Skip to main content
SpringerLink
Log in

Paternity following multiple mating in ladybird Harmonia axyridis

  • Published:
BioControl Aims and scope Submit manuscript

Abstract

We investigated factors which may determine realised paternity following multiple mating in a promiscuous ladybird Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae), namely the mating order and ability of males of different morphs to fertilize females. In experiments using males of two colour morphs, we found that the first male had a reproductive advantage over the second male (sperm precedence P2 = 0.38). Males of the melanic morph spectabilis had a reproductive advantage over males of the semi-melanic morph axyridis (P2 = 0.35). Analysis of paternity using microsatellites applied to young larvae, which avoids possible differential mortality of progeny, confirmed the precedence of the first male and higher paternity rate of colour morphs that are more frequent in the wild. Hatchability of eggs increased from 65% after the first mating to 85% after the second mating delayed by five days. Average duration of mating was 157 min and did not differ between the first and second mating and between the colour morphs of males.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Awad M, Kalushkov P, Nedvědová T, Nedvěd O (2013) Fecundity and fertility of ladybird beetle Harmonia axyridis after a prolonged cold storage. BioControl 58:657–666

    Article  Google Scholar 

  • Awad M, Kalushkov P, Karabüyük F, Nedvěd O (2015a) Non-random mating activity of colour morphs of ladybird Harmonia axyridis (Coleoptera: Coccinellidae). Acta Soc Zool Bohem 79:11–17

    Google Scholar 

  • Awad M, Laugier G, Loiseau A, Nedvěd O (2015b) Unbalanced polyandry in wild-caught ladybirds Harmonia axyridis (Coleoptera: Coccinellidae). Appl Entomol Zool 50:427–434

    Article  Google Scholar 

  • Bateman AJ (1948) Intra-sexual selection in Drosophila. Heredity 2:349–368

    Article  CAS  PubMed  Google Scholar 

  • Birkhead TR, Møller AP (eds) (1998) Sperm competition and sexual selection. Academic Press, London

    Google Scholar 

  • Chapuis M, Estoup A (2007) Microsatellite null alleles and estimation of population differentiation. Mol Biol Evol 24:621–631

    Article  CAS  PubMed  Google Scholar 

  • Chaudhary DD, Mishra G, Omkar (2016) Last male wins the egg fertilization fight: a case study in ladybird, Menochilus sexmaculatus. Behav Process 131:1–8

    Article  Google Scholar 

  • Darwin C (1871) The descent of man, and selection in relation to sex. John Murray, London

    Book  Google Scholar 

  • De Jong PW, Verhoog MD, Brakefield PM (1993) Sperm competition and melanic polymorphism in the 2-spot ladybird, Adalia bipunctata (Coleoptera, Coccinellidae). Heredity 70:172–178

    Article  Google Scholar 

  • De Jong PW, Brakefield PM, Geerinck BP (1998) The effect of female mating history on sperm precedence in the two-spot ladybird, Adalia bipunctata (Coleoptera, Coccinellidae). Behav Ecol 9:559–565

    Article  Google Scholar 

  • Dougherty LR, Simmons LW, Shuker DM (2016) Postcopulatory sexual selection when a female mates once Commentary. Anim Behav 116:13–16

    Article  Google Scholar 

  • Eberhard WG (1996) Female control: sexual selection by cryptic female choice. Princeton University Press, Princeton

    Google Scholar 

  • Garcia-Gonzalez F, Simmons LW (2007) Paternal indirect genetic effects on offspring viability and the benefits of polyandry. Curr Biol 17:32–36

    Article  CAS  PubMed  Google Scholar 

  • Haddrill PR, Shuker DM, Mayes S, Majerus MEN (2007) Temporal effects of multiple mating on components of fitness in the two-spot ladybird, Adalia bipunctata (Coleoptera: Coccinellidae). Eur J Entomol 104:393–398

    Article  Google Scholar 

  • Haddrill PR, Shuker DM, Amos W, Majerus MEN, Mayes S (2008) Female multiple mating in wild and laboratory populations of the two-spot ladybird, Adalia bipunctata. Mol Ecol 17:3189–3197

    Article  PubMed  Google Scholar 

  • Haelewaters D, Zhao S, Clusella-Trullas S, Cottrell TE, De Kese A, Fiedler L, Herz A, Hesketh H, Hui C, Kleespies RG, Losey JE, Minaar IA, Murray KM, Nedvěd O, Pfliegler WP, Raak-van den Berg CL, Riddick EW, Shapiro-Ilan DI, Smyth RR, Steenberg T, van Wielink PS, Viglášová S, Zhao Z, Ceryngier P, Roy HE (2017) Parasites of Harmonia axyridis: current research and perspectives. BioControl. doi:10.1007/s10526-016-9766-8

    Google Scholar 

  • Harvey IF, Parker GA (2000) ‘Sloppy’ sperm mixing and intraspecific variation in sperm precedence (P-2) patterns. Proc Royal Soc B 267:2537–2542

    Article  CAS  Google Scholar 

  • Hodek I (1973) Biology of Coccinellidae. Springer, The Hague and Academia, Prague

  • Hodek I, Ceryngier P (2000) Sexual activity in Coccinellidae (Coleoptera): a review. Eur J Entomol 97:449–456

    Article  CAS  Google Scholar 

  • Jones O, Wang J (2009) Colony: a program for parentage and sibship inference from multilocus genotype data. Mol Ecol Res 10:551–555

    Article  Google Scholar 

  • Kaufmann T (1996) Dynamics of sperm transfer, mixing, and fertilization in Cryptolaemus montrouzieri in Kenya. Ann Entomol Soc Am 89:238–242

    Article  Google Scholar 

  • Kenis M, Adriaens T, Brown PMJ, Katsanis A, San Martin G, Branquart E, Maes D, Eschen R, Zindel R, van Vlaenderen J, Babendreier D, Roy HE, Hautier L, Poland RL (2017) Assessing the ecological risk posed by a recently established invasive alien predator: Harmonia axyridis as a case study. BioControl. doi:10.1007/s10526-016-9764-x

    Google Scholar 

  • Loiseau A, Malausa T, Lombaert E, Martin J, Estoup A (2009) Isolation and characterization of microsatellites in the harlequin ladybird, Harmonia axyridis (Coleoptera, Coccinellidae), and cross-species amplification within the family Coccinellidae. Perm Gen Res Note 934–937

  • Mishra G, Omkar (2014) Phenotype-dependent mate choice in Propylea dissecta and its fitness consequences. J Ethol 32:165–172

    Article  Google Scholar 

  • Nedvěd O, Honěk A (2012) Life history and development. In: Hodek I, van Emden H, Honěk A (eds) Ecology and behaviour of the ladybird beetles (Coccinellidae). Wiley-Blackwell, London, pp 54–109

    Chapter  Google Scholar 

  • Nedvědová T, Awad M, Ungerová D, Nedvěd O (2013) Characteristics of ladybird Harmonia axyridis during autumn migration. IOBC/WPRS Bull 94:117–122

    Google Scholar 

  • Obata S (1988) Mating behaviour and sperm transfer in the ladybird beetle, Harmonia axyridis Pallas (Coleoptera: Coccinellidae). In: Niemczyk E, Dixon AFG (eds) Ecology and effectiveness of Aphidphaga. SPB Academic Publishing, The Hague, pp 39–42

    Google Scholar 

  • Obata S, Hidaka T (1987) Ejection and ingestion of the spermatophore by the female ladybird beetle, Harmonia axyridis Pallas (Coleoptera: Coccinellidae). Can Entomol 119:603–604

    Article  Google Scholar 

  • Obata S, Johki Y (1991) Comparative study on copulatory behaviour in four species of aphidophagous ladybirds. In: Polgár L, Chambers RJ, Dixon AFG, Hodek I (eds) Proceedings of 4th meeting of the IOBC W.G. Ecology of Aphidophaga, September 1990, Gödöllö, Hungary. SPB Academic, The Hague, pp 207–212

  • Okuda T (2000) DNA synthesis by testicular follicles in a lady-beetle, Coccinella septempunctata brucki (Coleoptera: Coccinellidae) in relation to aestivation diapause. Invertebr Reprod Dev 38:71–79

    Article  CAS  Google Scholar 

  • Omkar, Singh SK, Singh K (2006) Effect of age on reproductive attributes of aphidophagous ladybird, Chilomenes sexmaculata. Insect Sci 13:301–308

    Article  Google Scholar 

  • Omkar, Sahu J (2012) Costs and benefits of reproduction in predaceous ladybird: effect of multiple matings on reproduction and offspring development. J Asia-Pacific Entomol 15:219–224

    Article  Google Scholar 

  • Osawa N, Nishida T (1992) Seasonal variation in elytral colour polymorphism in Harmonia axyridis (the ladybird beetle): the role of non-random mating. Heredity 69:297–307

    Article  Google Scholar 

  • Parker GA (1970) Sperm competition and its evolutionary consequences in insects. Biol Rev 45:525–567

    Article  Google Scholar 

  • Perry JC, Sharpe DMT, Rowe L (2009) Condition-dependent female remating resistance generates sexual selection on male size in a ladybird beetle. Anim Behav 77:743–748

    Article  Google Scholar 

  • R Core Team (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/

  • Reznik SY, Dolgovskaya MY, Ovchinnikov AN (2015) Effect of photoperiod on adult size and weight in Harmonia axyridis (Coleoptera: Coccinellidae). Eur J Entomol 112:642–647

    Google Scholar 

  • Riddick EW (2017) Spotlight on the positive effects of the invasive ladybird Harmonia axyridis on agriculture. BioControl. doi:10.1007/s10526-016-9758-8

    Google Scholar 

  • Roy HE, Brown PMJ, Adriaens T, Berkvens N, Borges I, Clusella-Trullas S, Comont RF, De Clercq P, Eschen R, Estoup A, Evans EW, Facon B, Gardiner MM, Gil A, Grez AA, Guillemaud T, Haelewaters D, Herz A, Honek A, Howe AG, Hui C, Hutchison WD, Kenis M, Koch RL, Kulfan J, Lawson Handley L, Lombaert E, Loomans A, Losey J, Lukashuk AO, Maes D, Magro A, Murray KM, San Martin G, Martinkova Z, Minnaar IA, Nedved O, Orlova-Bienkowskaja MJ, Osawa N, Rabitsch W, Ravn HP, Rondoni G, Rorke SL, Ryndevich SK, Saethre M-G, Sloggett JJ, Soares AO, Stals R, Tinsley MC, Vandereycken A, van Wielink P, Viglášová S, Zach P, Zakharov IA, Zaviezo T, Zhao Z (2016) The harlequin ladybird, Harmonia axyridis: global perspectives on invasion history and ecology. Biol Invasions 18:997–1044

    Article  Google Scholar 

  • Shahid M, Siddiqui A, Omkar, Mishra G (2016) Mating alters the rate of development of ovarioles in the ladybird, Propylea dissecta (Coleoptera: Coccinellidae). Eur J Entomol 113:44–50

    Article  Google Scholar 

  • Simmons LW (2001) The evolution of polyandry: an examination of the genetic incompatibility and good-sperm hypotheses. J Evol Biol 14:585–594

    Article  Google Scholar 

  • Soper D (2013) Statistics calculators v. 3.0 beta. http://www.danielsoper.com/statcalc3/default.aspx. Accessed 4 Apr 2013

  • StatSoft, Inc. (2011) STATISTICA (data analysis software system), version 10. http://www.statsoft.com

  • Thomas ML, Simmons LW (2015) No coolidge effect in the Australian field cricket Teleogryllus oceanicus (Orthoptera: Gryllidae). Austral Entomol 54:433–437

    Article  Google Scholar 

  • Thornhill R, Alcock J (1983) The evolution of insect mating systems. Harvard University Press, Cambridge

    Book  Google Scholar 

  • Ueno H (1994) Intraspecific variation of P2 value in a coccinellid beetle, Harmonia axyridis. J Ethol 12:169–174

    Article  Google Scholar 

  • Ueno H (1996) Estimate of multiple insemination in a natural population of Harmonia axyridis (Coleoptera: Coccinellidae). Appl Entomol Zool 31:621–623

    Google Scholar 

  • Wang S, Tan XL, Michaud JP, Shi ZK, Zhang F (2015) Sexual selection drives the evolution of limb regeneration in Harmonia axyridis (Coleoptera: Coccinellidae). Bull Entomol Res 105:245–252

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The study was conducted with support from the Ministry of Agriculture, grant number QH82047, mobility project ASRT-16-06 funded by the Academy of Science of the Czech Republic, and with institutional support RVO:60077344 in Biology Center. We are grateful to Tom Fayle and John Sloggett for their valuable comments and corrections of the early version of the manuscript and an anonymous reviewer for his persistent force on the later improvement.

Author information

Authors and Affiliations

  1. Faculty of Science, University of South Bohemia, Branisovska 1760, Ceske Budejovice, Czech Republic

    Mona Awad, Lubomír Piálek, Alena Krejčí & Oldřich Nedvěd

  2. Institute of Entomology, Academy of Sciences of the Czech Republic, Branisovska 31, Ceske Budejovice, Czech Republic

    Mona Awad, Alena Krejčí & Oldřich Nedvěd

  3. Faculty of Agriculture, Cairo University, Giza, 12613, Egypt

    Mona Awad

  4. INRA-CBGP, Cedex 5, 34398, Montpellier, France

    Guillaume Laugier

  5. Centro de Estudios Avanzados en Zonas Áridas, Raúl Bitrán 1305, La Serena, Chile

    Guillaume Laugier

Authors
  1. Mona Awad
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Lubomír Piálek
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Alena Krejčí
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Guillaume Laugier
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Oldřich Nedvěd
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Oldřich Nedvěd.

Additional information

Handling Editor: Helen Roy.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 294 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Awad, M., Piálek, L., Krejčí, A. et al. Paternity following multiple mating in ladybird Harmonia axyridis . BioControl 62, 297–307 (2017). https://doi.org/10.1007/s10526-017-9806-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10526-017-9806-z

Keywords

Search

Navigation