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Extraordinary lifespans in ants: a test of evolutionary theories of ageing

Abstract

Senescence presents not only a medical problem, but also an evolutionary paradox because it should be opposed by natural selection. Evolutionary hypotheses propose that ageing evolves as the necessary cost of processes increasing early reproductive success1,2, or because of weaker selection against late-acting mutations3. A prediction of these hypotheses is that the rate of ageing should increase and the average lifespan decrease as therate of extrinsic mortality increases1,2,3,4,5,6,7. Alternatively, non-adaptive, purely mechanistic hypotheses invoke damage to DNA, cells, tissues and organs as being the unique cause of senescence and ineluctable death of organisms8. Here we show that the evolution of eusociality is associated with a 100-fold increase in insect lifespan. Such an increase is predicted by evolutionary theories because termite, bee and ant queens live in colonies that are sheltered and heavily defended against predators. Moreover, a comparison of ants with contrasting life histories also reveals an association between lifespan and extrinsic rate of mortality. Theseresults provide strong support for evolutionary theories of ageing, as purely mechanistic hypotheses of senescence do not propose any association between the rate of extrinsic mortality and lifespans.

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Figure 1: Mean lifespans of 87 solitary insect species from eight orders and 61 species of eusocial insects.
Figure 2: Average lifespans of adults from eight solitary orders of insects and queens from three eusocial insect taxa.
Figure 3: Average lifespans of ant queens in relation to their social organization.

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Acknowledgements

We thank P. Abrams, A. Bourke, W. Brown, M. Chapuisat, B. Charlesworth, M.Milinski, L. Partridge, N. Perrin, F. Ratnieks, M. Rose, K. Reeve, M. Ridley and S. Stearns for comments on the manuscript, and S. Cover for constructing the ant phylogeny. This work was funded by grants from the Swiss NSF (L.K.).

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Correspondence to Laurent Keller.

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Keller, L., Genoud, M. Extraordinary lifespans in ants: a test of evolutionary theories of ageing. Nature 389, 958–960 (1997). https://doi.org/10.1038/40130

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