Abstract
Sexual reproduction can lead to major conflicts between sexes and within genomes1,2,3,4. Here we report an extreme case of such conflicts in the little fire ant Wasmannia auropunctata. We found that sterile workers are produced by normal sexual reproduction, whereas daughter queens are invariably clonally produced. Because males usually develop from unfertilized maternal eggs in ants and other haplodiploid species, they normally achieve direct fitness only through diploid female offspring. Hence, although the clonal production of queens increases the queen's relatedness to reproductive daughters, it potentially reduces male reproductive success to zero. In an apparent response to this conflict between sexes, genetic analyses reveal that males reproduce clonally, most likely by eliminating the maternal half of the genome in diploid eggs. As a result, all sons have nuclear genomes identical to those of their father. The obligate clonal production of males and queens from individuals of the same sex effectively results in a complete separation of the male and female gene pools. These findings show that the haplodiploid sex-determination system provides grounds for the evolution of extraordinary genetic systems and new types of sexual conflict.
This is a preview of subscription content, access via your institution
Access options
Subscribe to this journal
Receive 51 print issues and online access
Buy this article
- Purchase on SpringerLink
- Instant access to the full article PDF.
USD 39.95
Prices may be subject to local taxes which are calculated during checkout



Similar content being viewed by others

Male fire ant neurotransmitter precursors trigger reproductive development in females after mating

The stony coral Fimbriaphyllia (Euphyllia) ancora’s reproductive strategy involves a sex change every year

A transcriptomic atlas of the parasitoid wasp Nasonia vitripennis across ploidy, sex, and tissue
Explore related subjects
Discover the latest articles and news in related subjects.References
Hamilton, W. D. Extraordinary sex ratios. Science 156, 477–488 (1967)
Eberhard, W. G. Evolutionary consequences of intracellular organelle competition. Q. Rev. Biol. 55, 231–249 (1980)
Hurst, L. D. Intragenomic conflict as an evolutionary force. Proc. R. Soc. Lond. B 248, 135–140 (1992)
Pomiankowski, A. in Levels of Selection in Evolution (ed. Keller, L.) 121–152 (Princeton Univ. Press, Princeton, 1999)
Hölldobler, B. & Wilson, E. O. The Ants (Springer, Berlin, 1990)
Torres, J. A., Snelling, R. R. & Canals, M. Seasonal and nocturnal periodicities in ant nuptial flights in the Tropics (Hymenoptera: Formicidae). Sociobiology 37, 601–626 (2001)
Sherman, P. W., Seeley, T. D. & Reeve, H. K. Parasites, pathogens, and polyandry in social Hymenoptera. Am. Nat. 131, 602–610 (1988)
Crozier, R. H. & Page, R. E. On being the right size: male contributions and multiple mating in social Hymenoptera. Behav. Ecol. Sociobiol. 18, 105–115 (1985)
Cole, B. J. & Wiernasz, D. C. The selective advantage of low relatedness. Science 285, 891–893 (1999)
Pearcy, M., Aron, S., Doums, C. & Keller, L. Conditional use of sex and parthenogenesis for worker and queen production in ants. Science 306, 1780–1783 (2004)
Baudry, E. et al. Whole-genome scan in thelytokous-laying workers of the Cape honeybee (Apis mellifera capensis): central fusion, reduced recombination rates and centromere mapping using half-tetrad analysis. Genetics 167, 243–252 (2004)
Koeniger, N., Hemmling, C. & Yoshida, T. Drones as sons of drones in Apis mellifera. Apidologie (Celle) 20, 391–394 (1989)
Cook, J. M. & Crozier, R. H. Sex determination and population biology in the Hymenoptera. Trends Ecol. Evol. 10, 281–286 (1995)
Simon, J.-C., Delmotte, F., Rispe, C. & Crease, T. Phylogenetic relationships between parthenogens and their sexual relatives: the possible routes to parthenogenesis in animals. Biol. J. Linn. Soc. 79, 151–163 (2003)
Normark, B. B. The evolution of alternative genetic systems in insects. Annu. Rev. Entomol. 48, 397–423 (2003)
Werren, J. H., Nur, U. & Eickbush, D. An extrachromosomal factor causing loss of paternal chromosomes. Nature 327, 75–76 (1987)
Nur, U., Werren, J. H., Eickbush, D. G., Burke, W. D. & Eickbush, T. H. A ‘selfish’ B chromosome that enhances its transmission by eliminating the paternal genome. Science 240, 512–514 (1988)
Ulloa-Chacon, P. & Cherix, D. Quelques aspects de la biologie de Wasmannia auropunctata (Roger) (Hymenoptera, Formicidae). Actes Colloq. Insectes Sociaux 4, 177–184 (1988)
Rice, W. R. Sexually antagonistic male adaptation triggered by experimental arrest of female evolution. Nature 381, 232–234 (1996)
Swanson, W. J., Yang, Z., Wolfner, M. F. & Aquadro, C. F. Positive Darwinian selection drives the evolution of several female reproductive proteins in mammals. Proc. Natl Acad. Sci. USA 98, 2509–2514 (2001)
Arnqvist, G. & Rowe, L. Antagonistic coevolution between the sexes in a group of insects. Nature 415, 787–789 (2002)
Helms-Cahan, S. & Keller, L. Complex hybrid origin of genetic caste determination in harvester ants. Nature 424, 306–309 (2003)
Parker, J. D. A major evolutionary transition to more than two sexes? Trends Ecol. Evol. 19, 83–86 (2004)
Chapuisat, M. Mating frequency of ant queens with alternative dispersal strategies, as revealed by microsatellite analysis of sperm. Mol. Ecol. 7, 1097–1105 (1998)
Fournier, D. et al. Characterization and PCR multiplexing of polymorphic microsatellite loci for the invasive ant Wasmannia auropunctata. Mol. Ecol. Notes 5, 239–242 (2005)
Raymond, M. & Rousset, F. GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J. Hered. 86, 248–249 (1995)
Page, R. D. M. TreeView: an application to display phylogenetic trees on personal computers. Comput. Appl. Biosci. 12, 357–358 (1996)
Acknowledgements
We are grateful to the Laboratoire Environment de Petit Saut (EDF-CNEH) for hosting us during field work, the Centre de Coopération Internationale en Recherche Agronomique pour le Développement (CIRAD) of French Guiana for allowing access to plantations, S. Aron for performing flow cytometry analysis, and M. Chapuisat, P. Christe, D. Haig, R. Hammond, S. Helms Cahan, K. Parker and D. Queller for comments on the manuscript. The work was supported by grants from the French Ministère de l'Écologie et du Développement Durable to A.E. and the Swiss NSF to L.K.
Author information
Denis Fournier
Present address: Behavioral and Evolutionary Ecology – CP 160/12, Université Libre de Bruxelles,, 50 avenue F. D. Roosevelt, 1050, Brussels, Belgium
Denis Fournier and Arnaud Estoup: *These authors contributed equally to this work
Authors and Affiliations
Centre de Biologie et de Gestion des Populations, INRA, Campus International de Baillarguet, CS 30 016, 34988, Montferrier/Lez Cedex, France
Denis Fournier, Arnaud Estoup & Julien Foucaud
Laboratoire Évolution et Diversité Biologique, UMR-CNRS 5174, Université Toulouse III, 118 route de Narbonne, 31062 cedex 4, Toulouse, France
Jérôme Orivel
Laboratoire de Zoologie Appliquée, IRD, 98948, Nouméa, Nouvelle-Calédonie
Hervé Jourdan
Laboratory of Sub-Tropical Zoology, University of the Ryukyus, 903-0213, Nishihara, Okinawa, Japan
Julien Le Breton
Department of Ecology and Evolution, Bâtiment de Biologie, University of Lausanne, 1015, Lausanne, Switzerland
Laurent Keller
- Denis Fournier
Search author on:PubMed Google Scholar
- Arnaud Estoup
Search author on:PubMed Google Scholar
- Jérôme Orivel
Search author on:PubMed Google Scholar
- Julien Foucaud
Search author on:PubMed Google Scholar
- Hervé Jourdan
Search author on:PubMed Google Scholar
- Julien Le Breton
Search author on:PubMed Google Scholar
- Laurent Keller
Search author on:PubMed Google Scholar
Corresponding authors
Correspondence to Denis Fournier or Arnaud Estoup.
Ethics declarations
Competing interests
Reprints and permissions information is available at npg.nature.com/reprintsandpermissions. The authors declare no competing financial interests.
Rights and permissions
About this article
Cite this article
Fournier, D., Estoup, A., Orivel, J. et al. Clonal reproduction by males and females in the little fire ant. Nature 435, 1230–1234 (2005). https://doi.org/10.1038/nature03705
Received:
Accepted:
Issue date:
DOI: https://doi.org/10.1038/nature03705
Share this article
Anyone you share the following link with will be able to read this content:
Sorry, a shareable link is not currently available for this article.
Provided by the Springer Nature SharedIt content-sharing initiative