Abstract
Although the majority of social insect colonies are headed by a single queen, some species possess nests that contain numerous reproductive queens (polygyny), a trait that is particularly widespread amongst the ants. Polygyny is often associated with a lack of conspecific inter-nest aggression between workers. This is hypothesised to result from increased nestmate cue diversity within nests, since polygynous nests are more genetically diverse than monogynous nests. Alternatively, it may reflect the common origin of polygynous nests that form polydomous networks. We exploit the recent discovery that the nestmate discrimination system in the ant Formica exsecta is based on cuticular hydrocarbons to investigate cue (Z9-alkenes) diversity in several monogynous and polygynous populations. Contrary to previous predictions, in all polygynous populations, the variation between nests in the Z9-alkene profiles was reduced relative to that found in monogynous populations. However, nest-specific Z9-alkene profiles with little variation amongst nestmate workers were still maintained irrespective of nest type or population. This suggests a very effective gestalt mechanism that homogenises the chemical discrimination cues, despite genetic diversity within colonies. Although the reduction in variation between nests was associated with reduced worker aggression on the population level, it cannot totally explain the weak aggression associated with polygynous populations.
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References
Aitchison J. 1986. The Statistical Analysis of Compositional Data. Monographs in Statistics and Applied Probability. Chapman and Hall London. 416 pp
Akino T., Terayama M., Wakamura S. and Yamaoka R. 2002. Intraspecific variation of cuticular hydrocarbon composition in Formica japonica Motschoulsky (Hymenoptera: Formicidae). Zool. Sci. 19: 1155–1165
Akino T., Yamamura K., Wakamura S. and Yamaoka R. 2004. Direct behavioural evidence for hydrocarbons as nestmate recognition cues in Formica japonica (Hymenoptera: Formicidae). Appl. Entomol. Zool. 39: 381–387
Beye M., Neumann P., Chapuisat M., Pamilo P. and Moritz R.F.A. 1998. Nest mate recognition and genetic relatedness of nests in the ant Formica pratensis. Behav. Ecol. Sociobiol. 43: 67–72
Beye M., Neumann P. and Moritz R.F.A. 2004. Nest mate recognition and the genetic gestalt in the mound-building ant Formica polyctena. Insect. Soc. 44: 49–58
Buschinger A. 1974. Monogynie und Polygynie in Insektensozietäten. In: Sozialpolymorphismus bei Insekten (G.H. Schmidt, Ed), Wissenschaftliche Verlagsgesellschhaft MBH Stuttgart. pp 862–896
Breed M.D. and Bennett B. 1987. Kin recognition in highly eusocial insects. In: Kin Recognition in Animals (D.J.C. Fletcher and C.D. Michener, Eds), Wiley, Chichester, UK. pp 243–285
Brown W.D., Liautard C. and Keller L. 2003. Sex ratio-dependent execution of queens in polygynous colonies of the ant Formica exsecta. Oecologia 134: 12–17
Carlin N.F., Reeve H.K. and Cover S.P. 1993. Kin discrimination and division of labour among matrilines in the polygynous carpenter ant Camponotus planatus. In: Queen number and Sociality in Insects (L. Keller, Ed), Oxford University Press, Oxford. pp 362–401
Chapuisat M., Bernasconi C., Hoehn S. and Reuter M. 2005. Nestmate recognition in the unicolonial ant Formica paralugubris. Behav. Ecol. 16: 15–19
Crosland M.W.J. 1990. The influence of the queen, colony size and worker ovarian development on nestmate recognition in the ant Rhytidoponera confuse. Anim. Behav. 39: 413–425
Coyne J.A., Wicker-Thomas C. and Jallon J.M. 1999. A gene responsible for a cuticular hydrocarbon polymorphism in Drosophila melanogaster. Genetic Res. 73: 189–203
Crozier R.H. and Dix M.W. 1979. Analysis of two genetic models for the innate components of colony odor in social Hymenoptera. Behav. Ecol. Sociobiol. 4: 217–224
Dallas J.F., Gow J.L., Jones A.M. and Young M.R. 2001. Genetic evidence for social polymorphism in the rare wood ant Formica exsecta Nyl. in Scotland. British Ecol. Soc. Bull. SEPG 1528
Dallerac R., Labeur C., Jallon J.-M., Knipple D.C., Roelofs W.L. and Wicker-Thomas C. 2000. A delta 9 desaturase gene with a different substrate specificity is responsible for the cuticular diene hydrocarbon polymorphism in Drosophila melanogaster. Proc. Natl Acad. Sci. USA 97: 9449–9454
Debout G., Schatz B., Elias M. and McKey D. 2007. Polydomy in ants: what we know, what we think we know, and what remains to be done. Biol. J. Linn. Soc. 90: 319–348
Ferveur J.-F. and Jallon J.-M. 1996. Genetic control of male cuticular hydrocarbons in Drosophila melanogaster. Genetic Res. 67: 211–218
Goropashnaya A.V., Fedorov V.B., Seifert B. and Pamilo P. 2007. Phylogeography and population structure in the ant Formica exsecta (Hymenoptera, Formicidae) across Eurasia as reflected by mitochondrial DNA variation and microsatellites. Ann. Zool. Fenn. 44: 462–474
Guerrieri F.J., Nehring V., Jörgensen C.G., Nielsen J., Galizia C.G. and D’Ettorre P. 2009. Ants recognise foes not friends. Proc. R. Soc. B. doi: 10.1098/rspb.2008.1860
Heinze J. 2008. The demise of the standard ant (Hymenoptera: Formicidae). Myrmecol. News 11: 9–20
Helanterä H., Strassmann J.E., Carrillo J. and Queller D.C. 2009. Unicolonial ants: where do they come from, what are they, and where are they going? Trends Ecol. Evol. 24: 341–349
Howard R.W. and Blomquist G.J. 2005. Ecological, behavioural and biochemical aspects of insect hydrocarbons. Annu. Rev. Entomol. 50: 371–393
Hölldobler B. and Michener C.D. 1980. Mechanisms of identification and discrimination in social Hymenoptera. In: Evolution of Social Behavior: Hypotheses and Empirical Tests (H. Markl, Ed), Verlag Chemie, Weinheim. pp 35–57
Hölldobler B. and Wilson E.O. 1977. The number of queens: an important trait in ant evolution. Naturwissenschaften 64: 8–15
Katzerke A., Neumann P., Pirk C.W.W., Bliss P. and Moritz R.F.A. 2006. Seasonal nestmate recognition in the ant Formica exsecta. Behav. Ecol. Sociobiol. 61: 143–150
Keller L. 1997. Indiscriminate altruism: unduly nice parents and siblings. Trends Ecol. Evol. 12: 99–103
Keller L. and Passera L. 1989. Influence of the number of queens on nestmate recognition and attractiveness of queens to workers in the Argentine ant, Iridomyrmex humilis (Mayr). Anim. Behav. 37: 733–740
Kümmerli R. and Keller L. 2007. Contrasting population genetic structure for workers and queens in the putatively unicolonial ant Formica exsecta. Mol. Ecol. 16: 4493–4503
Jaisson P. 1991. Kinship and fellowship in ants and social wasps. In: Kin Recognition (P.G. Hepper, Ed), Cambridge University Press, Cambridge. pp 60–93
Lockey K.H. 1991. Insect hydrocarbon classes—implications for chemotaxonomy. Insect Biochem. 21: 91–97
Martin S.J. and Drijfhout F.P. 2009. Nestmate and task cues are influenced and encoded differently within ant cuticular hydrocarbon profiles. J. Chem. Ecol. 35: 368–374
Martin S.J., Vitikainen E., Helanterä H. and Drijfhout F.P. 2008a. Chemical basis of nest-mate discrimination in the ant Formica exsecta. Proc. R. Soc. B. 275: 1271–1278
Martin S.J., Helanterä H. and Drijfhout F.P. 2008b. Evolution of species-specific cuticular hydrocarbon patterns in Formica ants. Biol. J. Linn. Soc. 95: 131–140
Ozaki M., Wada-Katsumata A., Fujikawa K., Iwasaki M., Yokohari F., Satoji Y., Nisimura T. and Yamaoka R. 2005. Ant nest mate and non-nest mate discrimination by a chemosensory sensillium. Science 309: 311–315
Pamilo P. 1982. Genetic population structure in polygynous Formica ants. Heredity 48: 95–106
Peeters C.P. 1988. Nestmate discrimination in a ponerine ant (Rhytidoponera sp. 12) without a queen caste and with a low intra-nest relatedness. Insect. Soc. 35: 34–46
Rosengren R. and Pamilo P. 1983. The evolution of polygyny and polydomy in mound-building Formica ants. Acta Entomol. Fenn. 42: 65–77
Rosengren R., Sundström L. and Fortelius W. 1993. Monogyny and polygyny in Formica ants: the result of alternative dispersal strategies. In: Queen Number and Sociality in Insects (Keller L., Ed), Oxford University Press, Oxford. pp 308–333
Rosset H., Schwander T. and Chapuisat M. 2007. Nestmate recognition and levels of aggression are not altered by changes in genetic diversity in a socially polymorphic ant. Anim. Behav. 74: 951–956
Satoh T. and Hirota T. 2005. Factors affecting internest variation in the aggressiveness of a polygynous ant, Camponotus yamaokai. Entomol. Sci. 8: 277–281
Savarit F., Sureau G., Cobb M. and Ferveur J.-F. 1999. Genetic elimination of known pheromones reveals the fundamental chemical bases of mating and isolation in Drosophila. Proc. Natl Acad. Sci. USA 96: 9015–9020
Seppä P., Gyllenstrand N., Corander J. and Pamilo P. 2004. Coexistence of the social types: Genetic population structure in the ant Formica exsecta. Evolution 58: 2462–2471
Singer T.L. 1998. Roles of hydrocarbons in the recognition systems of insects. Am. Zool. 38: 394–405
Snyder L.E. 1993. Non-random behavioural interactions among genetic sub-groups in a polygynous ant. Anim. Behav. 46: 431–439
Starks P.T., Watson R.E., Dipaola M.J. and Dipaola C.P. 1998. The effect of queen number on nestmate discrimination in the facultatively polygynous ant Pseudomyrmex pallidus (Hymenoptera: Formicidae). Ethology 104: 573–584
Steiner F.M., Schlick-Steiner B.C., Moder K., Stauffer C., Arthofer W., Buschinger A., Espadaler X., Christian E., Einfinger K., Lorber E., Schafellner C. and Crozier R.H. 2007. Abandoning aggression but maintaining self-nonself discrimination as a first stage in ant supercolony formation. Curr. Biol. 17: 1903–1907
Stuart R.J. 1988. Collective cues as a basis for nestmate recognition in polygynous Leptothoracine ants. Proc. Natl Acad. Sci. USA 85: 4572–4575
Stuart R.J. and Herbers J.M. 2000. Nest mate recognition in ants with complex colonies: within- and between-population variation. Behav. Ecol. 11: 676–685
Takahashi A., Tsaur S.C., Coyne J.A. and Wu C.I. 2001. The nucleotide changes governing cuticular hydrocarbon variation and their evolution in Drosophila melanogaster. Proc. Natl Acad. Sci. USA 98: 3920–3925
Wagner D., Tissot M. and Gordon D.M. 2001 Task-related environment alters the cuticular hydrocarbon composition of harvester ants. J. Chem. Ecol. 27: 1805–1819
Acknowledgments
Many thanks go to Liselotte Sundström of Helsinki University for allowing access to the F. exsecta study population and Duncan Jackson for his detailed comments. Funding for S.J.M. and F·P.D. was provided by NERC (NE/C512310/1) and to H.H. and L. Sundström by the Academy of Finland grants (213821; 121078 and 206505), respectively.
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Martin, S.J., Helanterä, H., Kiss, K. et al. Polygyny reduces rather than increases nestmate discrimination cue diversity in Formica exsecta ants. Insect. Soc. 56, 375–383 (2009). https://doi.org/10.1007/s00040-009-0035-z
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DOI: https://doi.org/10.1007/s00040-009-0035-z
Keywords
- Formica exsecta
- Ants
- Polygyny
- Cuticular hydrocarbons
- Aggression
- Nestmate recognition