Hostname: page-component-745bb68f8f-f46jp Total loading time: 0 Render date: 2025-01-26T22:56:14.660Z Has data issue: false hasContentIssue false
  • English
  • Français

Paternal effects correlate with female reproductive stimulation in the polyandrous ladybird Cheilomenes sexmaculata

Published online by Cambridge University Press:  24 March 2014

M.A. Mirhosseini ,
J.P. Michaud ,
M.A. Jalali  and
M. Ziaaddini
M.A. Mirhosseini
Affiliation:
Department of Crop Protection, Agriculture College, Vali-e-Asr University of Rafsanjan, Rafsanjan, Iran
J.P. Michaud*
Affiliation:
Department of Entomology, Kansas State University, Agricultural Research Center-Hays, Hays, Kansas, USA
M.A. Jalali
Affiliation:
Department of Crop Protection, Agriculture College, Vali-e-Asr University of Rafsanjan, Rafsanjan, Iran
M. Ziaaddini
Affiliation:
Department of Crop Protection, Agriculture College, Vali-e-Asr University of Rafsanjan, Rafsanjan, Iran
*
*Author for correspondence Phone: 785-625-3425 Fax: 785-623-4369 Email: jpmi@ksu.edu
Get access Rights & Permissions [Opens in a new window]

Abstract

Components of male seminal fluids are known to stimulate fecundity and fertility in females of numerous insect species and paternal effects on offspring phenotype are also known, but no studies have yet demonstrated links between male effects on female reproduction and those on progeny phenotype. In separate laboratory experiments employing 10-day-old virgin females of Cheilomenes sexmaculata (F.), we varied male age and mating history to manipulate levels of male allomones and found that the magnitude of paternal effects on progeny phenotype was correlated with stimulation of female reproduction. Older virgin males remained in copula longer than younger ones, induced higher levels of female fecundity, and sired progeny that developed faster to yield heavier adults. When male age was held constant (13 days), egg fertility declined as a function of previous male copulations, progeny developmental times increased, and the adult weight of daughters declined. These results suggest that male epigenetic effects on progeny phenotype act in concert with female reproductive stimulation; both categories of effects increased as a consequence of male celibacy (factor accumulation), and diminished as a function of previous matings (factor depletion). Male factors that influence female reproduction are implicated in sexual conflict and parental effects may extend this conflict to offspring phenotype. Whereas mothers control the timing of oviposition events and can use maternal effects to tailor progeny phenotypes to prevailing or anticipated conditions, fathers cannot. Since females remate and dilute paternity in polyandrous systems, paternal fitness will be increased by linking paternal effects to female fecundity stimulation, so that more benefits accrue to the male's own progeny.

Keywords

developmentfecundityfertilitysexual conflict
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 104 , Issue 4 , August 2014 , pp. 480 - 485
Copyright
Copyright © Cambridge University Press 2014 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Adler, M.I. & Bonduriansky, R. (2013) Paternal effects on offspring fitness reflect father's social environment. Evolutionary Biology 40, 288–292.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 . International Journal of Tropical Insect Science 27, 78–84.Google Scholar
Bonduriansky, R. & Head, M. (2007) Maternal and paternal condition effects on offspring phenotype in Telostylinus angusticollis (Diptera: Neriidae). Journal of Evolutionary Biology 20, 2379–2388.Google Scholar
Brown, W.D., Crespi, B.J. & Choe, J.C. (1997) Sexual conflict and the evolution of mating systems. pp. 352–377 in Choe, J.C. & Crespi, B.J. (Eds) The Evolution of Mating Systems in Insects and Arachnids. Cambridge, UK, Cambridge University Press.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
Eberhard, W.G. (1996) What is cryptic female choice? pp. 4–43 in Eberhard, W.G. (Ed.) Female Control: Sexual Selection by Cryptic Female Choice. Princeton, New Jersey, Princeton University Press.Google Scholar
Eberhard, W.G. (1997) Sexual selection by cryptic female choice in insects and arachnids. pp 32–57 in Choe, J.C. & Crespi, B.J. (Eds) The Evolution of Mating Systems in Insects and Arachnids. Cambridge, UK, Cambridge 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
Gioti, A., Wigby, S., Wertheim, B., Schuster, E., Martinez, P., Pennington, C.J., Partridge, L. & Chapman, T. (2012) Sex peptide of Drosophila melanogaster males is a global regulator of reproductive processes in females. Proceedings of the Royal Society of London, Series B 279, 4423–4432.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.Google Scholar
Hunt, J. & Simmons, L.W. (2000) Maternal and paternal effects on offspring phenotype in the dung beetle Onthophagus taurus . Evolution 54, 936–941.Google Scholar
Majerus, M.E.N. (1994) Female promiscuity maintains high fertility in ladybirds (Coleoptera: Coccinellidae). Entomologist's Monthly Magazine 130, 205–209.Google Scholar
Michaud, J.P. & Qureshi, J.A. (2006) Reproductive diapause in Hippodamia convergens (Coleoptera: Coccinellidae) and its life history consequences. Biological Control 39, 193–200.Google Scholar
Michaud, J.P., Bista, M., Mishra, G. & Singh, O. (2013) Sexual activity diminishes male virility in two Coccinella species: consequences for female fertility and progeny development. Bulletin of Entomological Research 103, 570–577.Google Scholar
Miller, P.M., Gavrilet, S. & Rice, W.R. (2006) Sexual conflict via maternal-effect genes in ZW species. Science 312, 73.Google Scholar
Mishra, G. & Omkar, (2006) Ageing trajectory and longevity trade-off in an aphidophagous ladybird, Propylea dissecta (Coleoptera: Coccinellidae). European Journal of Entomology 103, 33–40.Google Scholar
Mousseau, T.A. & Dingle, H. (1991) Maternal effects in insect life histories. Annual Review of Entomology 36, 511–534.Google Scholar
Mousseau, T.A. & Fox, C.W. (1998) Maternal Effects as Adaptations. New York, USA, 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, 364, 1035–1038.Google Scholar
Obata, S. (1987) Mating behavior and sperm transfer in the ladybird beetle, Harmonia axyridis Pallas (Coleoptera: Coccinellidae). Applied Entomology and Zoology 22, 434–442.Google Scholar
Omkar, & Mishra, G. (2005) Evolutionary significance of promiscuity in an aphidophagous ladybird, Propylea dissecta . Bulletin of Entomological Research 95, 527–533.Google Scholar
Omkar, & Pervez, A. (2005) Mating behaviour of an aphidophagous ladybird beetle, Propylea dissecta (Mulsant). Insect Science 12, 37–44.Google Scholar
Omkar, & Singh, S.K. (2009) Effect of parental ageing on offspring developmental and survival attributes in an aphidophagous ladybird, Cheilomenes sexmaculata . Journal of Applied Entomology 133, 500–504.Google Scholar
Omkar, , Mishra, G. & Singh, S.K. (2006 a) Optimal number of matings in two aphidophagous ladybirds. Ecological Entomology 31, 1–14.Google Scholar
Omkar, , Singh, S.K. & Singh, K. (2006 b) Effect of age on reproductive attributes of an aphidophagous ladybird, Cheilomenes sexmaculata . Insect Science 13, 301–308.Google Scholar
Omkar, , Singh, S.K. & Mishra, G. (2010) 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
Omkar, , Sahu, J. & Kumar, G. (2013) Age specific mating incidence and reproductive behavior of the ladybird beetle, Anegleis cardoni (Weise) (Coleoptera: Coccinellidae). Journal of Asia-Pacific Entomology 16, 263–268.Google Scholar
Qvarnstrom, A. & Price, T.D. (2001) Maternal effects, paternal effects and sexual selection. Trends in Ecology and Evolution 16, 95–100.Google Scholar
Semyanov, V.P. (1970) Biological properties of Adalia bibunctata L. (Coleoptera: Coccinellidae) in conditions of Leningrad region. Zashchita Rastenii ot Vreditelei i Boleznei 127, 105–112 (in Russian).Google Scholar
Shea, N., Pen, I. & Uller, T. (2011) Three epigenetic information channels and their different roles in evolution. Journal of Evolutionary Biology 24, 1178–1187.Google Scholar
Simmons, L.W. & Garcia-Gonzalez, F. (2007) Female crickets trade offspring viability for fecundity. Journal of Evolutionary Biology 20, 1617–1623.CrossRefGoogle ScholarPubMed
SPSS (2006) Version 15.0. Chicago, Illinois, SPSS Inc.Google Scholar
Srivastava, S. & Omkar, (2004) Age-specific mating and reproductive senescence in the seven-spotted ladybird, Coccinella septempunctata . Journal of Applied Entomology 128, 452–458.Google Scholar
Tregenza, T. & Wedell, N. (2002) Polyandrous females avoid costs of inbreeding. Nature 415, 71–73.Google Scholar
Vargas, G.A., Michaud, J.P. & Nechols, J.R. (2012 a) Cryptic maternal effects in Hippodamia convergens vary with maternal age and body size. Entomologia Experimentalis et Applicata 146, 302–311.Google Scholar
Vargas, G.A., Michaud, J.P. & Nechols, J.R. (2012 b) Maternal effects shape dynamic trajectories of reproductive allocation in the ladybird Coleomegilla maculata . Bulletin of Entomological Research 102, 558–565.Google Scholar
Wedell, N., Kvarnemo, C., Lessells, M. & Tregenza, T. (2006) Sexual conflict and life histories. Animal Behaviour 71, 999–1011.Google Scholar