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Worker senescence and the sociobiology of aging in ants

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Abstract

Senescence, the decline in physiological and behavioral function with increasing age, has been the focus of significant theoretical and empirical research in a broad array of animal taxa. Preeminent among invertebrate social models of aging are ants, a diverse and ecologically dominant clade of eusocial insects characterized by reproductive and sterile phenotypes. In this review, we critically examine selection for worker life span in ants and discuss the relationship between functional senescence, longevity, task performance, and colony fitness. We did not find strong or consistent support for the hypothesis that demographic senescence in ants is programmed, or its corollary prediction that workers that do not experience extrinsic mortality die at an age approximating their life span in nature. We present seven hypotheses concerning how selection could favor extended worker life span through its positive relationship to colony size and predict that large colony size, under some conditions, should confer multiple and significant fitness advantages. Fitness benefits derived from long worker life span could be mediated by increased resource acquisition, efficient division of labor, accuracy of collective decision-making, enhanced allomaternal care and colony defense, lower infection risk, and decreased energetic costs of workforce maintenance. We suggest future avenues of research to examine the evolution of worker life span and its relationship to colony fitness and conclude that an innovative fusion of sociobiology, senescence theory, and mechanistic studies of aging can improve our understanding of the adaptive nature of worker life span in ants.

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Acknowledgments

We thank Drs. Mario Muscedere, Wulfila Gronenberg, Kimberly McCall, and Karen Warkentin, as well as two anonymous reviewers and Dr. Olav Rueppell, for their critical reading of the manuscript. Andrew Hoadley, J. Frances Kamhi, Darcy G. Gordon, and Jake Uminski provided helpful discussions and suggestions. YMG was supported by the National Institute on Aging of the National Institutes of Health (grant F31AG041589) and the National Science Foundation (grant IOB 0725013; JFT sponsor for both awards). The work presented here is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health.

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  1. Ysabel Milton Giraldo

    Present address: Department of Neurobiology, Harvard Medical School, 220 Longwood Ave., Boston, MA, 02115, USA

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  1. Department of Biology, Boston University, 5 Cummington Mall, Boston, MA, 02215, USA

    Ysabel Milton Giraldo & James F. A. Traniello

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  1. Ysabel Milton Giraldo
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Correspondence to Ysabel Milton Giraldo.

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Communicated by O. Rueppell

This paper is dedicated to the memory of Professor Henry Hagedorn, mentor, colleague, and friend, and his generous spirit.

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Giraldo, Y.M., Traniello, J.F.A. Worker senescence and the sociobiology of aging in ants. Behav Ecol Sociobiol 68, 1901–1919 (2014). https://doi.org/10.1007/s00265-014-1826-4

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