Skip to main content
SpringerLink
Log in

Seasonal polydomy and unicoloniality in a polygynous population of the red wood ant Formica truncorum

  • Original Article
  • Published:
Behavioral Ecology and Sociobiology Aims and scope Submit manuscript

Abstract

Ant colonies may have a single or several reproductive queens (monogyny and polygyny, respectively). In polygynous colonies, colony reproduction may occur by budding, forming multinest, polydomous colonies. In most cases, budding leads to strong genetic structuring within populations, and positive relatedness among nestmates. However, in a few cases, polydomous populations may be unicolonial, with no structuring and intra-nest relatedness approaching zero. We investigated the spatial organisation and genetic structure of a polygynous, polydomous population of Formica truncorum in Finland. F. truncorum shifts nest sites between hibernation and the reproductive season, which raises the following question: are colonies maintained as genetic entities throughout the seasons, or is the population unicolonial throughout the season? Using nest-specific marking and five microsatellite loci, we found a high degree of mixing between individuals of the population, and no evidence for a biologically significant genetic structuring. The nestmate relatedness was also indistinguishable from zero. Taken together, the results show that the population is unicolonial. In addition, we found that the population has undergone a recent bottleneck, suggesting that the entire population may have been founded by a very limited number of females. The precise causes for unicoloniality in this species remain open, but we discuss the potential influence of intra-specific competition, disintegration of recognition cues and the particular hibernation habits of this species.

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

Similar content being viewed by others

References

  • Astruc C, Malosse C, Errard C (2001) Lack of intraspecific aggression in the ant Tetramorium bicarinatum: a chemical hypothesis. J Chem Ecol 27:1229–1248

    Article  CAS  PubMed  Google Scholar 

  • Banschbach VS, Herbers JM (1996a) Complex colony structure in social insects. I. Ecological determinants and genetic consequences. Evolution 50:285–297

    Google Scholar 

  • Banschbach VS, Herbers JM (1996b) Complex colony structure in social insects. II. Reproduction, queen-worker conflict, and levels of selection. Evolution 50:298–307

    Google Scholar 

  • Belkhir K, Borsa P, Chikhi L, Raufaste N, Bonhomme F (2001) GENETIX 4.02, logiciel sous Windows TM pour la génétique des populations. Laboratoire Génome Populations et Intéractions, Université Montpellier II, France

  • Beye M, Neumann P, Moritz RFA (1997) Nestmate recognition and the genetic gestalt in the mound-building ant Formica polyctena. Insectes Soc 44:49–58

    Article  Google Scholar 

  • 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 43:67–72

    Article  Google Scholar 

  • Bolton B (1980) The ant tribe Tetramoriini. The genus Tetramorium Mayr in the oriental and Indo-Australian regions, and in Australia. Bull Br Mus Nat Hist 40:192–384

    Google Scholar 

  • Boomsma JJ, Brouwer AH, Van Loon AJ (1990) A new polygynou Lasius species (Hymenoptera: Formicidae) from Central Europe. II. Allozymatic confirmation of specific status and social structure. Insectes Soc 37:363–375

    Google Scholar 

  • Boomsma JJ, Nielsen J, Sundström L, Oldham NJ, Tentschert J, Petersen HC, Morgan ED (2003) Informational constraint on optimal sex allocation in ants. Proc Natl Acad Sci USA 100:8799–8804

    Article  CAS  PubMed  Google Scholar 

  • Bourke AFG, Franks NR (1995) Social evolution in ants. Princeton University Press, Princeton

  • Bourke AFG, Heinze J (1994) The ecology of communal breeding: the case of multiple-queen leptothoracine ants. Philos Trans R Soc Lond Ser B 345:359–372

    Google Scholar 

  • Breed MD, Garry MF, Pearce AN, Hibbard BE, Bjostad LB, Page RE Jr (1995) The role of wax comb in honey bee nestmate recognition. Anim Behav 50:489–496

    Article  Google Scholar 

  • Bulmer MG (1983) Sex ratio theory in social insects with swarming. J Theor Biol 100:329–339

    Google Scholar 

  • Chapman RE, Bourke AFG (2001) The influence of sociality on the conservation biology of social insects. Ecol Lett 4:650–662

    Article  Google Scholar 

  • Chapuisat M (1996) Characterization of microsatellite loci in Formica lugubris B and their variability in other ant species. Mol Ecol 5:599–601

    Article  CAS  PubMed  Google Scholar 

  • Chapuisat M, Goudet J, Keller L (1997) Microsatellite reveal high population viscosity and limited dispersal in the ant Formica paralugubris. Evolution 51:475–482

    Google Scholar 

  • Clément JL, Bonavita-Courgourdan AB, Lange C (1987) Nestmate recognition and cuticular hydrocarbons in Camponotus vagus Scop.In: Eder J, Rembold H (eds) Chemistry and biology of social insects. Perperny, Munich, pp 473–474

  • Collingwood CA (1979) The Formicidae (Hymenoptera) of Fennoscandia and Denmark. Scandinavian Science, Klampenborg

  • Cornuet JM, Luikart G (1996) Description and power analysis of two test for detecting recent population bottlenecks from allele frequency data. Genetics 144:2001–2014

    CAS  PubMed  Google Scholar 

  • Crozier RH (1979) Genetics of sociality. In: Hermann HR (ed) Social insects, vol I. Academic, New York, pp 223–286

  • Crozier RH, Pamilo P (1996) Evolution of social insects colonies: sex allocation and kin selection. Oxford University Press, Oxford

    Google Scholar 

  • Debout G, Provost E, Renucci M, Tirard A, Schatz B, McKey D (2003) Colony structure in a plant-ant: behavioural, chemical and genetic study of polydomy in Cataulacus mckeyi (Myrmicinae). Oecologia 137:195–204

    Article  PubMed  Google Scholar 

  • DeHeer CJ, Backus VL, Herbers JM (2001) Sociogenetic responses to ecological variation in the ant Myrmica punctiventris are context dependent. Behav Ecol Sociobiol 49:375–386

    Article  Google Scholar 

  • Espadaler X, Rey S (2001) Biological constraints and colony founding in the polygynous invasive ant Lasius neglectus (Hymenoptera, Formicidae). Insectes Soc 48:159–164

    Google Scholar 

  • Giraud T, Pedersen JS, Keller L (2002) Evolution of supercolonies: the Argentine ants of southern Europe. Proc Natl Acad Sci USA 99:6075–6079

    Article  CAS  PubMed  Google Scholar 

  • Goudet J, Raymond M, De Meeüs T, Rousset F (1996) Testing differentiation in diploid populations. Genetics 144:1933–1940

    CAS  PubMed  Google Scholar 

  • Gyllenstrand N (2002) Effects of social organization on spatial genetic structures in Formica ants. PhD Thesis, Comprehensive Summaries of Uppsala Dissertations from the Faculty of Science and Technology

  • Gyllenstrand N, Gertsch PJ, Pamilo P (2002) Polymorphic microsatellite DNA markers in the ant Formica exsecta. Mol Ecol Notes 2:67–69

    CAS  Google Scholar 

  • Gyllenstrand P, Seppä P (2003) Conservation genetics of the wood ant, Formica lugubris, in a fragmented landscape. Mol Ecol 12:2931–2940

    Article  CAS  PubMed  Google Scholar 

  • Hamilton WD (1964) The genetical evolution of social behaviour. J Theor Biol 7:1–52

    CAS  PubMed  Google Scholar 

  • Helanterä H (2004) Kinship and conflicts over male production in Formica ants. PhD Thesis, University of Helsinki (in press)

  • Herbers JM (1986) Nest site limitation and facultative polygyny in the ant Leptothorax longispinosus. Behav Ecol Sociobiol 19:115–122

    Article  Google Scholar 

  • Higashi S (1976) Nest proliferation by budding and nest growth pattern in Formica (Formica) yessensis in Ishikari Shore. J Fac Sci Hokkaido Univ Ser VI Zool 20:359–389

    Google Scholar 

  • Higashi S (1978a) Analysis of of internest drifting in a super colonial ant Formica (Formica) yessensis by individually marked workers. Kontyû 46:176–191

  • Higashi S (1978b) Task and areal conservatism and internest drifting in a red wood ant Formica (Formica) yessensis Forel. Jpn J Ecol 28:257–264

    Google Scholar 

  • Hölldobler B, Lumsden CJ (1980) Territorial strategies in ants. Science 210:732–739

    Google Scholar 

  • Hölldobler B, Wilson EO (1977) The number of queens: an important trait in evolution. Naturwissenschaften 64:8–15

    Article  Google Scholar 

  • Hölldobler B, Wilson EO (1990) The ants. Harvard University Press, Cambridge, Mass

  • Holway DA (1999) Competitive mechanism underlying the displacement of native ants by the invasive Argentine ant. Ecology 80:238–251

    Google Scholar 

  • Holway DA, Case JT (2001) Effect of colony-level variation on competitive ability in the invasive Argentine ant. Anim Behav 61:1181–1192

    Article  Google Scholar 

  • Holway DA, Suarez AV, Case JT (1998) Loss of intraspecific aggression in the success of a widespread invasive social insect. Science 282:949–952

    Article  CAS  PubMed  Google Scholar 

  • Human KG, Gordon DM (1996) Exploitation and interference competition between the invasive Argentine ant, Linepithema humile, and native ant species. Oecologia 105:405–412

    Article  Google Scholar 

  • Ito M (1973) Seasonal population trends and nest structure in a polydomous ant, Formica (Formica) yessensis Forel. J Fac Sci Hokkaido Univ Ser VI Zool 19:270–293

    Google Scholar 

  • Ito M, Imamura S (1974) Observations on the nuptial flight and internidal relationship in a polydomous ant, Formica (Formica) yessensis Forel. J Fac Sci Hokkaido Univ Ser VI Zool 19:681–694

    Google Scholar 

  • Kaufmann B, Boomsma JJ, Passera L, Petersen KN (1992) Relatedness and inbreeding in a French population of the unicolonial ant Iridomyrmex humilis (Mayr). Insectes Soc 39:195–213

    Google Scholar 

  • Keller L (1988) Evolutionary implications of polygyny in the Argentine ant, Iridomyrmex humilis (Mayr) (Hymenoptera: Formicidae): an experimental study. Anim Behav 36:159–165

    Google Scholar 

  • Keller L (1993a) The assessment of reproductive success of queens in ants and social insects. Oikos 67:177–180

    Google Scholar 

  • Keller L (1993b) Queen number and sociality in insects. Oxford University Press, Oxford

  • Keller L (1995) Social life: the paradox of multiple-queen colonies. Trends Ecol Evol 10:353–360

    Article  Google Scholar 

  • Keller L, Ross KG (1998) Selfish genes: a green beard in the red fire ant. Nature 394:573–575

    Article  CAS  Google Scholar 

  • Liautard C, Keller L (2001) Restricted effective queen dispersal at a microgeographic scale in polygynous populations of the ant Formica exsecta. Evolution 55:2484–2492

    CAS  PubMed  Google Scholar 

  • Macewicz S (1979) Some consequences of Fisher’s sex ratio principle for social Hymenoptera that reproduce by colony fission. Am Nat 113:363–371

    Article  Google Scholar 

  • Mantel N (1967) The detection of disease clustering and a generalized regression approach. Cancer Res 27:209–220

    CAS  PubMed  Google Scholar 

  • Markin GP (1970) The seasonal life cycle of the Argentine ant, Iridomyrmex humilis, in southern California. Ann Entomol Soc Am 63:1238–1242

    Google Scholar 

  • Maruyama T, Fuerst PA (1985) Population bottlenecks and nonequilibrium models in population genetics. II. Number of alleles in a small population that was formed by a recent bottleneck. Genetics 111:675–689

    CAS  PubMed  Google Scholar 

  • Nei M (1978) Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89:583–590

    Google Scholar 

  • Nei M, Maruyama T, Chakraborty R (1975) The bottleneck effect and genetic variability in populations. Evolution 29:1–10

    Google Scholar 

  • Nielsen J, Boomsma JJ, Oldham NJ, Petersen HC, Morgan ED (1999) Colony-level and season-specific variation in cuticular hydrocarbon profiles of individual workers in the ant Formica truncorum. Insectes Soc 46:58–65

    Article  Google Scholar 

  • Nonacs P (1988) Queen number in colonies of social Hymenoptera as a kin-selected adaptation. Evolution 42:566–580

    Google Scholar 

  • Nonacs P (1993) The effects of polygyny and colony life history on optimal sex investissment. In Keller L (ed) Queen number and sociality in insects. Oxford University Press, Oxford, pp 110–131

  • Oster GF, Wilson EO (1978) Caste and ecology in the social insects. Princeton University Press, Princeton

  • Pamilo P (1982) Genetic population structure in polygynous Formica ants. Heredity 48:95–106

    CAS  PubMed  Google Scholar 

  • Pamilo P (1983) Genetic differentiation within subdivided population of Formica ants. Evolution 37:1010–1022

    Google Scholar 

  • Pamilo P (1991) Evolution of colony characteristics in social insects. II. Number of reproductive individuals. Am Nat 138:412–433

    Article  Google Scholar 

  • Pamilo P, Sundström L, Fortelius W, Rosengren R (1994) Diploid males and colony-level selection in Formica ants. Ethol Ecol Evol 6:221–235

    Google Scholar 

  • Passera L (1994) Characteristics of tramp species. In: Williams DF (ed) Exotic ants: biology, impact, and control of introduced species. Westview, Boulder, Colo, pp 23–43

  • Passera L, Gilbert M, Aron S (2001) Social parasitism in ants: effect of the inquiline parasite Plagiolepis xene St. on queen distribution and worker production of its host plagiolepis pygmaea Latr. Insectes Soc 48:1–82

    Google Scholar 

  • Pedersen JS, Boomsma JJ (1999) Genetic analysis of colony structure in polydmous and polygynous ant populations. Biol J Linn Soc 66:115–144

    Article  Google Scholar 

  • Pirk CWW, Neumann P, Moritz RFA, Pamilo P (2001) Intranest relatedness and nestmate recognition in the meadow ant Formica pratensis (R.). Behav Ecol Sociobiol 49:366–374

    Article  Google Scholar 

  • Piry S, Luikart G, Cornuet JM (1999) Bottleneck: a computer program for detecting recent reductions in effective population size from allele frequency data. J Hered 90:502–503

    Article  Google Scholar 

  • Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959

    CAS  PubMed  Google Scholar 

  • Queller DC, Goodnight KF (1989) Estimating relatedness using genetic markers. Evolution 242:258–275

    Google Scholar 

  • Queller DC, Strassman JE (1998) Kin selection and social insects. Bioscience 48:165–175

    Google Scholar 

  • Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Hered 86:248–249

    Google Scholar 

  • Rosengren R (1986) Competition and coexistence in an insular ant community—a manipulation experiment (Hymenoptera: Formicidae). Ann Zool Fenn 23:297–302

    Google Scholar 

  • Rosengren R, Pamilo P (1983) The evolution and polygyny and polydomy in mound building Formica ants. Acta Entomol Fenn 42:65–77

    Google Scholar 

  • Rosengren R, Cherix D, Pamilo P (1985) Insular ecology of the red wood ant Formica truncorum Fabr. I. Polydomous nesting, population size and foraging. Mitt Schweiz Entomol Ges 58:147–175

    Google Scholar 

  • Rosengren R, Cherix D, Pamilo P (1986) Insular ecology of the red wood ant Formica truncorum Fabr. I. Distribution, reproductive strategy and competition. Mitt Schweiz Entomol Ges 59:63–94

    Google Scholar 

  • Ross KG (1993) The breeding system of the fire ant Solenopsis invicta: effects of colony genetic structure. Am Nat 141:554–576

    Article  Google Scholar 

  • Ross KG, Keller L (1998) Genetic control of social organization in an ant. Proc Natl Acad Sci USA 95:14232–14237

    Article  CAS  PubMed  Google Scholar 

  • Ross KG, Vargo EL, Keller L (1996) Social evolution in a new environment: the case of introduced fire ants. Proc Natl Acad Sci USA 93:3021–3025

    Article  CAS  PubMed  Google Scholar 

  • Schmid-Hempel P (1998) Parasites in social insects. Princeton University Press, Princeton

  • Seppä P, Pamilo P (1995) Gene flow and population viscosity in Myrmica ants. Heredity 74:200–209

    Google Scholar 

  • Seppä P, Walin L (1996) Sociogenetic organization of the red ant Myrmica rubra. Behav Ecol Sociobiol 38:207–217

    Article  Google Scholar 

  • Seppä P, Sundström L, Punttila P (1995) Facultative polygyny and habitat succession in boreal ants. Biol J Linn Soc 56:533–551

    Article  Google Scholar 

  • Snyder LE, Herbers JM (1991) Polydomy and sexual allocation ratios in the ant Myrmica punctiventris. Behav Ecol Sociobiol 28:409–415

    Article  Google Scholar 

  • Sundström L (1989) Genetic relatedness and population structure in Formica truncorum Fabr. (Hymenoptera: Formicidae). Actes Coll Insectes Soc 5:93–100

    Google Scholar 

  • Sundström L (1993) Genetic population structure and sociogenetic organization in Formica truncorum. Behav Ecol Sociobiol 33:345–354

    Google Scholar 

  • Tsutsui ND, Case TJ (2001) Population genetics and colony structure of the Argentine ant (Linepithema humile) in its native and introduced ranges. Evolution 55:976–985

    CAS  PubMed  Google Scholar 

  • Tsutsui ND, Suarez AV, Holway DA, Case TJ (2000) Reduced genetic variation and the success of invasive species. Proc Natl Acad Sci USA 97:5948–5953

    Article  CAS  PubMed  Google Scholar 

  • Tsutsui ND, Suarez AV, Grosberg-RK (2003) Genetic diversity, asymmetrical aggression, and recognition in a widespread invasive species. Proc Natl Acad Sci USA 100:1078–1083

    Article  CAS  PubMed  Google Scholar 

  • Van der Hammen T, Pedersen JS, Boomsma JJ (2002) Convergent development of low-relatedness supercolonies in Myrmica ants. Heredity 89:83–89

    Article  PubMed  Google Scholar 

  • Weir BS (1979) Inferences about linkage disequilibrium. Biometrics 35:235–254

    CAS  PubMed  Google Scholar 

  • Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370

    Google Scholar 

  • Wenseleers T, Helanterä H, Hart AG, Ratnieks FLW (2004) Worker reproduction and policing in insect societies. An ESS analysis. J Evol Biol 17:1035–1047

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We are grateful to Katja Bargum, Christine Johnson, Soile Kupiainen, Kristian Lindqvist, Petro Pynnönen, Elina Ranta, Ayman Abu Saleh and Jaime de Vizcaya for their help in the field and in the laboratory, and to Cathy Liautard, Marie-Hélène Muller, Jes Pedersen, and especially Pekka Pamilo, for fruitful discussions and comments on early versions of this paper. We also thank Niclas Gyllenstrand, Pekka Pamilo and Perttu Seppä for allowing us to perform a bottleneck analysis on their data set, Marita Rosengren for “logistic” support and three anonymous referees, whose comments greatly improved the quality of this paper. This work was funded by the Center for International Mobility of Finland (CIMO), and by the Academy of Finland (grants 42725, 173227 and 206505). Marianne Elias acknowledges the financial support provided through the European Community’s Improving Human Potential Programme under contract HPRN-CT-2000-00052, INSECTS network, and under contract HPMF-CT-2002-01781 (Marie Curie individual fellowship). The experiments carried out in this study comply with the current laws of Finland.

Author information

Authors and Affiliations

  1. Department of Biological and Environmental Sciences, University of Helsinki, P.O. Box 65, 00014 , Helsinki, Finland

    Marianne Elias, Rainer Rosengren & Liselotte Sundström

Authors
  1. Marianne Elias
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Rainer Rosengren
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Liselotte Sundström
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Marianne Elias.

Additional information

Rainer Rosengren is deceased

Communicated by R.F.A. Moritz

Rights and permissions

Reprints and permissions

About this article

Cite this article

Elias, M., Rosengren, R. & Sundström, L. Seasonal polydomy and unicoloniality in a polygynous population of the red wood ant Formica truncorum. Behav Ecol Sociobiol 57, 339–349 (2005). https://doi.org/10.1007/s00265-004-0864-8

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00265-004-0864-8

Keywords

Search

Navigation