Insectes Sociaux

, Volume 58, Issue 1, pp 47–55 | Cite as

Variation in male body size and reproductive allocation in the leafcutter ant Atta colombica: estimating variance components and possible trade-offs

  • M. Stürup
  • S. P. A. den Boer
  • D. R. Nash
  • J. J. Boomsma
  • B. Baer
Research Article

Abstract

Remarkably little is known about the traits that determine reproductive success of males in eusocial insects. Their window for mate choice decisions is very short, the actual mating process is very difficult to observe, and their small body sizes have likely prevented systematic studies in many species. In 2008 and 2009, we revisited a Panamanian population of Atta colombica leafcutter ants to partially repeat and complement a study of more than 15 years ago. We compared within- and between-colony variation in male body size (mass and width of head, mesosoma and gaster) and sperm characteristics (length, number and survival after exposure to saline buffer with and without added accessory gland secretion). We also measured the size of accessory glands as the main contributor of seminal fluid and the accessory testes containing all mature sperm, but we found few correlations between these variables. We also obtained little or no evidence for expected trade-offs between sperm number and sperm length and between mesosoma mass and sperm complement, although this could be due to limited sample size and unknown variation in larval resource allocation that was beyond our control. However, we found an interestingly bimodal distribution in broad-sense heritabilities (intra-class correlations) among the variables that we measured. Low heritabilities suggest that mesosoma size (mass and width), accessory testes size, sperm viability (measured as % survival in saline) and probably also accessory gland size are traits directly correlated with reproductive success. However, the much higher heritabilities for total body mass, gaster mass, head width, sperm length and sperm number suggest that these traits are less likely to make direct contributions to male fitness.

Keywords

Sperm number Accessory gland size Sperm length Sperm viability Fungus growing ants 

References

  1. Baer B. 2003. Bumblebees as model organisms to study male sexual selection in social insects. Behav. Ecol. Sociobiol. 54: 521-533Google Scholar
  2. Baer B. 2005. Sexual selection in Apis bees. Apidologie 36: 187-200Google Scholar
  3. Baer B. 2010. The copulation biology of ants (Hymenoptera: Formicidae). Myrmecol. News 14: 55-68Google Scholar
  4. Baer B., Armitage S.A.O. and Boomsma J.J. 2006. Sperm storage induces an immunity cost in ants. Nature 441: 872-875Google Scholar
  5. Baer B. and Boomsma J.J. 2004. Male reproductive investment and queen mating-frequency in fungus-growing ants. Behav. Ecol. 15: 426-432Google Scholar
  6. Baer B., de Jong G., Schmid-Hempel R., Schmid-Hempel P., Hoeg J.T. and Boomsma J.J. 2006. Heritability of sperm length in the bumblebee Bombus terrestris. Genetica 127: 11-23Google Scholar
  7. Baer B., Dijkstra M.B., Mueller U.G., Nash D.R. and Boomsma J.J. 2009. Sperm length evolution in the fungus-growing ants. Behav. Ecol. 20: 38-45Google Scholar
  8. Birkhead T.R., Fletcher F., Pellatt E.J. and Staples A. 1995. Ejaculate quality and the success of extra-pair copulations in the zebra finch. Nature 377: 422-423Google Scholar
  9. Boomsma J.J., Baer B. and Heinze J. 2005. The evolution of male traits in social insects. Annu. Rev. Entomol. 50: 395-420Google Scholar
  10. Chown S.L. and Gaston K.J. 2010. Body size variation in insects: a macroecological perspective. Biol. Rev. 85: 139-169Google Scholar
  11. Couvillon M.J., Hughes W.O.H., Perez-Sato J.A., Martin S.J., Roy G.G.F. and Ratnieks F.L.W. 2010. Sexual selection in honey bees: colony variation and the importance of size in male mating success. Behav. Ecol. 21: 520-525Google Scholar
  12. Cremer S., Ugelvig L.V., Drijfhout F.P., Schlick-Steiner B.C., Steiner F.M., Seifert B., Hughes D.P., Schulz A., Petersen K.S., Konrad H., Stauffer C., Kiran K., Espadaler X., d’Ettorre P., Aktac N., Eilenberg J., Jones G.R., Nash D.R., Pedersen J.S. and Boomsma J.J. 2008. The evolution of invasiveness in garden ants. PLoS One 3: e3838Google Scholar
  13. Den Boer S.P.A., Baer B. and Boomsma J.J. 2010. Seminal fluid mediates ejaculate competition in social insects. Science 327: 1506-1509Google Scholar
  14. Den Boer S.P.A., Baer B., Dreier S., Aron S., Nash D.R. and Boomsma J.J. 2009. Prudent sperm use by leaf-cutter ant queens. Proc. R. Soc. B. 276: 3945-3953Google Scholar
  15. Den Boer S.P.A., Boomsma J.J. and Baer B. 2008. Seminal fluid enhances sperm viability in the leafcutter ant Atta colombica. Behav. Ecol. Sociobiol. 62: 1843-1849Google Scholar
  16. Den Boer S.P.A., Boomsma J.J. and Baer B. 2009. Honey bee males and queens use glandular secretions to enhance sperm viability before and after storage. J. Insect Physiol. 55: 538-543Google Scholar
  17. Falconer D.S. 1981. Introduction to Quantitative Genetics. Longmans Green LondonGoogle Scholar
  18. Fjerdingstad E.J. 2005. Control of body size of Lasius niger ant sexuals - worker interests, genes and environment. Mol. Ecol. 14: 3123-3132Google Scholar
  19. Fjerdingstad E.J. and Boomsma J.J. 1997. Variation in size and sperm content of sexuals in the leafcutter ant Atta colombica. Insect. Soc. 44: 209-218Google Scholar
  20. Gage M.J.G. 1991. Risk of sperm competition directly affects ejaculate size in the mediterranean fruit-fly. Anim. Behav. 42: 1036-1037Google Scholar
  21. Gage M.J.G. 1994. Associations between body-size, mating pattern, testis size and sperm lengths across butterflies. Proc. R. Soc. Lond. Ser. B-Biol. Sci. 258: 247-254Google Scholar
  22. Heinze J. and Hölldobler B. 1993. Fighting for a harem of queens - physiology of reproduction in Cardiocondyla male ants. Proc. Natl. Acad. Sci. USA. 90: 8412-8414Google Scholar
  23. Heinze J. and Schrempf A. 2008. Aging and reproduction in social insects - A mini-review. Gerontology 54: 160-167Google Scholar
  24. Holman L. 2009. Drosophila melanogaster seminal fluid can protect the sperm of other males. Funct. Ecol. 23: 180-186Google Scholar
  25. Hughes W.O.H., Oldroyd B.P., Beekman M. and Ratnieks F.L.W. 2008. Ancestral monogamy shows kin selection is key to the evolution of eusociality. Science. 320: 1213-1216Google Scholar
  26. Hughes W.O.H., Sumner S., Van Borm S. and Boomsma J.J. 2003. Worker caste polymorphism has a genetic basis in Acromyrmex leaf-cutting ants. Proc. Natl. Acad. Sci. USA. 100: 9394-9397Google Scholar
  27. Hölldobler B. and Bartz S.H. 1985. Sociobiology of reproduction in ants. Progr. Zool. 31: 237-257Google Scholar
  28. Hölldobler B. and Wilson E.O. 1990. The Ants. The Belknap Press of Harvard University Press Cambridge Massachusetts. 732 ppGoogle Scholar
  29. Kronauer D.J.C., Johnson R.A. and Boomsma J.J. 2007. The evolution of multiple mating in army ants. Evolution 61: 413-422Google Scholar
  30. Moore P.J., Harris W.E., Montrose V.T., Levin D. and Moore A.J. 2004. Constraints on evolution and postcopulatory sexual selection: trade-offs among ejaculate characteristics. Evolution 58: 1773-1780Google Scholar
  31. Peeters C. and Ito F. 2001. Colony dispersal and the evolution of queen morphology in social Hymenoptera. Annu. Rev. Entomol. 46: 601-630Google Scholar
  32. Peeters C.P. 1991. Ergatoid queens and intercastes in ants - Two distinct adult forms which look morphologically intermediate between workers and winged queens. Insect. Soc. 38: 1-15Google Scholar
  33. Schlüns H., Schlüns E.A., van Praagh J. and Moritz R.F.A. 2003. Sperm numbers in drone honeybees (Apis mellifera) depend on body size. Apidologie. 34: 577-584Google Scholar
  34. Simmons L.W. and Kotiaho J.S. 2002. Evolution of ejaculates: Patterns of phenotypic and genotypic variation and condition dependence in sperm competition traits. Evolution 56: 1622-1631Google Scholar
  35. Smith C.R., Anderson K.E., Tillberg C.V., Gadau J. and Suarez A.V. 2008. Caste determination in a polymorphic social insect: Nutritional, social, and genetic factors. Am. Nat. 172: 497-507Google Scholar
  36. Stearns S.C. 1992. The Evolution of Life Histories. Oxford University Press Oxford, New York. 248 ppGoogle Scholar
  37. Van Noordwijk A.J. and De Jong G. 1986. Acquisition and allocation of resources: their influence on variation in life history tactics. Am. Nat. 128: 137-142Google Scholar
  38. Villesen P., Murakami T., Schultz T.R. and Boomsma J.J. 2002. Identifying the transition between single and multiple mating of queens in fungus-growing ants. Proc. R. Soc. Lond. Ser. B-Biol. Sci. 269: 1541-1548Google Scholar

Copyright information

© International Union for the Study of Social Insects (IUSSI) 2010

Authors and Affiliations

  • M. Stürup
    • 1
  • S. P. A. den Boer
    • 1
  • D. R. Nash
    • 1
  • J. J. Boomsma
    • 1
  • B. Baer
    • 2
    • 3
  1. 1.Department of Biology, Centre for Social EvolutionUniversity of CopenhagenCopenhagenDenmark
  2. 2.ARC Centre of Excellence in Plant Energy BiologyThe University of Western AustraliaCrawleyAustralia
  3. 3.School of Animal Biology (MO92)The University of Western AustraliaNedlandsAustralia

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