applied Entomology 130, 103–107.Google Scholar
Omkar, , Singh, S.K. & Mishra, G. (2010 a) Multiple matings affect the reproductive performance of the aphidophagous ladybird beetle, Coelophora saucia (Coleoptera: Coccinellidae). European Journal of Entomology 107, 177–182.Google Scholar
Omkar, , Singh, S.K. & Mishra, G. (2010 b) Parental age at mating affects reproductive attributes of the aphidophagous ladybird beetle, Coelophora saucia (Coleoptera: Coccinellidae). European Journal of Entomology 107, 341–347.Google Scholar
Parker, G.A. & Simmons, L.W. (1989) Nuptial feeding in insects: theoretical models of male and female interests. Ethology 82, 3–26.Google Scholar
Parthasarathy, R., Tan, A., Sun, Z., Chen, Z., Rankin, M. & Palli, S.R. (2009) Juvenile hormone regulation of male accessory gland activity in the red flour beetle, Tribolium castaneum. Mechanisms of Development 126, 563–579.Google Scholar
Perry, J.C. & Rowe, L. (2008) Ingested spermatophores accelerate reproduction and increase mating resistance but are not a source of sexual conflict. Animal Behaviour 76, 993–1000.Google Scholar
Perry, J.C. & Rowe, L. (2010) Condition-dependent ejaculate size and composition in a ladybird beetle. Proceedings of the Royal Society of London. Series B. Biological Sciences 1700, 3639–3647.Google Scholar
Poiani, A. (2006) Complexity of seminal fluid: a review. Behavioral Ecology and Sociobiology 60, 289–310.Google Scholar
Quinones Pando, F.J., Chavez-Sanchez, N. & Tarango Rivero, S.H. (2001) Effect of the time of availability of the male in the fecundity of Harmonia axyridis Pallas (Coleoptera: Coccinellidae). Folio Entomologica Mexicana 40, 47–52.Google Scholar
Reinhardt, K., Wong, C.H. & Georgiou, A.S. (2009) Seminal fluid proteins in the bed bug, Cimex lectularius, detected using two-dimensional gel electrophoresis and mass spectrometry. Parasitology 136, 283–292.CrossRefGoogle ScholarPubMed
Reinhardt, K., Naylor, R. & Siva-Jothy, M.T. (2011) Male mating rate is constrained by seminal fluid availability in bedbugs, Cimex lectularius. Public Library of Science One 6, e22082.Google Scholar
Ridley, M. (1988) Mating frequency and fecundity in insects. Biological Reviews 63, 509–549.Google Scholar
Simmons, L.W. & Siva-Jothy, M.T. (1998) Sperm competition in insects: mechanisms and potential for selection. pp. 341–434in Birkhead, T.R. & Moller, A.P. (Eds) Sperm Competition and Sexual Selection. San Diego, CA, USA, Academic Press.Google Scholar
Srivastava, S. & Omkar, (2005) Short- and long-term benefits of promiscuity in the seven-spotted ladybird Coccinella septempunctata (Coleoptera: Coccinellidae). International Journal of Tropical Insect Science 25, 176–181.Google Scholar
Vargas, G., Michaud, J.P. & Nechols, J.R. (2012 a) Maternal effects shape dynamic trajectories of reproductive allocation in the ladybird Coleomegilla maculata. Bulletin of Entomological Research 102, 558–565.Google Scholar
Vargas, G., Michaud, J.P. & Nechols, J.R. (2012 b) Larval food supply constrains female reproductive schedules in Hippodamia convergens (Coleoptera: Coccinellidae). Annals of the Entomological Society of America 105, 832–839.Google Scholar
Vargas, G., Michaud, J.P. & Nechols, J.R. (2012 c) Cryptic maternal effects in Hippodamia convergens (Coleoptera: Coccinellidae) vary with maternal age and body size. Entomologia Experimentalis et Applicata 146, 302–311.CrossRefGoogle Scholar
Wang, S., Michaud, J.P., Zhang, R., Zhang, F. & Liu, S. (2009) Seasonal cycles of assortative mating and reproductive behaviour in polymorphic populations of Harmonia axyridis in China. Ecological Entomology 34, 483–494.Google Scholar
Wang, S., Michaud, J.P., Tan, X.L., Murray, L. & Zhang, F. (2013) Melanism in a Chinese population of Harmonia axyridis (Coleoptera: Coccinellidae): A citerion for male investment with pleiotropic effects on behavior and fertility. Journal of Insect Behavior (in press).Google Scholar
Wedell, N. (2005) Female receptivity in butterflies and moths. Journal of Experimental Biology 208, 3433–3440.Google Scholar
Wilson, N., Tufton, T.J. & Eady, P.E. (1999) The effect of single, double, and triple matings on the lifetime fecundity of Callosobruchus analis and Callosobruchus maculatus (Coleoptera: Bruchidae). Journal of Insect Behavior 12, 295–306.Google Scholar
Yadav, R., Yadav, N., Yadav, R. & Katiyar, R.R. (2011) Predation by various predators on major insect pests of field crops in Uttar Pradesh. Journal of Experimental Zoology 14, 637–638.Google Scholar
Yaginuma, T., Mizuno, T., Mizuno, C., Wada, T., Hattori, K., Yamashita, O. & Happ, G.M. (1996) Trehalase in the spermatophore from the bean-shaped accessory gland of the male mealworm beetle, Tenebrio molitor: Purification, kinetic properties and localization of the enzyme. Journal of Comparative Physiology. B, Biochemical, Systemic, and Environmental Physiology 166, 1–10.Google Scholar