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Selfish genes: a green beard in the red fire ant

Abstract

A ‘green-beard’ gene is defined as a gene that causes a phenotypic effect (such as the presence of a green beard or any other conspicuous feature), allows the bearer of this feature to recognize it in other individuals, and causes the bearer to behave differently towards other individuals depending on whether or not they possess the feature1,2,3. Such genes have been proposed on theoretical grounds to be agents mediating both altruism and intragenomic conflicts1,2, but until now few, if any, of these genes have been identified4,5. Here we provide evidence of a green-beard gene in the red imported fire ant, Solenopsis invicta. In polygyne (multiple-queen) colonies, all egg-laying queens are Bb heterozygotes at the locus Gp-9 (ref. 6). Previous studies suggested that bb females die prematurely from intrinsic causes6; we now show that BB queens initiating reproduction are killed by workers, and that it is primarily Bb rather than BB workers that are responsible for these executions. This implies that allele Gp-9b is linked to a green-beard allele that preferentially induces workers bearing the allele to kill all queens that do not bear it. Workers appear to distinguish BB from Bb queens on the basis of a transferable odour cue.

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References

  1. 1

    Hamilton, W. D. The genetical evolution of social behavior. 2. J. Theor. Biol. 7, 17–52 (1964).

    CAS  Article  Google Scholar 

  2. 2

    Dawkins, R. The Selfish Gene (Oxford University Press, New York, (1976)).

    Google Scholar 

  3. 3

    Haig, D. in Behavioural Ecology. An Evolutionary Approach (eds Krebs, J. R. & Davies, N. B.) 4th edn 284–304 (Blackwell, Oxford, (1997)).

    Google Scholar 

  4. 4

    Queller, D. J. C. Kin selection and frequency dependence: a game theoretical approach. Biol. J. Linn. Soc. 23, 133–143 (1984).

    Article  Google Scholar 

  5. 5

    Haig, D. Gestational drive and the green-bearded placenta. Proc. Natl Acad. Sci. USA 93, 6547–6551 (1996).

    ADS  CAS  Article  Google Scholar 

  6. 6

    Ross, K. G. Multilocus evolution in fire ants—effects of selection, gene flow and recombination. Genetics 145, 961–974 (1997).

    CAS  PubMed  PubMed Central  Google Scholar 

  7. 7

    Keller, L. & Ross, K. G. Phenotypic basis of reproductive success in a social insect: genetic and social determinants. Science 260, 1107–1110 (1993).

    ADS  CAS  Article  Google Scholar 

  8. 8

    Willer, D. E. & Fletcher, D. J. C. Differences in inhibitory capability among queens of the ant Solenopsis invicta. Physiol. Entomol. 11, 475–482 (1986).

    Article  Google Scholar 

  9. 9

    Fletcher, D. J. C. & Blum, M. S. Regulation of queen number by workers in colonies of social insects. Science 219, 312–314 (1983).

    ADS  CAS  Article  Google Scholar 

  10. 10

    Ross, K. G. Strong selection on a gene that influences reproductive competition in a social insect. Nature 355, 347–349 (1992).

    ADS  Article  Google Scholar 

  11. 11

    Ross, K. G., Vargo, E. L. & Keller, L. Simple genetic basis for important social traits in the fire ant Solenopsis invicta. Evolution 50, 2387–2399 (1996).

    Article  Google Scholar 

  12. 12

    Vargo, E. L. & Fletcher, D. J. C. On the relationship between queen number and fecundity in polygynous colonies of the fire ant, Solenopsis invicta. Physiol. Entomol. 14, 223–232 (1989).

    Article  Google Scholar 

  13. 13

    Ridley, M. & Grafen, A. Are green beard genes outlaws? Anim. Behav. 29, 954–955 (1981).

    Article  Google Scholar 

  14. 14

    Wade, M. J. & Beeman, R. W. The population dynamics of maternal-effect selfish genes. Genetics 138, 1309–1314 (1994).

    CAS  PubMed  PubMed Central  Google Scholar 

  15. 15

    Wilson, D. S. & Dugatkin, L. Nepotism vs TFT or why should you be nice to your rotten brother? Evol. Ecol. 5, 291–299 (1991).

    Article  Google Scholar 

  16. 16

    Durand, D., Ardlie, K., Buttel, L., Levin, S. A. & Silver, L. M. Impact of migration and fitness on the stability of lethal t-haplotype polymorphism in Mus musculus: a computer study. Genetics 145, 1093–1108 (1997).

    CAS  PubMed  PubMed Central  Google Scholar 

  17. 17

    Silver, L. M. The peculiar journey of a selfish chromosome: mouse t haplotypes and meiotic drive. Genetics 9, 250–254 (1993).

    CAS  Google Scholar 

  18. 18

    Sokal, R. R. & Rohlf, F. J. Biometry. The Principles and Practice of Statistics in Biological Research3rd edn (Freeman, San Francisco, (1995)).

    MATH  Google Scholar 

  19. 19

    Glancey, B. M., Vandenburgh, M. K. & St Romain, M. K. Testis degeneration in the imported fire ant, Solenopsis invicta. J. Georgia Entomol. Soc. 2, 83–88 (1976).

    Google Scholar 

  20. 20

    Keller, L. & Ross, K. G. Phenotypic plasticity and cultural transmission of alternative reproductive strategies in the fire ant Solenopsis invicta. Behav. Ecol. Sociobiol. 33, 121–129 (1993).

    Google Scholar 

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Acknowledgements

We thank A. Bourke, C. DeHeer, J. Evans, M. Goodisman, D. Haig, L. Hurst and D.Queller for comments on the manuscript. This work was funded by grants from the Swiss and US National Science Foundations and the National Geographic Society.

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Correspondence to Laurent Keller.

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Keller, L., Ross, K. Selfish genes: a green beard in the red fire ant. Nature 394, 573–575 (1998). https://doi.org/10.1038/29064

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