Article

Perceptive costs of reproduction drive ageing and physiology in male Drosophila

  • Nature Ecology & Evolution 1, Article number: 0152 (2017)
  • doi:10.1038/s41559-017-0152
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Abstract

Costs of reproduction are thought to result from natural selection optimizing organismal fitness within putative physiological constraints. Phenotypic and population genetic studies of reproductive costs are plentiful across taxa, but an understanding of their mechanistic basis would provide important insight into the diversity in life-history traits, including reproductive effort and ageing. Here, we dissect the causes and consequences of specific costs of reproduction in male Drosophila melanogaster. We find that key survival and physiological costs of reproduction arise from perception of the opposite sex, and they are reversed by the act of mating. In the absence of pheromone perception, males are free from reproductive costs on longevity, stress resistance and fat storage. The costs of perception and the benefits of mating are both mediated by evolutionarily conserved neuropeptidergic signalling molecules, as well as the transcription factor dFoxo. These results provide a molecular framework in which certain costs of reproduction arise as a result of self-imposed ‘decisions’ in response to perceptive neural circuits, which then orchestrate the control of life-history traits independently of physical or energetic effects associated with mating itself.

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Acknowledgements

Members of the Pletcher laboratory provided comments on the experimental design and analysis. This research was supported by the US National Institutes of Health (R01AG030593 and R01AG051649 to S.D.P., R01AG049494 to D.E.L.P., and R01GM102279 to S.D.P and D.E.L.P.), the Glenn Medical Foundation (to S.D.P.), a Ruth L. Kirschstein National Research Service Award from NIA (F30AG048661, to Z.M.H.) and the University of Michigan Systems Biology Training Grant (T32GM008322, to Z.M.H.).

Author information

Affiliations

  1. Department of Molecular & Integrative Physiology, University of Michigan, Ann Arbor, Michigan 48109, USA.

    • Zachary M. Harvanek
    • , Yang Lyu
    • , Christi M. Gendron
    • , Jacob C. Johnson
    •  & Scott D. Pletcher
  2. Medical Scientist Training Program, University of Michigan, Ann Arbor, Michigan 48109, USA.

    • Zachary M. Harvanek
  3. Genetic Strains Research Center, National Institute of Genetics, Mishima, Shizuoka 411-8540, Japan.

    • Shu Kondo
  4. Department of Pathology, University of Washington, Seattle, Washington 98195, USA.

    • Daniel E. L. Promislow
  5. Department of Biology, University of Washington, Seattle, Washington 98195, USA.

    • Daniel E. L. Promislow
  6. Geriatrics Center, University of Michigan, Ann Arbor, Michigan 48109, USA.

    • Scott D. Pletcher

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Contributions

Z.M.H. and S.D.P. conceptualized the project, and Z.M.H., Y.L., D.E.L.P. and S.D.P. designed the experiments. Z.M.H., C.M.G. and J.C.J. performed the in vivo experiments, and Z.M.H., C.M.G. and S.D.P. analysed them. D.E.L.P. performed the metabolomics. Y.L. and S.D.P. analysed the metabolomics data, with input from Z.M.H. and D.E.L.P. S.K. created the NPF mutant used in Fig. 3. Z.M.H., Y.L. and S.D.P. wrote the manuscript, with comments from C.M.G. and D.E.L.P.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Scott D. Pletcher.

Supplementary information

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    Supplementary Information

    Supplementary Figures 1–8; Supplementary Tables 1,2

Excel files

  1. 1.

    Supplementary File 1

    Neurometabolomic dataset