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Clonal reproduction by males and females in the little fire ant

Nature volume 435, pages 1230–1234 (2005)Cite this article

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.

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Figure 1: Site and nest locations.
Figure 2: Neighbour-joining dendrogram of the genetic (allele-shared) distances between queens (Q), gynes (G) and male sperms (M) collected over all the five sites (A–E).
Figure 3

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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.

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Author notes

  1. Denis Fournier

    Present address: Behavioral and Evolutionary Ecology – CP 160/12, Université Libre de Bruxelles,, 50 avenue F. D. Roosevelt, 1050, Brussels, Belgium

  2. Denis Fournier and Arnaud Estoup: *These authors contributed equally to this work

Authors and Affiliations

  1. 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

  2. Laboratoire Évolution et Diversité Biologique, UMR-CNRS 5174, Université Toulouse III, 118 route de Narbonne, 31062 cedex 4, Toulouse, France

    Jérôme Orivel

  3. Laboratoire de Zoologie Appliquée, IRD, 98948, Nouméa, Nouvelle-Calédonie

    Hervé Jourdan

  4. Laboratory of Sub-Tropical Zoology, University of the Ryukyus, 903-0213, Nishihara, Okinawa, Japan

    Julien Le Breton

  5. Department of Ecology and Evolution, Bâtiment de Biologie, University of Lausanne, 1015, Lausanne, Switzerland

    Laurent Keller

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Correspondence to Denis Fournier or Arnaud Estoup.

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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

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