Skip to main content
SpringerLink
Log in

Mating flights select for symmetry in honeybee drones (Apis mellifera)

  • SHORT COMMUNICATION
  • Published:
Naturwissenschaften Aims and scope Submit manuscript

Abstract

Males of the honeybee (Apis mellifera) fly to specific drone congregation areas (DCAs), which virgin queens visit in order to mate. From the thousands of drones that are reared in a single colony, only very few succeed in copulating with a queen, and therefore, a strong selection is expected to act on adult drones during their mating flights. In consequence, the gathering of drones at DCAs may serve as an indirect mate selection mechanism, assuring that queens only mate with those individuals having a better flight ability and a higher responsiveness to the queen’s visual and chemical cues. Here, we tested this idea relying on wing fluctuating asymmetry (FA) as a measure of phenotypic quality. By recapturing marked drones at a natural DCA and comparing their size and FA with a control sample of drones collected at their maternal hives, we were able to detect any selection on wing size and wing FA occurring during the mating flights. Although we found no solid evidence for selection on wing size, wing FA was found to be significantly lower in the drones collected at the DCA than in those collected at the hives. Our results demonstrate the action of selection during drone mating flights for the first time, showing that developmental stability can influence the mating ability of honeybee drones. We therefore conclude that selection during honeybee drone mating flights may confer some fitness advantages to the queens.

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

References

  • Abramoff MD, Magelhaes PJ, Ram SJ (2004) Image Processing with Image. J Biophotonics International 11:36–42. ImageJ is available from: http://rsb.info.nih.gov/ij/

  • Andersson M, Simmons LW (2006) Sexual selection and mate choice. Trends Ecol Evol 21:296–302

    Article  PubMed  Google Scholar 

  • Baer B (2005) Sexual selection in Apis bees. Apidologie 36:187–200

    Article  Google Scholar 

  • Berg S, Koeniger N, Koeniger G, Fuchs S (1997) Body size and reproductive success of drones (Apis mellifera L). Apidologie 28:449–460

    Article  Google Scholar 

  • Bishop GH (1920) Fertilization in the honey-bee I. The male sexual organs: their histological structure and physiological functioning. J Exp Zool 31:225–265

    Google Scholar 

  • Boomsma JJ, Ratnieks FLW (1996) Paternity in eusocial hymenoptera. Philos T Roy Soc B 351:947–975

    Article  Google Scholar 

  • Boomsma JJ, Baer B, Heinze J (2005) The evolution of male traits in social insects. Annu Rev Entomol 50:395–420

    Article  CAS  PubMed  Google Scholar 

  • Brückner D (1976) The influence of genetic variability on wing asymmetry in honeybees (Apis mellifera). Evolution 30:100–108

    Article  Google Scholar 

  • Clarke GM, Oldroyd BP (1996) The genetic basis of developmental stability in Apis mellifera II. Relationships between character size, asymmetry and single-locus heterozygosity. Genetica 97:211–224

    Article  CAS  Google Scholar 

  • Clarke GM, Oldroyd BP, Hunt P (1992) The genetic basis of developmental stability in Apis mellifera: heterozygosity versus genic balance. Evolution 46:753–762

    Article  Google Scholar 

  • Collins AM, Caperna TJ, Williams V, Garrett WM, Evans JD (2006) Proteomic analyses of male contributions to honey bee sperm storage and mating. Insect Mol Biol 15:541–549

    Article  CAS  PubMed  Google Scholar 

  • De Block M, Stocks R (2007) Flight-related body morphology shapes mating success in a damselfly. Anim Behav 74:1093–1098

    Article  Google Scholar 

  • De Miranda J, Fries I (2008) Venereal and vertical transmission of deformed wing virus in honeybees (Apis mellifera L.). J Invertebr Pathol 98:184–189

    Article  PubMed  Google Scholar 

  • Duay P, De Jong D, Engels W (2002) Decreased flight performance and sperm production in drones of the honey bee (Apis mellifera) slightly infested by Varroa destructor mites during pupal development. Genet Mol Res 1:227–232

    PubMed  Google Scholar 

  • Gary NE (1992) Activities and behavior of honey bees. In: Graham JM (ed) The hive and the honey bee. Dadant & Sons Inc., Hamilton, pp 269–372

    Google Scholar 

  • Hepburn HR, Radloff SE, Fuchs S (1999) Flight machinery dimensions of honeybees, Apis mellifera. J Comp Physiol B 169:107–112

    Article  Google Scholar 

  • Herbert EW Jr (1992) Honey bee nutrition. In: Graham JM (ed) The hive and the honey bee. Dadant & Sons Inc, Hamilton, pp 197–233

    Google Scholar 

  • Koeniger N, Koeniger G (2000) Reproductive isolation among species of the genus Apis. Apidologie 31:313–339

    Article  Google Scholar 

  • Koeniger N, Koeniger G (2007) Mating flight duration of Apis mellifera queens: as short as possible, as long as necessary. Apidologie 38:606–611

    Article  Google Scholar 

  • Koeniger N, Koeniger G, Gries M, Tingek S (2005a) Drone competition at drone congregation areas in four Apis species. Apidologie 36:211–221

    Article  Google Scholar 

  • Koeniger N, Koeniger G, Pechhacker H (2005b) The nearer the better? Drones (Apis mellifera) prefer nearer drone congregation areas. Insect Soc 52:31–35

    Article  Google Scholar 

  • Lens L, Van Dongen S, Kark S, Matthysen E (2002) Fluctuating asymmetry as an indicator of fitness: can we bridge the gap between studies? Biol Rev Camb Philos Soc 77:27–38

    PubMed  Google Scholar 

  • Loper GM, Wolf WW, Taylor OR (1988) The use of radar to document honey-bee (Apis mellifera) drone flight behavior. In: Needham GR, Page RE Jr, Delfinado-Baker M, Bowman CE (eds) Africanized bees and bee mites. Ellis Horwood, Chichester, pp 193–198

    Google Scholar 

  • Markow TA, Ricker JP (1992) Male size, developmental stability, and mating success in natural populations of three Drosophila species. Heredity 69:122–127

    Article  PubMed  Google Scholar 

  • Møller AP (1991) Sexual ornament size and the cost of fluctuating asymmetry. P Roy Soc Lond B Biol 243:59–62

    Article  Google Scholar 

  • Møller AP, Swaddle JP (1997) Developmental stability and evolution. Oxford University Press, Oxford

    Google Scholar 

  • Moritz RFA (1981) Der Einfluss der Inzucht auf die fitness der Drohnen von Apis mellifera carnica. Apidologie 12:41–55

    Article  Google Scholar 

  • Page RE Jr, Erickson EH Jr (1988) Reproduction by worker honey bees (Apis mellifera L.). Behav Ecol Sociobiol 23:117–126

    Article  Google Scholar 

  • Page RE Jr, Metcalf RA (1984) A population investment sex ratio for the honey bee (Apis mellifera L.). Am Nat 124:680–702

    Article  Google Scholar 

  • Palmer RA, Strobeck C (1986) Fluctuating assymetry: measurement, analysis, patterns. Ann Rev Ecol Syst 17:391–421

    Article  Google Scholar 

  • Polak M (1993) Parasites increase fluctuating asymmetry of male Drosophila nigrospiracula: implications for sexual selection. Genetica 89:255–265

    Article  Google Scholar 

  • Polak M (2003) Developmental instability: causes and consequences. Oxford University Press, New York

    Google Scholar 

  • Ruttner F (1988) Biogeography and taxonomy of honeybees. Springer Verlag, Berlin

    Google Scholar 

  • Schlüns H, Schlüns EA, van Praagh J, Moritz RFA (2003) Sperm numbers in drone honeybees (Apis mellifera) depend on body size. Apidologie 34:577–584

    Article  Google Scholar 

  • Schneider SS, Leamy LJ, Lewis LA, DeGrandi-Hoffman G (2003) The influence of hybridization between African and European honeybees, Apis mellifera, on asymmetries in wing size and shape. Evolution 57:2350–2364

    CAS  PubMed  Google Scholar 

  • Schoeters E, Billen J (2000) The importance of the spermathecal duct in bumblebees. J Insect Physiol 46:1303–1312

    Article  CAS  PubMed  Google Scholar 

  • Shaibi T, Lattorff HMG, Moritz RFA (2008) A microsatellite DNA toolkit for studying population structure in Apis mellifera. Mol Ecol Res 8:1034–1036

    Article  CAS  Google Scholar 

  • Shimanuki H, Knox DA, Furgala B, Caron DM, Williams JL (1992) Diseases and pests of honey bees. In: Graham JM (ed) The hive and the honey bee. Dadant & Sons Inc., Hamilton, pp 1083–1151

    Google Scholar 

  • Simmons LW (2001) Sperm competition and its evolutionary consequences in the insects. Princeton University Press, Princeton

    Google Scholar 

  • Smith DR, Crespi BJ, Bookstein FL (1997) Fluctuating asymmetry in the honey bee, Apis mellifera: effects of ploidy and hybridization. J Evol Biol 10:551–574

    Article  Google Scholar 

  • Snodgrass RE, Erickson EH (1992) The anatomy of the honey bee. In: Graham JM (ed) The Hive and the Honey Bee. Dadant & Sons Inc., Hamilton, pp 103–169

    Google Scholar 

  • Thomas ALR (1993) The aerodynamic costs of asymmetry in the wings and tail of birds: asymmetric can’t fly round tight corners. Proc Roy Soc Lond B Biol 254:181–189

    Article  Google Scholar 

  • Thornhill R, Alcock J (2001) The evolution of insect mating systems. ¡Universe.com Inc, Lincoln

    Google Scholar 

  • Walsh PS, Metzgar DA, Higuchi R (1991) Chelex-100 as a medium for simple extraction of DNA for PCR-based typing from forensic material. Biotechniques 10:506–513

    CAS  PubMed  Google Scholar 

  • Williams JL (1987) Wind-directed pheromone trap for drone honey bees (Hymenoptera: Apidae). J Econ Entomol 80:532–536

    Google Scholar 

  • Wilson EO (1971) The insect societies. Belknap/Harvard University Press, Cambridge, Massachusetts

    Google Scholar 

  • Winston ML (1987) The biology of the honey bee. Harvard University Press, Cambridge

    Google Scholar 

  • Woyke J (1983) Dynamics of entry of spermatozoa into the spermatheca of instrumentally inseminated queen honeybees. J Apicult Res 22:150–154

    Google Scholar 

Download references

Acknowledgments

We thank Marie Nitzschner and Stefanie Finger for helping to mark, collect, and dissect the drones; Antje Jarosch for support during the genotyping; Petra Leibe for assistance in the laboratory; and Michael Lattorff for providing guidance during the morphological analyses and improving earlier versions of this manuscript. We are also grateful to Stan Schneider and two anonymous referees for their helpful suggestions and constructive critiques. This project was funded by the BEESHOP European network (FOOD-CT-2006-022568).

Author information

Author notes

  1. Rodolfo Jaffé

    Present address: Centre for Evolutionary Biology, School of Animal Biology (M092), The University of Western Australia, 35 Stirling Highway, Crawley, WA, 6009, Australia

Authors and Affiliations

  1. Molecular Ecology, Institute of Biology, Martin Luther University Halle-Wittenberg, Hoher Weg 4, 06120, Halle (Saale), Germany

    Rodolfo Jaffé & Robin F. A. Moritz

  2. ARC Centre of Excellence in Plant Energy Biology, Molecular and Chemical Sciences Building, The University of Western Australia, 35 Stirling Highway, Crawley, WA, 6009, Australia

    Rodolfo Jaffé

Authors
  1. Rodolfo Jaffé
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Robin F. A. Moritz
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Rodolfo Jaffé.

Electronic supplementary material

The following files are available as supplementary material:

S1

Map showing the location of the study hives and the drone congregation area in Halle, Germany (courtesy of Google Earth V4.3.7). (DOC 571 kb)

S2

Table showing the haplotype assignments and consensus reconstruction of the sibships of 144 marked Apis mellifera drones recaptured at their maternal hives and at a nearby drone congregation area. (XLS 69 kb)

S3

Figure showing the 14 morphological characters measured in the forewings of Apis mellifera drones. Distances (D) are shown in red, while angles (A) are shown in yellow. (DOC 256 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Jaffé, R., Moritz, R.F.A. Mating flights select for symmetry in honeybee drones (Apis mellifera). Naturwissenschaften 97, 337–343 (2010). https://doi.org/10.1007/s00114-009-0638-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00114-009-0638-2

Keywords

Search

Navigation