Skip to main content
SpringerLink
Log in

Mating with large males decreases the immune defence of females in Drosophila melanogaster

  • Research Article
  • Published:
Journal of Genetics Aims and scope Submit manuscript

Abstract

Mating has been widely reported to be a costly event for females. Studies indicate that female cost of mating in terms of fecundity and survivorship can be affected by their mates, leading to antagonistic coevolution between the sexes. However, as of now, there is no evidence that the female cost of mating in terms of immune defence is affected by their mates. We assess the effect of different sized males on antibacterial immune defence and reproductive fitness of their mates. We used a large outbred population of Drososphila melanogaster as the host and Serratia marcescens as the pathogen. We generated three different male phenotypes: small, medium and large, by manipulating larval densities. Compared to females mating with small males, those mating with large males had higher bacterial loads and lower fecundity. There was no significant effect of male phenotype on the fraction of females mated or copulation duration (an indicator of ejaculate investment). Thus, our study is the first clear demonstration that male phenotype can affect the cost of mating to females in terms of their antibacterial immune defence. Mating with large males imposes an additional cost of mating to females in terms of reduced immune defence. The observed results are very likely due to qualitative/quantitative differences in the ejaculates of the three different types of males. If the phenotypic variation that we observed in males in our study is mirrored by genetic variation, then, it can potentially lead to antagonistic coevolution of the sexes over immune defence.

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

Similar content being viewed by others

References

  • Atkinson W. D. 1979 A field investigation of larval competition in domestic Drosophila. J. Anim. Ecol. 48, 91–102.

    Article  Google Scholar 

  • Bretman A., Fricke C. and Chapman T. 2009 Plastic responses of male Drosophila melanogaster to the level of sperm competition increase male reproductive fitness. Proc. R. Soc. London, Ser. B 276, 1705–1711.

    Article  Google Scholar 

  • Brown W. D., Bjork A., Schneider K. and Pitnick S. 2004 No evidence that polyandry benefits females in Drosophila melanogaster. Evolution 58, 1242–1250.

    PubMed  Google Scholar 

  • Chapman T., Liddle L. F., Kalb J. M., Wolfner M. F. and Partridge L. 1995 Cost of mating in Drosophila melanogaster females is mediated by male accessory gland products. Nature 373, 241–244.

    Article  PubMed  CAS  Google Scholar 

  • Chen P. S. 1984 The functional morphology and biochemistry of insect male accessory glands and their secretions. Annu. Rev. Entomol. 29, 233–255.

    Article  CAS  Google Scholar 

  • Chen P. S., Stumm-Zollinger E., Aigaki T., Balmer J., Bienz M. and Bohlen P. 1988 A male accessory gland peptide that regulates reproductive behavior of female D. melanogaster. Cell 54, 291–298.

    CAS  Google Scholar 

  • Chippindale A. K. and Rice W. R. 2001 Y chromosome polymorphism is a strong determinant of male fitness in Drosophila melanogaster. Proc. Natl. Acad. Sci. USA 98, 5677–5682.

    Article  PubMed  CAS  Google Scholar 

  • Cox C. R. and Gilmore M. S. 2007 Native microbial colonization of Drosophila melanogaster and its use as a model of Enterococcus faecalis pathogenesis. Infect. Immun. 75, 1565–1576.

    Article  PubMed  CAS  Google Scholar 

  • Fedorka K. M., Zuk M. and Mousseau T. A. 2004 Immune suppression and the cost of reproduction in the ground cricket, Allonemobius socius. Evolution 58, 2478–2485.

    PubMed  Google Scholar 

  • Fedorka K. M., Linder J. E., Winterhalter W. and Promislow D. 2007 Post-mating disparity between potential and realized immune response in Drosophila melanogaster. Proc. R. Soc. London, Ser. B 274, 1211–1217.

    Article  Google Scholar 

  • Fellowes M. D. E., Kraaijeveld A. and Godfray H. C. J. 1999 The relative fitness of Drosophila melanogaster (Diptera, Drosophilidae) that have successfully defended themselves against the parasitoid Asobara tabida (Hymenoptera, Braconidae). J. Evol. Biol. 12, 123–128.

    Article  Google Scholar 

  • Flyg C. and Xanthopoulos K. 1983 Insect pathogenic properties of Serratia marcescens. Passive and active resistance to insect immunity studied with protease-deficient and phage-resistant mutants. J. Gen. Microbiol. 129, 453–464.

    CAS  Google Scholar 

  • Flyg C., Kenne K. and Boman H. G. 1980 Insect pathogenic properties of Serratia marcescens: phage-resistant mutants with a decreased resistance to Cecropia immunity and a decreased virulence to Drosophila. J. Gen. Microbiol. 120, 173–181.

    Article  CAS  Google Scholar 

  • Fowler K. and Partridge L. 1989 A cost of mating in female fruitflies. Nature 338, 760–761.

    Article  Google Scholar 

  • Friberg U. 2006 Male perception of female mating status: its effect on copulation duration, sperm defence and female fitness. Anim. Behav. 72, 1259–1268.

    Article  Google Scholar 

  • Friberg U. and Arnqvist G. 2003 Fitness effects of female choice: preferred males are detrimental for Drosophila melanogaster females. J. Evol. Biol. 16, 797–811.

    Article  PubMed  CAS  Google Scholar 

  • Gilchrist A. S. and Partridge L. 2000 Why it is difficult to model sperm displacement in Drosophila melanogaster: the relation between sperm transfer and copulation duration. Evolution 54, 534–542.

    PubMed  CAS  Google Scholar 

  • Heifetz Y., Lung O., Frongillo E. A. and Wolfner M. F. 2000 The Drosophila seminal fluid protein Acp26Aa stimulates release of oocytes by the ovary. Curr. Biol. 10, 99–102.

    Article  PubMed  CAS  Google Scholar 

  • Herndon L. A. and Wolfner M. F. 1995 A Drosophila seminal fluid protein, Acp26Aa, stimulates egg laying in females for 1 day after mating. Proc. Natl. Acad. Sci. USA 92, 10114–10118.

    Article  PubMed  CAS  Google Scholar 

  • Holland B. and Rice W. R. 1998 Perspective: chase-away sexual selection: antagonistic seduction versus resistance. Evolution 52, 1–7.

    Article  Google Scholar 

  • Holland B. and Rice W. R. 1999 Experimental removal of sexual selection reverses intersexual antagonistic coevolution and removes a reproductive load. Proc. Natl. Acad. Sci. USA 96, 5083–5088.

    Article  PubMed  CAS  Google Scholar 

  • Imroze K. and Prasad N. G. 2011 Sex-specific effect of bacterial infection on components of adult fitness in Drosophila melanogaster. J. Evol. Biol. Res. 3, 79–86.

    Google Scholar 

  • Kalb J. M., DiBenedetto A. J. and Wolfner M. F. 1993 Probing the function of Drosophila melanogaster accessory glands by directed cell ablation. Proc. Natl. Acad. Sci. USA 90, 8093–8097.

    Article  PubMed  CAS  Google Scholar 

  • Kemp D. J. and Rutowski R. L. 2004 A survival cost to mating in a polyandrous butterfly, Colias eurytheme. Oikos 105, 65–70.

    Article  Google Scholar 

  • Kraaijeveld A. R. and Godfray H. C. 1997 Trade-off between parasitoid resistance and larval competitive ability in Drosophila melanogaster. Nature 389, 278–280.

    Article  PubMed  CAS  Google Scholar 

  • Kuijper B., Stewart A. D. and Rice W. R. 2006 The cost of mating rises non-linearly with copulation frequency in a laboratory population of Drosophila melanogaster. J. Evol. Biol. 19, 1795–1802.

    Article  PubMed  CAS  Google Scholar 

  • Lawniczak M. K., Barnes A. I., Linklater J. R., Boone J. M., Wigby S. and Chapman T. 2007 Mating and immunity in invertebrates. Trends Ecol. Evol. 22, 48–55.

    Article  PubMed  Google Scholar 

  • Lazzaro B. P., Sceurman B. K. and Clark A. G. 2004 Genetic basis of natural variation in D. melanogaster antibacterial immunity. Science 303, 1873–1876.

    Article  PubMed  CAS  Google Scholar 

  • Lazzaro B. P., Sackton T. B. and Clark A. G. 2006 Genetic variation in Drosophila melanogaster resistance to infection: a comparison across bacteria. Genetics 174, 1539–1554.

    Article  PubMed  CAS  Google Scholar 

  • Lew T. A., Morrow E. H. and Rice W. R. 2006 Standing genetic variance for female resistance to harm from males and its relationship to intra-locus sexual conflict. Evolution 60, 97–105.

    PubMed  Google Scholar 

  • Linder J. E. and Rice W. R. 2005 Natural selection and genetic variation for female resistance to harm from males. J. Evol. Biol. 18, 568–575.

    Article  PubMed  CAS  Google Scholar 

  • McKean K. A. and Nunney L. 2001 Increased sexual activity reduces male immune function in Drosophila melanogaster. Proc. Natl. Acad. Sci. USA 98, 7904–7909.

    Article  PubMed  CAS  Google Scholar 

  • McKean K. A., Yourth C. P., Lazzaro B. P. and Clark A. G. 2008 The evolutionary costs of immunological maintenance and deployment. BMC Evol. Biol. 8, 76–95.

    Article  PubMed  Google Scholar 

  • Moret Y. and Schmid-Hempel P. 2000 Survival for immunity: the price of immune system activation for bumblebee workers. Science 290, 1166–1168.

    Article  PubMed  CAS  Google Scholar 

  • Nunney L. 1990 Drosophila on oranges: colonization, competition and coexistence. Ecology 71, 1904–1915.

    Article  Google Scholar 

  • Pitnick S. 1991 Male size influences mate fecundity and remating interval in Drosophila melanogaster. Anim. Behav. 41, 735–745.

    Article  Google Scholar 

  • Pitnick S. and Garcia-Gonzalez F. 2002 Harm to females increases with male body size in Drosophila melanogaster. Proc. R. Soc. London, Ser. B 269, 1821–1828.

    Article  Google Scholar 

  • Rice W. R. 1996 Sexually antagonistic male adaptation triggered by experimental arrest of female evolution. Nature 381, 232–234.

    Article  PubMed  CAS  Google Scholar 

  • Rolff J. and Siva-Jothy M. T. 2002 Copulation corrupts immunity: a mechanism for a cost of mating in insects. Proc. Natl. Acad. Sci. USA 99, 9916–9918.

    Article  PubMed  CAS  Google Scholar 

  • Schwarzenbach G. A., Hosken D. J. and Ward P. I. 2005 Sex and immunity in the yellow dung fly Scathophaga stercoraria. J. Evol. Biol. 18, 455–463.

    Article  PubMed  CAS  Google Scholar 

  • Sheldon B. C. and Verhulst S. 1996 Ecological immunology: costly parasite defences and trade-offs in evolutionary ecology. Trends Ecol. Evol. 11, 317–321.

    Article  PubMed  CAS  Google Scholar 

  • Shoemaker K. L., Parsons N. M. and Adamo S. A. 2006 Mating enhances parasite resistance in the cricket Gryllus texensis. Anim. Behav. 71, 371–380.

    Article  Google Scholar 

  • Short S. M. and Lazzaro B. P. 2010 Female and male genetic contributions to post-mating immune defence in female Drosophila melanogaster. Proc. Biol. Sci. 277, 3649–3657.

    Article  PubMed  Google Scholar 

  • Siva-Jothy M. T., Tsubaki Y. and Hooper R. E. 1998 Decreased immune response as a proximate cost of copulation and oviposition in a damselfly. Physiol. Entomol. 23, 274–277.

    Article  Google Scholar 

  • Swanson W. J., Clark A. G., Waldrip-Dail H. M., Wolfner M. F. and Aquadro C. F. 2001 Evolutionary EST analysis identifies rapidly evolving male reproductive proteins in Drosophila. Proc. Natl. Acad. Sci. USA 98, 7375–7379.

    Article  PubMed  CAS  Google Scholar 

  • Thomas R. H. 1993 Ecology of body size in Drosophila buzzatii: untangling the effects of temperature and nutrition. Ecol. Entomol. 18, 84–90.

    Article  Google Scholar 

  • Wigby S. and Chapman T. 2004 Female resistance to male harm evolves in response to manipulation of sexual conflict. Evolution 58, 1028–1037.

    PubMed  Google Scholar 

  • Wigby S. and Chapman T. 2005 Sex peptide causes mating costs in female Drosophila melanogaster. Curr. Biol. 15, 316–321.

    Article  PubMed  CAS  Google Scholar 

  • Wilkinson G. 1987 Equilibrium analysis of sexual selection in Drosophila melanogaster. Evolution 41, 11–21.

    Article  Google Scholar 

  • Yanagi S. and Miyatake T. 2003 Costs of mating and egg production in female Callosobruchus chinensis. J. Insect. Physiol. 49, 823–827.

    Article  PubMed  CAS  Google Scholar 

  • Ye Y. H., Chenoweth S. F. and McGraw E. A. 2009 Effective but costly, evolved mechanisms of defense against a virulent opportunistic pathogen in Drosophila melanogaster. PLoS Pathog. 5, e1000385.

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Indian Institute of Science Education and Research, BCVK Campus, Mohanpur, 741 252, India

    K. IMROZE

  2. Indian Institute of Science Education and Research, Mohali, Knowledge City, Sector 81, SAS Nagar, Manauli PO 140306, India

    K. IMROZE & N. G. PRASAD

Authors
  1. K. IMROZE
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. N. G. PRASAD
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to N. G. PRASAD.

Additional information

Imroze K. and Prasad N. G. 2011 Mating with large males decreases the immune defence of females in Drosophila melanogaster. J. Genet. 90, xx–xx

Rights and permissions

Reprints and permissions

About this article

Cite this article

IMROZE, K., PRASAD, N.G. Mating with large males decreases the immune defence of females in Drosophila melanogaster . J Genet 90, 427–434 (2011). https://doi.org/10.1007/s12041-011-0105-7

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12041-011-0105-7

Keywords

Search

Navigation