Advertisement

Apidologie

pp 1–17 | Cite as

Sperm competition in honey bees (Apis mellifera L.): the role of body size dimorphism in drones

  • H. Vasfi GençerEmail author
  • Yasin Kahya
Original article
  • 214 Downloads

Abstract

Previous experimental studies demonstrated that small drones (SD) had lower paternity share since they were not successful in mating with queens as large drones (LD) in the mating arena. However, it remains unclear whether spermatozoa of SD can compete in vivo with those of LD if SD have mating opportunity. We, therefore, tested the spermatozoal competitiveness of SD against LD by instrumentally inseminating the queens with varying proportions of semen from LD and SD. Sister queens from a Buckfast colony and LD and SD from 15 Caucasian colonies were reared synchronously as experimental test individuals. The virgin sister queens were randomly allocated into three semen composition groups. The queens in groups A, B and C were inseminated with an equal volume of semen (7.2 μl) collected successively from 6 LD and 6 SD (50%:50% treatment), 3 LD and 9 SD (25%:75% treatment), and 9 LD and 3 SD (75%:25% treatment), respectively. Once oviposition starts in mating nucs, the queens were introduced into field colonies to proceed to lay eggs. After 3 months, about 100 newly emerged worker daughters from each queen were individually collected from the colonies for paternity assignment. Five polymorphic microsatellite loci (A024, A079, A43, A113, and Ap226) were analysed in 144 drones that were used to inseminate 12 experimental queens and 908 offspring workers. The observed patriline frequencies of LD and SD were 67.0% and 33.0% in group A, 34.6% and 65.4% in group B, and 79.8% and 20.2% in group C, respectively. The patriline frequencies within each colony were noticeably skewed. LD that were reared in QRC sired more offspring, whereas SD that were reared in LWC had lower paternity shares. When all three semen composition groups were pooled, the overall observed patriline frequency of SD (40%) was found to be 10% less than the overall expected patriline frequency (50%). The results demonstrated that SD remained a little behind LD in sperm competition.

Keywords

polyandry sperm competition patriline frequency drone size dimorphism 

Notes

Acknowledgements

We thank Ali Ergül for his guidence in microsatellite DNA analysis, and Ensar Başpınar for his help on statistical analysis.

Authors’ Contribution

HVG conceived this research and designed experiments; YK participated in the design and interpretation of the data; HVG and YK performed experiments and analyses; HVG wrote the paper. Both authors read and approved the final manuscript.

Funding information

This study was financially supported by the fund (TOVAG-108O447) from the Scientific and Technological Research Council of Turkey (TUBITAK) to HVG.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Baer, B. (2005) Sexual selection in Apis bees. Apidologie 36, 187–200CrossRefGoogle Scholar
  2. Baer, B., Collins, J., Maalaps, K., den Boer, S. P. A. (2016) Sperm use economy of honeybee (Apis mellifera) queens. Ecol. Evol. 6, 2877–2885PubMedPubMedCentralCrossRefGoogle Scholar
  3. Baudry, E., Solignac, M., Garnery, L., Gries, M., Cornuet, J.-M., Koeniger, N. (1998) Relatedness among honeybees (Apis mellifera) of a drone congregation. Proc. R. Soc. Lond. B 265, 2009–2014CrossRefGoogle Scholar
  4. Berg, S. (1991) Investigation on the rates of large and small drones at a drone congregation area. Apidologie 22, 437–438Google Scholar
  5. Berg, S., Koeniger, N., Koeniger, G., Fuchs, S. (1997) Body size and reproductive success of drones (Apis mellifera L). Apidologie 28, 449–460CrossRefGoogle Scholar
  6. Boes, K. E. (2010) Honeybee colony drone production and maintenance in accordance with environmental factors: an interplay of queen and worker decisions. Insectes Soc. 57, 1–9.CrossRefGoogle Scholar
  7. Boomsma, J. J., Ratnieks, F. L. W. (1996) Paternity in eusocial Hymenoptera. Phil. Trans. R. Soc. Lond. B 351, 947–975CrossRefGoogle Scholar
  8. Boomsma, J. J., Baer, B., Heinze, J. (2005) The evolution of male traits in social insects. Annu. Rev. Entomol. 50, 395–420PubMedCrossRefGoogle Scholar
  9. Brodschneider, R., Arnold, G., Hrassnigg, N., Crailsheim, K. (2012) Does patriline composition change over a honey bee queen’s lifetime? Insects 3, 857–869PubMedPubMedCentralCrossRefGoogle Scholar
  10. Coelho, J. R. (1996) The flight characteristics of drones in relation to mating. Bee Sci. 4, 21–25Google Scholar
  11. Collins, A. M. (2000) Relationship between semen quality and performance of instrumentally inseminated honey bee queens. Apidologie 31, 421–429CrossRefGoogle Scholar
  12. Couvillon, M. J., Hughes, W. O. H., Perez-Sato J. A., Martin, S. J., Roy, G. G. F., Ratnieks, F. L. W. (2010) Sexual selection in honey bees: colony variation and the importance of size in male mating success. Behav. Ecol. 21, 520–525CrossRefGoogle Scholar
  13. Czekońska, K., Szentgyörgyi, H., Tofilski, A. (2019) Body mass but not wing size or symmetry correlates with life span of honey bee drones. B. Entomol. Res. 109, 383–389PubMedCrossRefPubMedCentralGoogle Scholar
  14. DeGrandi-Hoffman, G., Tarpy, D. R., Schneider, S. S. (2003) Patriline compositions of worker populations in honey bee (Apis mellifera) colonies headed by queens inseminated with semen from African and European drones. Apidologie 34, 111–120CrossRefGoogle Scholar
  15. Estoup, A., Garnery, L., Solignac, M., Cornuet, J.-M. (1995) Microsatellite variation in honey bee (Apis mellifera L.) populations: Hierarchical genetic structure and test of the infinite allele and stepwise mutation models. Genetics 140, 679–695PubMedPubMedCentralGoogle Scholar
  16. Franck, P., Coussy, H., Le Conte, Y., Solignac, M., Garnery, L., Cornuet, J.-M. (1999) Microsatellite analysis of sperm admixture in honeybee. Insect Mol. Biol. 8, 419–421PubMedCrossRefPubMedCentralGoogle Scholar
  17. Franck, P., Solignac, M., Vautrin, D., Cornuet, J.-M., Koeniger, G., Koeniger, N. (2002) Sperm competition and last-male precedence in the honeybee. Anim. Behav. 64, 503–509CrossRefGoogle Scholar
  18. García-González, F., Simmons L W (2005) Sperm viability matters in insect sperm competition. Curr. Biol. 15, 271–275.PubMedCrossRefPubMedCentralGoogle Scholar
  19. Gençer H. V., Firatli, Ç. (2005) Reproductive and morphological comparisons of drones reared in queenright and laying worker colonies. J. Apic. Res. 44, 163–167CrossRefGoogle Scholar
  20. Gençer, H. V., Kahya, Y. (2011) Are sperm traits of drones (Apis mellifera L.) from laying worker colonies noteworthy? J. Apic. Res. 50, 130–137CrossRefGoogle Scholar
  21. Gençer, H. V., Kahya, Y., Woyke, J. (2014) Why the viability of spermatozoa diminishes in the honeybee (Apis mellifera) within short time during natural mating and preparation for instrumental insemination. Apidologie 45, 757–770CrossRefGoogle Scholar
  22. Gessner B., Ruttner F., (1977) Transfer der Spermatozoen in die Spermatheka der Bienenkonigin, Apidologie 8, 1–18CrossRefGoogle Scholar
  23. Gloag, R. S., Christie J. R., Ding, G., Stephens, R. E., Buchmann, G., Oldroyd, B. P. (2019) Workers’ sons rescue genetic diversity at the sex locus in an invasive honey bee population. Mol. Ecol. 28, 1585–1592PubMedCrossRefPubMedCentralGoogle Scholar
  24. Goins, A., Schneider, S. S. (2013) Drone “quality” and caste interactions in the honey bee, Apis mellifera L. Insect. Soc. 60, 453–461CrossRefGoogle Scholar
  25. Haberl, M., Tautz, D. (1998) Sperm usage in honey bees. Behav. Ecol. Sociobiol. 42, 247–255CrossRefGoogle Scholar
  26. Hall, H. G. (1986) DNA differences found between Africanized and European honeybees. Proc. Natl. Acad. Sci. USA 83, 4874–4877PubMedCrossRefPubMedCentralGoogle Scholar
  27. Harbo, J. R. (1988) Sperm competition. Am. Bee J. 128, 803–804Google Scholar
  28. Harbo, J. R. (1990) Artificial mixing of honey bee spermatozoa from honeybees and evidence for sperm competition. J. Apic. Res. 29, 151–158CrossRefGoogle Scholar
  29. Harbo, J. R. (1991) Laying workers produce a drone population that genetically represent their colony. Am. Bee J. 131, 776–777Google Scholar
  30. Hayashi, M, Nakamura, J., Sasaki, K, Harano, K. I. (2016) Honeybee males use highly concentrated nectar as fuel for mating flights. J. Insect Physiol. 93–94, 50–55PubMedCrossRefPubMedCentralGoogle Scholar
  31. Hemmling C. (1991) Production and sexual maturity of drones in queenless colonies. Apidologie 22, 435–436Google Scholar
  32. Herrmann, M., Trenzcek, T., Fahrenhorst, H., Engels, W. (2005) Characters that differ between diploid and haploid honey bee (Apis mellifera) drones. Genet. Mol. Res. 4, 624–641PubMedPubMedCentralGoogle Scholar
  33. Holmes, M. J., Allsopp, M. H., Noach-Pienaar, L.-A., Wossler, T. C., Oldroyd, B. P., Beekman, M. (2011) Sperm utilization in honeybees (Apis mellifera scutellata and Apis mellifera capensis) in South Africa. Apidologie 42, 23–28CrossRefGoogle Scholar
  34. Hunter, F. M., Birkhead, T. R. (2002) Sperm viability and sperm competition in insects. Curr. Biol. 12, 121–123PubMedCrossRefPubMedCentralGoogle Scholar
  35. Jaffé, R., Moritz, R. F. A. (2010) Mating flights select for symmetry in honeybee drones (Apis mellifera). Naturwissenschaften 97, 337–343PubMedCrossRefPubMedCentralGoogle Scholar
  36. Jarolimek, J., Otis, G. W. (2001) A comparison of fitness components in large and small honey-bee drones. Am. Bee J. 141, 891–892Google Scholar
  37. Kalinowski, S. T., Taper, M. L., Marshall, T. C. (2007) Revising how the computer program CERVUS accommodates genotyping error increases success in paternity assignment. Mol. Ecol. 16, 1099–1006PubMedCrossRefGoogle Scholar
  38. Koeniger, N., Koeniger, G. (1991) An evolutionary approach to mating behavior and drone copulatory organs in Apis. Apidologie 22, 581–590CrossRefGoogle Scholar
  39. Koeniger, G., Koeniger, N., Fabritius, M. (1979) Some detailed observations of mating in the honey bee. Bee World 60, 53–57CrossRefGoogle Scholar
  40. Koeniger, N., Koeniger, G., Pechhacker, H. (1992) Utilisation of sperm in naturally mated honey bee queens (Apis mellifera carnica). Apidologie 23, 349–351Google Scholar
  41. Koeniger, N., Koeniger, G., Gries, M., Tingek, S. (2005) Drone competition at drone congregation areas in four Apis species. Apidologie 36, 211–221CrossRefGoogle Scholar
  42. Koffler, S., Meneses, H. M., Kleinert, A. M., Jaffé, R (2016) Competitive males have higher quality sperm in a monogamous social bee. BMC Evol. Biol. 16, 195Google Scholar
  43. Kraus, F. B., Neumann, P., Scharpenberg, H., Van Praagh, J., Morıtz, R. F. A. (2003) Male fitness of honeybee colonies (Apis mellifera L.). J. Evol. Biol. 16, 914–920.PubMedCrossRefPubMedCentralGoogle Scholar
  44. Laidlaw, H. H. Jr. (1944) Artificial insemination of the queen bee (Apis mellifera L): Morphological basis and results. J. Morphol. 74, 429–465CrossRefGoogle Scholar
  45. Laidlaw, H. H. Jr., Page, R. E. Jr. (1984) Polyandry in honey bees (Apis mellifera L.): sperm utilization and intracolony genetic relationship. Genetics 108, 985–997PubMedPubMedCentralGoogle Scholar
  46. Laidlaw, H. H. Jr., Page, R. E. Jr. (1997) Queen Rearing and Bee Breeding. Wicwas Press, Cheshire, ConnecticutGoogle Scholar
  47. McAneney-Lannen, G. E. (2004) Honeybee (Apis mellifera L.) drone size and its effects on aspects of male fitness. A Thesis Presented to the Faculty of Graduate Studies of the University of Guelph for the Degree of Master of Science; Guelph, CanadaGoogle Scholar
  48. Miller, C. W., Svensson, E. I. (2014) Sexual selection in complex environments. Annu. Rev. Entomol. 59, 427–445PubMedCrossRefGoogle Scholar
  49. Moritz, R. F. A. (1981) Der Einfluss der Inzucht auf die Fitness der Drohnen von Apis mellifera carnica. Apidologie 12, 41–55CrossRefGoogle Scholar
  50. Moritz, R. F. A. (1986) Intracolonial worker relationship and sperm competition in the honeybee (Apis mellifera L.). Experientia 40, 182–184Google Scholar
  51. Page, R. E. Jr. (1986) Sperm utilization in social insects. Annu. Rev. Entomol. 31, 297–320CrossRefGoogle Scholar
  52. Page, R. E. Jr. (2013) The Spirit of the Hive - The Mechanisms of Social Evolution. Harvard University Press, London, EnglandGoogle Scholar
  53. Page, R. E. Jr., Erickson, E. H. Jr. (1988) Reproduction by worker honeybees (Apis mellifera L.). Behav. Ecol. Sociobiol. 23, 117–126CrossRefGoogle Scholar
  54. Page, R. E. Jr., Metcalf, R. A. (1982) Multiple mating, sperm utilization, and social evolution. Am. Nat. 119, 263–281CrossRefGoogle Scholar
  55. Page, R. E. Jr., Metcalf, R. A. (1984) A population investment sex ratio for the honey bee (Apis mellifera L.). Am. Nat. 124, 680–702Google Scholar
  56. Page, R. E. Jr., Kimsey, R. B., Laidlaw, H. H. Jr. (1984) Migration and dispersal of spermatozoa in spermathecae of queen honeybees (Apis mellifera L.). Experientia 40, 182–184CrossRefGoogle Scholar
  57. Palmer, K. A., Oldroyd, B. P. (2000) Evolution of multiple mating in the genus Apis. Apidologie 31, 235–242CrossRefGoogle Scholar
  58. Parker, G. A. (1970) Sperm competition and its evolutionary consequences in the insects. Biol. Rev. 45, 525–567CrossRefGoogle Scholar
  59. Peer, D. F. (1956) Multiple mating of queen honey bees. J. Econ. Entomol. 49, 741–743CrossRefGoogle Scholar
  60. Ratnieks, F. L. W. (2002) Conflict in the bee hive: worker reproduction and worker policing. The Beekeepers Quarterly 70, 16–17Google Scholar
  61. Ratnieks, F. L. W., Visscher, P. K. (1989) Worker policing in honeybees. Nature 342, 796–797CrossRefGoogle Scholar
  62. Rinderer, T. E., Collins, A. M., Pesante, D. (1985) A comparison of Africanized and European drones: weights, mucus gland and seminal vesicle weights, and counts of spermatozoa. Apidologie 16, 407–412CrossRefGoogle Scholar
  63. Ruttner, F. (1956) The mating of the honeybee. Bee World 37, 3–15CrossRefGoogle Scholar
  64. Ruttner, F., Koeniger, G. (1971) Die Füllung der Spermatheca der Bienenkönigin. Aktive Wandering oder Passiver Transport der Spermatozoen? Z. Vergl. Physiolgie 72, 411–422Google Scholar
  65. Sasaki, K., Satoh, T., Obara, Y. (1995) Sperm utilization by honey bee queens; DNA fingerprinting analysis. Appl. Entomol. Zool. 30, 335–341CrossRefGoogle Scholar
  66. Schlüns, H., Schlüns, E. A., Van Praagh, J., Moritz, R. F. A. (2003) Sperm numbers in drone honeybees (Apis mellifera) depend on body size. Apidologie 34, 577–584CrossRefGoogle Scholar
  67. Schlüns, H., Koeniger, G., Koeniger, N., Moritz, R. F. A. (2004) Sperm utilization pattern in the honeybee (Apis mellifera). Behav. Ecol. Sociobiol. 56, 458–463CrossRefGoogle Scholar
  68. Shafir, S., Kabanoff, L., Duncan, M., Oldroyd, B. P. (2009) Honey bee (Apis mellifera) sperm competition in vitro – two are no less viable than one. Apidologie 40, 556–561CrossRefGoogle Scholar
  69. Shuster, S. M., Wade, M. J. (2003) Mating Systems and Strategies. Princeton University Press, USAGoogle Scholar
  70. Slone, J. D., Stout, T. L., Huang, Z. Y., Schneider, S. S. (2012) The influence of drone physical condition on the likelihood of receiving vibration signals from worker honey bees, Apis mellifera. Insect. Soc. 59, 101–107CrossRefGoogle Scholar
  71. Solignac, M., Vautrin D., Loiseau, A., Mougel, F., Baudry, E. Estoup, A., Garnery, L., Haberl, M., Cornuet, J.-M. (2003) Five hundred and fifty microsatellite markers for the study of the honeybee (Apis mellifera L.) genome. Mol. Ecol. Notes 3, 307–313Google Scholar
  72. Strassmann, J. (2001) The rarity of multiple mating by females in the social Hymenoptera. Insect. Soc. 48, 1–13CrossRefGoogle Scholar
  73. Streinzer, M., Spaethe, J. (2015) A scientific note on peripheral compound eye morphology of small and normal-sized honey bee drones. J. Apic. Res. 54, 59–61CrossRefGoogle Scholar
  74. Sundin, J. (2009) The evolution of animal mating systems. Introductory Research Essay No. 96 (ISSN 1404 – 4919), Uppsala, SwedenGoogle Scholar
  75. Taber, S. (1954) The frequency of multiple mating of queen honey bees. J. Econ. Entomol. 47, 995–998CrossRefGoogle Scholar
  76. Tofilski, A., Chuda-Mickiewicz, B., Czekońska, K., Chorbiński, P. (2012) Flow cytometry evidence about sperm competition in honey bee (Apis mellifera). Apidologie 43, 63–70CrossRefGoogle Scholar
  77. Visscher, P. K. (1989) A quantitative study of worker reproduction in honey bee colonies. Behav. Ecol. Sociobiol. 25, 247–254CrossRefGoogle Scholar
  78. Wang, J., (2004) Sibship reconstruction from genetic data with typing errors. Genetics 166, 1963–1979PubMedPubMedCentralCrossRefGoogle Scholar
  79. Woyciechowski, M., Król, E. (1996) On intraoviductal sperm competition in the honeybee (Apis mellifera). Folia Biol.-Kraków 44, 1–2Google Scholar
  80. Woyke, J. (1956) Anatomo-physiological changes in queen bees returning from mating flights, and the process of multiple mating. Bull. Acad. Polon. Sci. 4, 81–87Google Scholar
  81. Woyke, J. (1962) Natural and artificial insemination of queen honeybees. Bee World 43, 21–25CrossRefGoogle Scholar
  82. Woyke, J. (1964) Causes of repeated mating flights by queen honeybees. J. Apic. Res. 3, 17–23CrossRefGoogle Scholar
  83. Woyke, J. (1983) Dynamics of entry of spermatozoa into the spermatheca of instrumentally inseminated queen honeybees. J. Apic. Res. 22, 150–154CrossRefGoogle Scholar
  84. Woyke, J. (2008) Why the eversion of endophallus of honey bee drone stops at the partly everted stage and significance of this. Apidologie 39, 627–636CrossRefGoogle Scholar
  85. Zaitoun, S., Al-Ghzawi, A., Kridli, R. (2009) Monthly changes in various drone characteristics of Apis mellifera ligustica and Apis mellifera syriaca. Entomol. Sci. 12, 208–214CrossRefGoogle Scholar

Copyright information

© INRA, DIB and Springer-Verlag France SAS, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of Animal Science, Faculty of AgricultureAnkara UniversityAnkaraTurkey

Personalised recommendations