Skip to main content
SpringerLink
Log in

Variation of clutch size and trophic egg proportion in a ladybird with and without male-killing bacterial infection

  • Original Paper
  • Published:
Evolutionary Ecology Aims and scope Submit manuscript

Abstract

Maternally inherited bacterial endosymbionts can kill male embryos of their arthropod hosts to enhance the transmission efficiency of the endosymbionts. The resources from killed male eggs can be reallocated to infected female hatchlings as additional maternal investment. As a result, the number of offspring per patch and the maternal investment per offspring are expected to differ from the original optimal values for the host mother. Thus, in response to infection, these trait values should be adjusted to maximize the lifetime reproductive success of host females and the fitness of inherited endosymbionts as well. Here, we examined clutch size, egg size, and the proportion of trophic eggs (i.e., production of unhatched eggs, a maternal phenotype) per clutch of host mothers infected with male-killing bacteria. First, we developed a mathematical model to predict the optimal clutch size and trophic egg proportion in uninfected and infected females. Next, we experimentally compared these life-history traits in a ladybird, Harmonia yedoensis, between females infected or uninfected with male-killing Spiroplasma bacteria. Consistent with our predictions, clutch size was larger, egg size was smaller, and trophic egg proportion was lower in infected H. yedoensis females, compared with uninfected females. To our knowledge, this is the first empirical demonstration of variation in these life-history traits depending on infection with bacterial endosymbionts.

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
Fig. 4

Similar content being viewed by others

References

  • Baba N, Hironaka M, Hosokawa T et al (2011) Trophic eggs compensate for poor offspring feeding capacity in a subsocial burrower bug. Biol Lett 7:194–196

    Article  PubMed  Google Scholar 

  • Bandi C, Dunn AM, Hurst GD et al (2001) Inherited microorganisms, sex-specific virulence and reproductive parasitism. Trends Parasitol 17:88–94

    Article  CAS  PubMed  Google Scholar 

  • Bian G, Xu Y, Lu P et al (2010) The endosymbiotic bacterium Wolbachia induces resistance to dengue virus in Aedes aegypti. PLoS Pathog 6:e1000833

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brownlie JC, Cass BN, Riegler M et al (2009) Evidence for metabolic provisioning by a common invertebrate endosymbiont, Wolbachia pipientis, during periods of nutritional stress. PLoS Pathog 5:e1000368

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brumin M, Kontsedalov S, Ghanim M (2011) Rickettsia influences thermotolerance in the whitefly Bemisia tabaci B biotype. Insect Sci 18:57–66

    Article  Google Scholar 

  • Crespi BJ (1992) Cannibalism and trophic egg in subsocial and eusocial insects. In: Elgar MA, Crespi BJ (eds) Cannibalism: ecology and evolution among diverse taxa. Oxford University Press, New York, pp 176–213

    Google Scholar 

  • Elnagdy S, Majerus MEN, HANDLEY LJL (2011) The value of an egg: resource reallocation in ladybirds (Coleoptera: Coccinellidae) infected with male-killing bacteria. J Evol Biol 24:2164–2172

    Article  CAS  PubMed  Google Scholar 

  • Elnagdy S, Majerus MEN, Gardener M et al (2013) The direct effects of male killer infection on fitness of ladybird hosts (Coleoptera: Coccinellidae). J Evol Biol 26:1816–1825

    Article  CAS  PubMed  Google Scholar 

  • Engelstädter J, Hurst GD (2007) The impact of male-killing bacteria on host evolutionary processes. Genetics 175:245–254

    Article  PubMed  PubMed Central  Google Scholar 

  • Engelstädter J, Hurst GD (2009) The ecology and evolution of microbes that manipulate host reproduction. Ann Rev Ecol Evol Syst 40:127–149

    Article  Google Scholar 

  • Feldhaar H (2011) Baterial symbionts as mediators of ecologically important traits of insect hosts. Ecol Entomol 36:533–543

    Article  Google Scholar 

  • Ferrari J, Vavre F (2011) Bacterial symbionts in insects or the story of communities affecting communities. Philo Trans Roy Soc B Biol Sci 366:1389–1400

    Article  Google Scholar 

  • Gelman A, Carlin JB, Stern HS et al (2014) Bayesian data analysis, vol 2. Chapman and Hall/CRC, London

    Google Scholar 

  • Goodacre SL, Martin OY (2012) Modification of insect and arachnid behaviours by vertically transmitted endosymbionts: infections as drivers of behavioural change and evolutionary novelty. Insects 3:246–261

    Article  PubMed  PubMed Central  Google Scholar 

  • Goodacre SL, Martin OY, Bonte D et al (2009) Microbial modification of host long-distance dispersal capacity. BMC Biol 7:32

    Article  PubMed  PubMed Central  Google Scholar 

  • Hedges LM, Brownlie JC, O’Neill SL et al (2008) Wolbachia and virus protection in insects. Science 322:702

    Article  CAS  PubMed  Google Scholar 

  • Hilgenboecker K, Hammerstein P, Schlattmann P et al (2008) How many species are infected with Wolbachia?—a statistical analysis of current data. FEMS Microbiol Lett 281:215–220

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hurst LD (1991) The incidences and evolution of cytoplasmic male killers. Proc R Soc Lond B Biol Sci 244:91–99

    Article  Google Scholar 

  • Hurst GDD, Jiggins FM (2000) Male-killing bacteria in insects: mechanism, incidence, and implications. Emerg Infec Dis 6:329–336

    Article  CAS  Google Scholar 

  • Hurst GDD, Majerus MEN (1993) Why do maternally inherited microorganisms kill males? Heredity 71:81–95

    Article  Google Scholar 

  • Hurst GDD, McVean GAT (1998) Parasitic male-killing bacteria and the evolution of clutch size. Ecol Entomol 23:350–353

    Article  Google Scholar 

  • Hurst GG, Hurst LD, Majerus MEN (1997) Cytoplasmic sex-ratio distorters. In: O’Neill SL, Hoffmann AA, Werren JH (eds) Influential passengers: inherited microorganisms and arthropod reproduction. Oxford University Press, Oxford, pp 125–154

    Google Scholar 

  • Jaenike J (2007) Fighting back against male-killers. Trends Ecol Evol 22:167–169

    Article  PubMed  Google Scholar 

  • Jaenike J, Dyer KA, Reed LK (2003) Within-population structure of competition and the dynamics of male-killing Wolbachia. Evol Ecol Res 5:1023–1036

    Google Scholar 

  • Jaenike J, Unckless R, Cockburn SN et al (2010) Adaptation via symbiosis: recent spread of a Drosophila defensive symbiont. Science 329:212–215

    Article  CAS  PubMed  Google Scholar 

  • Kenyon SG, Hunter MS (2007) Manipulation of oviposition choice of the parasitoid wasp, Encarsia pergandiella, by the endosymbiotic bacterium Cardinium. J Evol Biol 20:707–716

    Article  CAS  PubMed  Google Scholar 

  • Kudo S, Nakahira T (2004) Effects of trophic-eggs on offspring performance and rivalry in a sub-social bug. Oikos 107:28–35

    Article  Google Scholar 

  • Kudo S, Nakahira T (2005) Trophic-egg production in a subsocial bug: adaptive plasticity in response to resource conditions. Oikos 111:459–464

    Article  Google Scholar 

  • Majerus MEN (2003) Sex wars: genes, bacteria, and biased sex ratios. Princeton University Press, Princeton

    Google Scholar 

  • Majerus MEN, Majerus TMO (2000) Female-biased sex ratio due to male-killing in the Japanese ladybird Coccinula sinensis. Ecol Entomol 25:234–238

    Article  Google Scholar 

  • Majerus TMO, Majerus MEN (2012) Male-killing in the Coccinellidae: testing the predictions. Evol Ecol 26:207–225

    Article  Google Scholar 

  • Miller WJ, Schneider D (2012) Endosymbiotic microbes as adaptive manipulators of arthropod behaviour and natural driving sources of host speciation. In: Hughes D, Brodeur J, Thomas F (eds) Host manipulation by parasites. Oxford University Press, Oxford, pp 119–137

    Chapter  Google Scholar 

  • Noriyuki S, Osawa N (2012) Intrinsic prey suitability in specialist and generalist Harmonia ladybirds: a test of the trade-off hypothesis for food specialization. Entomol Exp Appl 144:279–285

    Article  Google Scholar 

  • Noriyuki S, Osawa N, Nishida T (2011) Prey capture performance in hatchlings of two sibling Harmonia ladybird species in relation to maternal investment through sibling cannibalism. Ecol Entomol 36:282–289

    Article  Google Scholar 

  • Noriyuki S, Kameda Y, Osawa N (2014) Prevalence of male-killer in a sympatric population of two sibling ladybird species, Harmonia yedoensis and Harmonia axyridis (Coleoptera: Coccinellidae). Eur J Entomol 111:307–311

    Google Scholar 

  • Osawa N (1992) Sibling cannibalism in the ladybird beetle Harmonia axyridis Pallas: fitness consequences for mothers and offspring. Res Popul Ecol 34:45–55

    Article  Google Scholar 

  • Osawa N, Ohashi K (2008) Sympatric coexistence of sibling species Harmonia yedoensis and H. axyridis (Coleoptera: Coccinellidae) and the roles of maternal investment through egg and sibling cannibalism. Eur J Entomol 105:445–454

    Article  Google Scholar 

  • Parker GA, Begon M (1986) Optimal egg size and clutch size: effects of environment and maternal phenotype. Am Nat 128:573–592

    Article  Google Scholar 

  • Parker GA, Courtney SP (1984) Models of clutch size in insect oviposition. Theor Popul Biol 26:27–48

    Article  Google Scholar 

  • Parker GA, Royle NJ, Hartley IR (2002) Intrafamilial conflict and parental investment: a synthesis. Philos Trans R Soc B 357:295–307

    Article  Google Scholar 

  • Perry JC, Roitberg BD (2005a) Games among cannibals: competition to cannibalize and parent-offspring conflict lead to increased sibling cannibalism. J Evol Biol 18:1523–1533

    Article  CAS  PubMed  Google Scholar 

  • Perry JC, Roitberg BD (2005b) Ladybird mothers mitigate offspring starvation risk by laying trophic eggs. Behav Ecol Sociobiol 58:578–586

    Article  Google Scholar 

  • Perry JC, Roitberg BD (2006) Trophic egg laying: hypotheses and tests. Oikos 112:706–714

    Article  Google Scholar 

  • Sasaji H (1998) Tentomushi no shizenshi (Natural history of the ladybirds). University of Tokyo Press, Tokyo

    Google Scholar 

  • Spiegelhalter DJ, Thomas A, Best NG et al (2003) WinBUGS version 1.4 users manual. Available from http://www.mrc-bsu.cam.ac.uk/wp-content/uploads/manual14.pdf (accessed March 2016)

  • Stouthamer R, Breeuwer JA, Hurst GD (1999) Wolbachia pipientis: microbial manipulator of arthropod reproduction. Annu Rev Microbiol 53:71–102

    Article  CAS  PubMed  Google Scholar 

  • Telschow A, Engelstädter J, Yamamura N et al (2006) Asymmetric gene flow and constraints on adaptation caused by sex ratio distorters. J Evol Biol 19:869–878

    Article  CAS  PubMed  Google Scholar 

  • Unckless RL, Jaenike J (2012) Maintenance of a male-killing Wolbachia in Drosophila innubila by male-killing dependent and male-killing independent mechanisms. Evolution 66:678–689

    Article  PubMed  Google Scholar 

  • Vala F, Egas M, Breeuwer JAJ et al (2004) Wolbachia affects oviposition and mating behaviour of its spider mite host. J Evol Biol 17:692–700

    Article  CAS  PubMed  Google Scholar 

  • Weeks AR, Reynolds KT, Hoffmann AA (2002) Wolbachia dynamics and host effects: what has (and has not) been demonstrated? Trends Ecol Evol 17:257–262

    Article  Google Scholar 

  • Werren JH, Baldo L, Clark ME (2008) Wolbachia: master manipulators of invertebrate biology. Nat Rev Microbiol 6:741–751

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This study was supported by a Grant-in-Aid for Scientific Research (No. 26840137) to S.N. and a Grant-in-Aid for JSPS Fellows (22.6920) to Y.S.O. from the Japan Society for the Promotion of Science.

Author information

Author notes

    Authors and Affiliations

    1. Department of Environmental Science, Policy, and Management, University of California, 201 Wellman Hall, Berkeley, CA, 94720, USA

      Suzuki Noriyuki

    2. Center for Geo-Environmental Science, Rissho University, 1700 Magechi, Kumagaya, Saitama, 360-0194, Japan

      Suzuki Noriyuki

    3. Division of Ecology and Evolutionary Biology, Graduate School of Life Sciences, Tohoku University, 6-3 Aramaki-Aoba, Aoba, Sendai, Miyagi, 980-8578, Japan

      Yukari Suzuki-Ohno

    4. School of Environmental Science, The University of Shiga Prefecture, 2500 Yasaka, Hikone, Shiga, 522-0057, Japan

      Koh-Ichi Takakura

    Authors
    1. Suzuki Noriyuki
      View author publications

      You can also search for this author in PubMed Google Scholar

    2. Yukari Suzuki-Ohno
      View author publications

      You can also search for this author in PubMed Google Scholar

    3. Koh-Ichi Takakura
      View author publications

      You can also search for this author in PubMed Google Scholar

    Corresponding author

    Correspondence to Suzuki Noriyuki.

    Ethics declarations

    Conflict of interest

    This study was supported by a Grant-in-Aid for Scientific Research (No. 26840137) to S.N. and a Grant-in-Aid for JSPS Fellows (22.6920) to Y.S.O. from the Japan Society for the Promotion of Science.

    Ethical standards

    All experiments using insects were carried out according to local ethical guidelines.

    Additional information

    The authors Suzuki Noriyuki and Yukari Suzuki-Ohno both are contributed equally.

    Electronic supplementary material

    Below is the link to the electronic supplementary material.

    Supplementary material 1 (PDF 11546 kb)

    Rights and permissions

    Reprints and permissions

    About this article

    Check for updates. Verify currency and authenticity via CrossMark

    Cite this article

    Noriyuki, S., Suzuki-Ohno, Y. & Takakura, KI. Variation of clutch size and trophic egg proportion in a ladybird with and without male-killing bacterial infection. Evol Ecol 30, 1081–1095 (2016). https://doi.org/10.1007/s10682-016-9861-4

    Download citation

    • Received:

    • Accepted:

    • Published:

    • Issue Date:

    • DOI: https://doi.org/10.1007/s10682-016-9861-4

    Keywords

    Search

    Navigation