Eur. J. Entomol. 114: 249-256, 2017 | DOI: 10.14411/eje.2017.030

Sexual dimorphism in the Drosophila melanogaster (Diptera: Drosophilidae) metabolome increases throughout development

Fiona C. INGLEBY, Edward H. MORROW*
Evolution, Behaviour and Environment Group, School of Life Sciences, University of Sussex, John Maynard Smith Building, Falmer, Brighton, UK; e-mails: f.ingleby@sussex.ac.uk, ted.morrow@sussex.ac.uk

The expression of sexually dimorphic phenotypes from a shared genome between males and females is a longstanding puzzle in evolutionary biology. Increasingly, research has made use of transcriptomic technology to examine the molecular basis of sexual dimorphism through gene expression studies, but even this level of detail misses the metabolic processes that ultimately link gene expression with the whole organism phenotype. We use metabolic profiling in Drosophila melanogaster to complete this missing step, with a view to examining variation in male and female metabolic profiles, or metabolomes, throughout development. We show that the metabolome varies considerably throughout larval, pupal and adult stages. We also find significant sexual dimorphism in the metabolome, although only in pupae and adults, and the extent of dimorphism increases throughout development. We compare this to transcriptomic data from the same population and find that the general pattern of increasing sex differences throughout development is mirrored in RNA expression. We discuss our results in terms of the usefulness of metabolic profiling in linking genotype and phenotype to more fully understand the basis of sexually dimorphic phenotypes.

Keywords: Diptera, Drosophilidae, Drosophila melanogaster; metabolome, ontogeny, sexual dimorphism, transcriptome

Received: May 3, 2017; Accepted: May 13, 2017; Revised: May 13, 2017; Published online: May 23, 2017Show citation

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INGLEBY, F.C., & MORROW, E.H. (2017). Sexual dimorphism in the Drosophila melanogaster (Diptera: Drosophilidae) metabolome increases throughout development. Eur. J. Entomol.,114(1),2017.000. doi:10.14411/eje.2017.030.
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References

  1. Baldwin J.E. & Krebs H. 1981: The evolution of metabolic cycles. - Nature 291: 381-382. Go to original source...
  2. Callier V., Hand S.C., Campbell J.B., Biddulph T. & Harrison J.F. 2016: Developmental changes in hypoxic exposure and responses to anoxia in Drosophila melanogaster. - J. Exp. Biol. 218: 2927-2934. Go to original source...
  3. Chintapalli V.R., Bratty M.A., Korzekwa D., Watson D.G. & Dow J.A.T. 2013: Mapping an atlas of tissue-specific Drosophila melanogaster metabolomes by high resolution mass spectrometry. - PLoS One 8: e78066, 13 pp. Go to original source...
  4. Colinet H., Larvor V., Laparie M. & Renault D. 2012: Exploring the plastic response to cold acclimation through metabolomics. - Funct. Ecol. 26: 711-722. Go to original source...
  5. Darwin C. 1871: The Descent of Man and Selection in Relation to Sex. John Murray, London, 690 pp.
  6. Dean C.A.E., Teets N.M., Kostal V., Simek P. & Denlinger D.L. 2016: Enhanced stress responses and metabolic adjustments linked to diapause and onset of migration in the large milkweed bug. - Physiol. Entomol. 41: 152-161. Go to original source...
  7. Ellegren H. & Parsch J. 2007: The evolution of sex-biased genes and sex-biased gene expression. - Nat. Rev. 8: 689-698. Go to original source...
  8. Hadfield J.D. 2010: MCMC methods for multi-response generalised linear mixed models: the MCMCglmm R package. - J. Stat. Software 33: 1-22. Go to original source...
  9. Hahn D.A. & Denlinger D.L. 2007: Meeting the energetic demands of insect diapause: nutrient storage and utilization. - J. Insect Physiol. 53: 760-773. Go to original source...
  10. Hoffmann J.M., Soltow Q.A., Li S., Sidik A., Jones D.P. & Promislow D.E.L. 2014: Effects of age, sex, and genotype on high-sensitivity metabolomics profiles in the fruit fly, Drosophila melanogaster. - Aging Cell 13: 596-604. Go to original source...
  11. Ingleby F.C., Flis I. & Morrow E.H. 2015: Sex-biased gene expression and sexual conflict throughout development. - Cold Spring Harbor Persp. Biol. 7: a017632, 18 pp. Go to original source...
  12. Ingleby F.C., Webster C.L., Pennell T.M., Flis I. & Morrow E.H. 2016: Sex-biased gene expression in Drosophila melanogaster is constrained by ontogeny and genetic architecture. - BioRxiv unpublished pre-print, doi: http://dx.doi.org/10.1101/034728, 36 pp. Go to original source...
  13. Innocenti P. & Morrow E.H. 2010: The sexually antagonistic genes of Drosophila melanogaster. - PLoS Biol. 8: e1000335, 10 pp. Go to original source...
  14. Kochhar S., Jacobs D.M., Ramadan Z., Berruex F., Fuerholz A. & Fay L.B. 2006: Probing gender-specific metabolism in humans by nuclear magnetic resonance-based metabonomics. - Anal. Biochem. 352: 274-281. Go to original source...
  15. Kostal V., Korbelova J., Rozsypal J., Zahradnickova H., Cimlova J., Tomcala A. & Simek P. 2011: Long-term cold acclimation extends survival time at 0C and modifies the metabolomics profiles of the larvae of the fruit fly Drosophila melanogaster. - PLoS One 9: e25025, 10 pp. Go to original source...
  16. Lande R. 1980: Sexual dimorphism, sexual selection, and adaptation to polygenic characters. - Evolution 34: 292-305. Go to original source...
  17. Laye M.J., Tran V., Jones D.P., Kapahi P. & Promislow D.E.L. 2015: The effects of age and dietary restriction on the tissue-specific metabolome of Drosophila. - Aging Cell 14: 797-808. Go to original source...
  18. Li Y., Zhang L., Chen H., Kostal V., Simek P., Moos M. & Denlinger D.L. 2015: Shifts in metabolomics profiles of the parasitoid Nasonia vitripennis associated with elevated cold tolerance induced by the parasitoid's diapause, host diapause and host diet augmented with proline. - Insect Biochem. Mol. Biol. 63: 34-46. Go to original source...
  19. Magnusson K., Mendes A.M., Windbichler N., Papathanos P.A., Nolan T., Dottorini T., Rizzi E., Christophides G.K. & Crisanti A. 2011: Transcription regulation of sex-biased genes during ontogeny in the malaria vector Anopheles gambiae. - PLoS One 6: e21572, 11 pp. Go to original source...
  20. Michaud M.R. & Denlinger D.L. 2007: Shifts in the carbohydrate, polyol, and amino acid pools during rapid cold-hardening and diapause-associated cold-hardening in flesh flies: a metabolomic comparison. - J. Compar. Physiol. (B) 177: 753-763. Go to original source...
  21. Overgaard J., Malmendal A., Sorensen J.G., Bundy J.G., Loeschcke V., Nielsen N.C. & Homstrup M. 2007: Metabolomic profiling of rapid cold hardening and cold shock in Drosophila melanogaster. - J. Insect Physiol. 53: 1218-1232. Go to original source...
  22. Pawlowsky-Glahn V. & Buccianti A. 2011: Compositional Data Analysis: Theory and Applications. John Wiley & Sons, London, 378 pp.
  23. Perry J.C., Harrison P.W. & Mank J.E. 2014: The ontogeny and evolution of sex-biased gene expression in Drosophila melanogaster. - Mol. Biol. Evol. 31: 1206-1219. Go to original source...
  24. Sarup P., Pedersen S.M.M., Nielsen N.C., Malmendal A. & Loeschcke V. 2012: The metabolic profile of long-lived Drosophila melanogaster. - PLoS One 7: e47461, 11 pp. Go to original source...
  25. Suhre K., Shin S.Y., Petersen A.K., Mohney R.P., Meredith D., Wagele B., Altmaier E., CARDIoGRAM, Deloukas P., Erdmann J. et al. 2011: Human metabolic individuality in biomedical and pharmaceutical research. - Nature 477: 54-60. Go to original source...
  26. Williams S., Dew-Budd K., Davis K., Anderson J., Bishop R., Freeman K., Davis D., Bray K., Perkins L., Hubickey J. et al. 2015: Metabolomic and gene expression profiles exhibit modular genetic and dietary structure linking metabolic syndrome phenotypes in Drosophila. - G3 5: 2817-2829.
  27. Zhao M., Zha X.F., Liu J., Zhang W.J., He N.J., Cheng D.J., Dai Y., Xiang Z.H. & Xia Q.Y. 2011: Global expression profile of silkworm genes from larval to pupal stages: toward a comprehensive understanding of sexual differences. - Insect Sci. 18: 607-618. Go to original source...

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