Oecologia

, Volume 157, Issue 4, pp 717–723

Foreign ant queens are accepted but produce fewer offspring

Behavioral Ecology - Original Paper

Abstract

Understanding social evolution requires us to understand the processes regulating the number of breeders within social groups and how they partition reproduction. Queens in polygynous (multiple queens per colony) ants often seek adoption in established colonies instead of founding a new colony independently. This mode of dispersal leads to potential conflicts, as kin selection theory predicts that resident workers should favour nestmate queens over foreign queens. Here we compared the survival of foreign and resident queens as well as their relative reproductive share. We used the ant Formica exsecta to construct colonies consisting of one queen with workers related to this resident queen and introduced a foreign queen. We found that the survival of foreign queens did not differ from that of resident queens over a period of 136 days. However, the genetic analyses revealed that resident queens produced a 1.5-fold higher number of offspring than introduced queens, and had an equal or higher share in 80% of the colonies. These data indicate that some discrimination can occur against dispersing individuals and that dispersal can thus have costs in terms of direct reproduction for dispersing queens.

Keywords

Queen acceptance Reproductive skew Dispersal Social insects Ants 

References

  1. Bennett B (1988) Discrimination of nestmate and non-nestmate sexuals by ants (Hymenoptera: Formicidae). Insect Soc 35:82–91CrossRefGoogle Scholar
  2. Beye M, Neumann P, Chapuisat M, Pamilo P, Moritz RFA (1998) Nestmate recognition and the genetic relatedness of nests in the ant Formica pratensis. Behav Ecol Sociobiol 43:67–72CrossRefGoogle Scholar
  3. Boomsma JJ, Franks NR (2006) Social insects: from selfish genes to self organisation and beyond. Trends Ecol Evol 21:303–308PubMedCrossRefGoogle Scholar
  4. Bourke AFG, Franks NR (1995) Social evolution in ants. Princeton University Press, PrincetonGoogle Scholar
  5. Bourke AFG, Green HAA, Bruford MW (1997) Parentage, reproductive skew and queen turnover in a multiple-queen ant analysed with microsatellites. Proc R Soc Lond B 264:277–283CrossRefGoogle Scholar
  6. Breed MD, Welch CK, Cruz R (1994) Kin discrimination within honey-bee (Apis mellifera) colonies: an analysis of the evidence. Behav Processes 33:25–39CrossRefGoogle Scholar
  7. Breed MD, Diaz PH, Lucero KD (2004) Olfactory information processing in honeybee, Apis mellifera, nestmate recognition. Anim Behav 68:921–928. doi:10.1016/j.anbehav.2003.10.033 CrossRefGoogle Scholar
  8. Brown WD, Keller L (2002) Queen recruitment and split sex ratios in polygynous colonies of the ant Formica exsecta. Ecol Lett 5:102–109. doi:10.1046/j.1461-0248.2002.00291.x CrossRefGoogle Scholar
  9. Brown WD, Liautard C, Keller L (2003) Sex-ratio dependent execution of queens in polygynous colonies of the ant Formica exsecta. Oecologia 134:12–17. doi:10.1007/s00442-002-1072-8 PubMedCrossRefGoogle Scholar
  10. Chapuisat M (1996) Characterization of microsatellite loci in Formica lugubris B and their variability in other ant species. Mol Ecol 5:599–601PubMedCrossRefGoogle Scholar
  11. Chapuisat M, Goudet J, Keller L (1997) Microsatellites reveal high population viscosity and limited dispersal in the ant Formica paralugubris. Evolution 51:475–482CrossRefGoogle Scholar
  12. Cherix D, et al (1991) Alternative reproductive strategies in Formica lugubris Zett. (Hymenoptera Formicidae). Ethol Ecol Evol:61–66Google Scholar
  13. Crozier RH, Pamilo P (1996) Evolution of social insect colonies: sex allocation and kin selection. Oxford University Press, OxfordGoogle Scholar
  14. Evans JD (1996) Queen longevity, queen adoption, and posthumous indirect fitness in the facultatively polygynous ant Myrmica tahoensis. Behav Ecol Sociobiol 39:275–284CrossRefGoogle Scholar
  15. Fortelius W, Rosengren R, Cherix D, Chautems D (1993) Queen recruitment in a highly polygynous supercolony of Formica lugubris (Hymenoptera, Formicidae). Oikos 67:193–200CrossRefGoogle Scholar
  16. Fournier D, Keller L (2001) Partitioning of reproduction among queens in the Argentine ant, Linepithema humile. Anim Behav 62:1039–1045. doi:10.1006/anbe.2001.1848 CrossRefGoogle Scholar
  17. Fournier D, Aron S, Keller L (2004) Significant reproductive skew in the facultatively polygynous ant Pheidole pallidula. Mol Ecol 13:203–210. doi:10.1046/j.1365-294X.2003.02036.x PubMedCrossRefGoogle Scholar
  18. Gyllenstrand N, Gertsch PJ, Pamilo P (2002) Polymorphic microsatellite DNA markers in the ant Formica exsecta. Mol Ecol Notes 2:67–69. doi:10.1046/j.1471-8286.2002.00152.x CrossRefGoogle Scholar
  19. Hamilton WD (1987) Discriminating nepotism: expectable, common, overlooked. In: Fletcher DJC, Michener CD (eds) Kin recognition in animals. Wiley, New York, pp 417–437Google Scholar
  20. Hammond RL, Bruford MW, Bourke AFG (2006) A test of reproductive skew models in a field population of a multiple-queen ant. Behav Ecol Sociobiol 61:265–275. doi:10.1007/s00265-006-0257-2 CrossRefGoogle Scholar
  21. Hannonen M, Sundström L (2003a) Reproductive sharing among queens in the ant Formica fusca. Behav Ecol 14:870–875. doi:10.1093/beheco/arg069 CrossRefGoogle Scholar
  22. Hannonen M, Sundström L (2003b) Worker nepotism among polygynous ants. Nature 421:910. doi:10.1038/421910a PubMedCrossRefGoogle Scholar
  23. Heinze J, Trunzer B, Holldobler B, Delabie JHC (2001) Reproductive skew and queen relatedness in an ant with primary polygyny. Insect Soc 48:149–153. doi:10.1007/PL00001758 CrossRefGoogle Scholar
  24. Holzer B, Kümmerli R, Keller L, Chapuisat M (2006) Sham nepotism as a result of intrinsic differences in brood viability in ants. Proc R Soc Lond B 273:2049–2052. doi:10.1098/rspb.2006.3553 CrossRefGoogle Scholar
  25. Keller L (1988) Evolutionary implications of polygyny in the Argentine ant, Iridomyrmex humilis (Mayr) (Hymenoptera: Formicidae): an experimental study. Anim Behav 36:159–165CrossRefGoogle Scholar
  26. Keller L (1991) Queen Number, mode of colony founding, and queen reproductive success in ants (Hymenoptera, Formicidae). Ethol Ecol Evol 3:307–316Google Scholar
  27. Keller L (1993a) Queen number and sociality in insects. Oxford University Press, OxfordGoogle Scholar
  28. Keller L (1993b) The assessment of reproductive success of queens in ants and other social insects. Oikos 67:177–180CrossRefGoogle Scholar
  29. Keller L (1995) Social life: the paradox of multiple-queen colonies. Trends Ecol Evol 10:355–360CrossRefGoogle Scholar
  30. Keller L (1997) Indiscriminate altruism: unduly nice parents and siblings. Trends Ecol Evol 12:99–103CrossRefGoogle Scholar
  31. Keller L, Chapuisat M (1999) Cooperation among selfish individuals in insect societies. Bioscience 49:899–909CrossRefGoogle Scholar
  32. Kikuchi T, Tsuji K, Ohnishi H, Le Breton J (2007) Caste-biased acceptance of non-nestmates in a polygynous ponerine ant. Anim Behav 73:559–565. doi:10.1016/j.anbehav.2006.04.015 CrossRefGoogle Scholar
  33. Komdeur J (2006) Variation in individual investment strategies among social animals. Ethology 112:729–747CrossRefGoogle Scholar
  34. Kümmerli R, Keller L (2007a) Contrasting population genetic structure for workers and queens in the putatively unicolonial ant Formica exsecta. Mol Ecol 16:4493–4503PubMedCrossRefGoogle Scholar
  35. Kümmerli R, Keller L (2007b) Reproductive specialization in multiple-queen colonies of the ant Formica exsecta. Behav Ecol 18:375–383. doi:10.1093/beheco/arl088 CrossRefGoogle Scholar
  36. Kümmerli R, Keller L (2008) Reproductive parameters vary with social and ecological factors in the polygynous ant Formica exsecta. Oikos 117:580–590. doi:10.1111/j.2007.0030-1299.16207.x CrossRefGoogle Scholar
  37. Kümmerli R, Helms KR, Keller L (2005) Experimental manipulation of queen number affects colony sex ratio investment in the highly polygynous ant Formica exsecta. Proc R Soc Lond B 272:1789–1794. doi:10.1098/rspb.2005.3163 CrossRefGoogle Scholar
  38. Kutter H (1969) Die sozialparasitischen Ameisen der Schweiz. Neujahrsblatt Naturforsch Ges Zürich 5–62Google Scholar
  39. Langer P, Hogendoorn K, Keller L (2004) Tug-of-war over reproduction in a social bee. Nature 428:844–847. doi:10.1038/nature02431 PubMedCrossRefGoogle Scholar
  40. Liang D, Silverman J (2000) “You are what you eat”: diet modifies cuticular hydrocarbons and nestmate recognition in the Argentine ant, Linepithema humile. Naturwissenschaften 87:412–416. doi:10.1007/s001140050752 PubMedCrossRefGoogle Scholar
  41. Maynard Smith J, Szathmary E (1995) The major transitions in evolution. Freeman, OxfordGoogle Scholar
  42. Nonacs P (1988) Queen number in colonies of social Hymenoptera as a kin-selected adaptation. Evolution 42:566–580CrossRefGoogle Scholar
  43. Ozaki M et al (2005) Ant nestmate and non-nestmate discrimination by a chemosensory sensillum. Science 309:311–314PubMedCrossRefGoogle Scholar
  44. Pamilo P, Seppä P (1994) Reproductive competition and conflicts in colonies of the ant Formica sanguinea. Anim Behav 48:1201–1206CrossRefGoogle Scholar
  45. Queller DC, Goodnight KF (1989) Estimating relatedness using genetic markers. Evolution 43:258–275CrossRefGoogle Scholar
  46. Queller DC, Strassmann JE (2002) The many selves of social insects. Science 296:311–313. doi:10.1126/science.1070671 PubMedCrossRefGoogle Scholar
  47. Ratnieks FLW, Foster KR, Wenseleers T (2006) Conflict resolution in insect societies. Annu Rev Entomol 51:581–608. doi:10.1146/annurev.ento.51.110104.151003 PubMedCrossRefGoogle Scholar
  48. Reeve HK, Keller L (2001) Test of reproductive skew models in social insects. Annu Rev Entomol 46:347–385. doi:10.1007/s00265-006-0257-2 PubMedCrossRefGoogle Scholar
  49. Rosengren R, Cherix D, Pamilo P (1986) Insular ecology of the red wood ant Formica truncorum. II. Distribution, reproductive strategy and competition. Mitt Schweiz Entomol Ges 59:63–93Google Scholar
  50. Rosengren R, Pamilo P (1983) The evolution of polygyny and polydomy in mound-building Formica ants. Acta Entomol Fenn 42:65–77Google Scholar
  51. Ross KG (1988) Differential reproduction in multiple-queen colonies of the fire ant Solenopsis invicta (Hymenoptera: Formicidae). Behav Ecol Sociobiol 23:341–355CrossRefGoogle Scholar
  52. Ross KG (1993) The breeding system of the fire ant Solenopsis invicta, and its effects on colony genetic structure. Am Nat 141:554–576CrossRefGoogle Scholar
  53. Rüppell O, Heinze J, Hölldobler B (2002) Intracolonial patterns of reproduction in the queen-size dimorphic ant Leptothorax rugatulus. Behav Ecol 13:239–247CrossRefGoogle Scholar
  54. Stuart R, Gresham-Bisset L, Alloway T (1993) Queen adoption in the polygynous and polydomous ant, Leptothorax curvispinosus. Behav Ecol 4:276–281CrossRefGoogle Scholar
  55. Sundström L (1997) Queen acceptance and nestmate recognition in monogyne and polygyne colonies of the ant Formica truncorum. Anim Behav 53:499–510CrossRefGoogle Scholar
  56. Szathmary E, Maynard Smith JM (1995) The major evolutionary transitions. Nature 374:227–232. doi:10.1038/374227a0 PubMedCrossRefGoogle Scholar
  57. Tarpy DR, Gilley DC, Seeley TD (2004) Levels of selection in a social insect: a review of conflict and cooperation during honey bee (Apis mellifera) queen replacement. Behav Ecol Sociobiol 55:513–523. doi:10.1007/s00265-003-0738-5 CrossRefGoogle Scholar
  58. Vásquez G, Silverman J (2008) Queen acceptance and the complexity of nestmate discrimination in the Argentine ant. Behav Ecol Sociobiol 62:537–548. doi:10.1007/s00265-007-0478-z CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2008

Authors and Affiliations

  • Barbara Holzer
    • 1
  • Michel Chapuisat
    • 1
  • Laurent Keller
    • 1
  1. 1.Department of Ecology and EvolutionUniversity of Lausanne1015LausanneSwitzerland

Personalised recommendations