Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Disposable-soma senescence mediated by sexual selection in an ungulate

Abstract

Senescence may result from an optimal balance between current reproductive investment and bodily repair processes required for future reproduction1, a theoretical prediction difficult to prove especially in large, long-lived animals. Here we propose that teeth that have fixed dimensions early in life, but that wear during chewing, can be taken as a measure of total lifetime ‘repair’, and their wear rate as a measure of current expenditure in performance. Our approach also considers the sexual selection process to investigate the advance of senescence in males compared with females, when selection favouring competition over mates reduces the reproductive lifespan of males2. We studied carcasses of 2,141 male and 739 female red deer (Cervus elaphus) of different ages, finding that male molariform teeth emerged at a far smaller size than expected from body size dimorphism. This led to higher workload, steeper wear rate and earlier depletion of male teeth than in females, in concordance with sex-specific patterns of lifetime performance and reproduction. These findings provide the empirical support for the disposable-soma hypothesis of senescence3, which predicts that investment in bodily repair will decrease when the return from this investment may not be realized as a result of other causes that limit survival or reproduction.

This is a preview of subscription content, access via your institution

Relevant articles

Open Access articles citing this article.

Access options

Buy article

Get time limited or full article access on ReadCube.

$32.00

All prices are NET prices.

Figure 1: Performance and tooth wear throughout life in males and females.
Figure 2: Sexual dimorphism (male/female ratio, standardized; see Methods), for different dental (open bars) and body size (filled bars) traits.
Figure 3: Postcanine working areas and wear.

References

  1. Kirkwood, T. B. L. & Austad, S. N. Why do we age? Nature 408, 233–238 (2000)

    Article  ADS  CAS  Google Scholar 

  2. Andersson, M. Sexual Selection (Princeton Univ. Press, Princeton, New Jersey, 1994)

    Google Scholar 

  3. Kirkwood, T. B. L. in Handbook of the Biology of Ageing (eds Finch, C. E. & Schneider, E. L.) 27–44 (Van Nostrand Reinhold, New York, 1985)

    Google Scholar 

  4. Medawar, P. B. Old age and natural death. Mod. Q. 1, 30–56 (1946)

    Google Scholar 

  5. Edney, R. B. & Gill, R. W. Evolution of senescence and specific longevity. Nature 220, 281–282 (1968)

    Article  ADS  CAS  Google Scholar 

  6. Williams, G. C. Pleiotropy, natural selection and the evolution of senescence. Evolution 11, 398–411 (1957)

    Article  Google Scholar 

  7. Hamilton, W. D. The moulding of senescence by natural selection. J. Theor. Biol. 12, 12–45 (1966)

    Article  CAS  Google Scholar 

  8. Rose, M. R. Evolutionary Biology of Aging (Oxford Univ. Press, New York, 1991)

    Google Scholar 

  9. Kirkwood, T. B. L. & Rose, M. R. Evolution of senescence: late survival sacrificed for reproduction. Phil. Trans. R. Soc. Lond. B 332, 15–24 (1991)

    Article  ADS  CAS  Google Scholar 

  10. Haldane, J. B. S. New Paths in Genetics (Allen & Unwin, London, 1941)

    Google Scholar 

  11. Ricklefs, R. E. Evolutionary theories of ageing: confirmation of a fundamental prediction, with implications for the genetic basis and evolution of lifespan. Am. Nat. 152, 24–44 (1998)

    Article  CAS  Google Scholar 

  12. Tyler, N. J. C. Natural Limitation of the Abundance of the High Arctic Svalbard Reindeer. Thesis, Univ. Cambridge (1987)

    Google Scholar 

  13. Skogland, T. Tooth wear by food limitation and its life history consequences in wild reindeer. Oikos 51, 238–242 (1988)

    Article  Google Scholar 

  14. Gaillard, J.-M., Delorme, D., Boutin, J.-M., Van Laere, G. & Pradel, R. Roe deer survival patterns: a comparative analysis of contrasting populations. J. Anim. Ecol. 62, 778–791 (1993)

    Article  Google Scholar 

  15. Ericsson, G. & Wallin, K. Age-specific moose (Alces alces) mortality in a predator-free environment: evidence for senescence in females. Ecoscience 8, 157–163 (2001)

    Article  Google Scholar 

  16. Loe, L. E., Mysterud, A., Langvatn, R. & Stenseth, N. C. Decelerating and sex-dependent tooth wear in Norwegian red deer. Oecologia 135, 346–353 (2003)

    Article  ADS  Google Scholar 

  17. Clutton-Brock, T. H., Albon, S. D. & Guinness, F. E. in Reproductive Success (ed. Clutton-Brock, T. H.) 325–343 (Chicago Univ. Press, Chicago, 1988)

    Google Scholar 

  18. Gompertz, B. On the nature of the function expressive of the law of human mortality and on the new mode of determining life contingencies. Phil. Trans. R. Soc. Lond. 115, 513–585 (1825)

    Article  ADS  Google Scholar 

  19. Clutton-Brock, T. H., Guinness, F. E. & Albon, S. D. Red Deer. Behaviour and Ecology of Two Sexes (Edinburgh Univ. Press, Edinburgh, 1982)

    Google Scholar 

  20. Mysterud, A., Yoccoz, N. G., Stenseth, N. C. & Langvatn, R. Effects of age, sex, and density on body weight of Norwegian red deer: evidence of density-dependence senescence. Proc. R. Soc. Lond. B 268, 911–919 (2001)

    Article  CAS  Google Scholar 

  21. Fortelius, M. Ungulate cheek teeth: developmental, functional, and evolutionary interrelations. Acta Zool. Fenn. 180, 1–76 (1985)

    Google Scholar 

  22. Lucas, P. W. Dental Functional Morphology (Cambridge Univ. Press, Cambridge, 2004)

    Book  Google Scholar 

  23. Staines, B. W. & Crisp, J. M. Observations on food quality in Scottish red deer (Cervus elaphus) as determined by chemical analysis of the rumen contents. J. Zool. 185, 253–259 (1978)

    Google Scholar 

  24. Clutton-Brock, T. H., Iason, G. R. & Guinness, F. E. Sexual segregation and density related changes in habitat use in female and male red deer (Cervus elaphus L.). J. Zool. 211, 275–289 (1987)

    Article  Google Scholar 

  25. Mysterud, A. The relationship between ecological segregation and sexual body-size dimorphism in large herbivores. Oecologia 124, 40–54 (2000)

    Article  ADS  CAS  Google Scholar 

  26. Conradt, L., Gordon, I. J., Clutton-Brock, T. H., Thomson, D. & Guinness, F. E. Could the indirect competition hypothesis explain inter-sexual site segregation in red deer (Cervus elaphus L.)? J. Zool. 254, 285–293 (2001)

    Article  Google Scholar 

  27. Bonenfant, C., Gaillard, J.-M., Loison, A. & Klein, F. Sex-ratio variation and reproductive costs in relation to density in a forest-dwelling population of red deer. Behav. Ecol. 14, 862–869 (2003)

    Article  Google Scholar 

  28. Mitchell, B. Growth layers in dental cement for determining the age of red deer (Cervus elaphus L.). J. Anim. Ecol. 36, 279–293 (1967)

    Article  Google Scholar 

Download references

Acknowledgements

We thank T. Kirkwood, P. W. Lucas, A. Mysterud and J. Pérez-Barbería for comments; R. Álvarez, L. Castillo, P. Cidoncha, A. Flores, B. Gutiérrez, J. G. Martínez, Y. Moreno, S. del Río and B. Sánchez for help in field and laboratory work, the Dirección General de Medio Ambiente of Extremadura for permissions and facilities, and J. A. Campón for allowing data and sample collection. Financial support came from Spanish Ministry of Science, FEDER and Junta de Extremadura (Consejería de Agricultura y Medio Ambiente, and Consejería de Educación Ciencia y Tecnología). C.B.S.P. and S.A. were supported by a predoctoral grant of the Autonomic Government of Extremadura.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Juan Carranza.

Ethics declarations

Competing interests

The authors declare that they have no competing financial interests.

Supplementary information

Supplementary Table 1

Relationships of dental variables and body size variables with age in males and females. Equations of regression lines were used to obtain maximum trait values in males and females to estimate sexual dimorphism (see Methods). (DOC 23 kb)

Supplementary Figure 1

Variation of the index of workload on occlusal surface areas of postcanine teeth along age for males and females. (DOC 54 kb)

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Carranza, J., Alarcos, S., Sánchez-Prieto, C. et al. Disposable-soma senescence mediated by sexual selection in an ungulate. Nature 432, 215–218 (2004). https://doi.org/10.1038/nature03004

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nature03004

This article is cited by

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing