Abstract
Only high-quality males can bear the costs of an extreme sexual display1,2,3,4. As a consequence, such males are not only more attractive, but they often live longer than average5. Recent theory predicts, however, that high-quality males should sometimes invest so heavily in sexual displays that they die sooner than lower quality males2,6,7,8,9. We manipulated the phenotypic quality of field crickets, Teleogryllus commodus, by altering the protein content of their diet. Here we show that nymphs and adult females reared on a high-protein diet lived longer than those on a low-protein diet. In contrast, adult males reared on a high-protein diet died sooner than those on low-protein diets because they invested more energy in calling during early adulthood. Our findings uphold the theoretical prediction that the relationship between longevity and sexual advertisement may be dynamic2,3,6,7,8 (that is, either positive or negative), depending on local conditions3,6 such as resource availability. Moreover, they caution the use of longevity as a proxy for fitness in sexual selection studies, and suggest avenues for future research on the relationship between sexual attractiveness and ageing.
This is a preview of subscription content, access via your institution
Access options
Subscribe to this journal
Receive 51 print issues and online access
$199.00 per year
only $3.90 per issue
Buy this article
- Purchase on Springer Link
- Instant access to full article PDF
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
References
Zahavi, A. Mate selection—a selection for a handicap. J. Theor. Biol. 53, 205–214 (1975)
Grafen, A. Biological signals as handicaps. J. Theor. Biol. 144, 517–546 (1990)
Nur, N. & Hasson, O. Phenotypic plasticity and the handicap principle. J. Theor. Biol. 110, 275–297 (1984)
Rowe, L. & Houle, D. The lek paradox and the capture of genetic variance by condition dependent traits. Proc. R. Soc. Lond. B 263, 1415–1421 (1996)
Jennions, M. D., Møller, A. P. & Petrie, M. Sexually selected traits and adult survival: a meta-analysis. Q. Rev. Biol. 76, 3–36 (2001)
Kokko, H., Brooks, R., McNamara, J. M. & Houston, A. I. The sexual selection continuum. Proc. R. Soc. Lond. B 269, 1331–1340 (2002)
Eshel, I., Volovik, I. & Sansone, E. On Fisher-Zahavi's handicapped sexy son. Evol. Ecol. Res. 2, 509–523 (2000)
Höglund, J. & Sheldon, B. C. The cost of reproduction and sexual selection. Oikos 83, 478–483 (1998)
Hansen, T. F. & Price, D. K. Good genes and old age: Do old mates provide superior genes? J. Evol. Biol. 8, 759–778 (1995)
Hunt, J., Bussière, L. F., Jennions, M. D. & Brooks, R. What is genetic quality? Trends Ecol. Evol. 19, 329–333 (2004)
Tomkins, J. L., Radwan, J., Kotiaho, J. S. & Tregenza, T. Genic capture and resolving the lek paradox. Trends Ecol. Evol. 19, 323–328 (2004)
Kotiaho, J. S., Simmons, L. W. & Tomkins, J. L. Towards a resolution of the lek paradox. Nature 410, 684–686 (2001)
Kokko, H. Good genes, old age and life-history trade-offs. Evol. Ecol. 12, 739–750 (1998)
Wagner, W. E. J. & Hoback, W. W. Nutritional effects on male calling behaviour in the variable field cricket. Anim. Behav. 57, 89–95 (1999)
Holzer, B., Jacot, A. & Brinkhof, M. W. G. Condition-dependent signaling affects male sexual attractiveness in field crickets, Gryllus campestris. Behav. Ecol. 14, 353–359 (2003)
Roff, D. A. Life History Evolution (Sinauer Associates, Sunderland, Massachusetts, 2002)
Gerhardt, H. C. & Huber, F. Acoustic Communication in Insects and Anurans (Princeton Univ. Press, Princeton, 2002)
Zuk, M. & Kolluru, G. R. Exploitation of sexual signals by predators and parasitoids. Q. Rev. Biol. 73, 415–438 (1998)
Kotiaho, J. S. Costs of sexual traits: a mismatch between theoretical considerations and empirical evidence. Biol. Rev. 76, 365–376 (2001)
Kotiaho, J. S. Testing the assumptions of conditional handicap theory: costs and condition dependence of a sexually selected trait. Behav. Ecol. Sociobiol. 48, 188–194 (2000)
Kotiaho, J., Alatalo, R. V., Mappes, J., Parri, S. & Rivero, A. Male mating success and risk of predation in a wolf spider: a balance between sexual and natural selection? J. Anim. Ecol. 67, 287–291 (1998)
Lin, S.-J. et al. Calorie restriction extends Saccharomyces cerevisiae lifespan by increasing respiration. Nature 418, 344–348 (2002)
Sohal, R. S. & Weindruch, R. Oxidative stress, caloric restriction, and aging. Science 273, 59–63 (1996)
Chippindale, A. K., Leroi, A. M., Kim, S. B. & Rose, M. R. Phenotypic plasticity and selection in Drosophila life-history evolution. I. Nutrition and the cost of reproduction. J. Evol. Biol. 6, 171–193 (1993)
Carey, J. R., Liedo, P., Müller, H.-G., Wang, J.-L. & Vaupel, J. W. Dual modes of ageing in Mediterranean fruit fly females. Science 281, 996–998 (1998)
Müller, H.-G., Wang, J.-L., Capra, W. B., Liedo, P. & Carey, J. R. Early mortality surge in protein-deprived females causes reversal of sex differential of life expectancy in Mediterranean fruit flies. Proc. Natl Acad. Sci. USA 94, 2762–2765 (1997)
Magwere, T., Chapman, T. & Partridge, L. Sex differences in the effect of dietary restriction on life span and mortality rates in female and male Drosophila melanogaster. J. Gerontol. Biol. Sci. 59A, 3–9 (2004)
Gustafsson, L., Qvarnström, A. & Sheldon, B. C. Trade-offs between life-history traits and a secondary sexual character in male collared flycatchers. Nature 375, 311–313 (1995)
Kokko, H. et al. Female choice selects for lifetime lekking performance in black grouse males. Proc. R. Soc. Lond. B 266, 2109–2115 (1999)
Candolin, U. Changes in expression and honesty of sexual signalling over the reproductive lifetime of sticklebacks. Proc. R. Soc. Lond. B 267, 2425–2430 (2000)
Acknowledgements
We are grateful to S. Bertram for advice on the construction of the call-monitoring device. Thanks to J. Evans, S. Griffith, D. Gwynne, M. Head, T. Ivy, H. Kokko, J. Kotiaho and A. Lindholm for discussions and help in the field. J.H., R.B. and M.D.J. were funded by an ARC grant and L.F.B. by a NSERC Fellowship.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Competing interests
The authors declare that they have no competing financial interests.
Supplementary information
Supplementary Methods
Further methodological information and details of statistical analyses. (DOC 122 kb)
Supplementary Tables
Four tables containing full details of statistical analyses referred to in the manuscript. (DOC 79 kb)
Rights and permissions
About this article
Cite this article
Hunt, J., Brooks, R., Jennions, M. et al. High-quality male field crickets invest heavily in sexual display but die young. Nature 432, 1024–1027 (2004). https://doi.org/10.1038/nature03084
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1038/nature03084
This article is cited by
-
Predation stress experienced as immature mites extends their lifespan
Biogerontology (2023)
-
Modeling reproductive fitness of predator, Hippodamia variegata (Coleoptera: Coccinellidae) using support vector machine (SVM) on three nitrogen treatments
Neural Computing and Applications (2023)
-
Relationships between male secondary sexual traits, physiological state and offspring viability in the three-spined stickleback
BMC Ecology and Evolution (2022)
-
A comparative study on insect longevity: tropical moths do not differ from their temperate relatives
Evolutionary Ecology (2022)
-
Encounter with heavier females changes courtship and fighting efforts of male field crickets Gryllus bimaculatus (Orthoptera: Gryllidae)
Journal of Ethology (2022)
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.