Sex-specific transcriptomic responses to changes in the nutritional environment

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Abstract

Males and females typically pursue divergent reproductive strategies and accordingly require different dietary compositions to maximise their fitness. Here we move from identifying sex-specific optimal diets to understanding the molecular mechanisms that underlie male and female responses to dietary variation in Drosophila melanogaster. We examine male and female gene expression on male-optimal (carbohydrate-rich) and female-optimal (protein-rich) diets. We find that the sexes share a large core of metabolic genes that are concordantly regulated in response to dietary composition. However, we also observe smaller sets of genes with divergent and opposing regulation, most notably in reproductive genes which are over-expressed on each sex's optimal diet. Our results suggest that nutrient sensing output emanating from a shared metabolic machinery are reversed in males and females, leading to opposing diet-dependent regulation of reproduction in males and females. Further analysis and experiments suggest that this reverse regulation occurs within the IIS/TOR network.

Data availability

All data generated or analysed during this study are included in the supplementary datafiles.We compare our results to data from three papers, with results discussed throughout our paper.- Dobson, A.J., He, X., Blanc, E., Bolukbasi, E., Feseha, Y., Yang, M., and Piper, M.D.W. (2018). Tissue-specific transcriptome profiling of Drosophila reveals roles for GATA transcription factors in longevity by dietary restriction. Aging and Mechanisms of Disease 4, 5.- Graze, R.M., Tzeng, R.Y., Howard, T.S., and Arbeitman, M.N. (2018). Perturbation of IIS/TOR signaling alters the landscape of sex-differential gene expression in Drosophila. BMC Genomics 19, 893- Tiebe, M., Lutz, M., De La Garza, A., Buechling, T., Boutros, M., and Teleman, A.A. (2015). REPTOR and REPTOR-BP Regulate Organismal Metabolism and Transcription Downstream of TORC1. Dev Cell 33, 272-284.

The following data sets were generated

1. Camus F
2. Piper M
3. Reuter M
(2019) Data from: Sex-specific transcriptomic responses to changes in the nutritional environment
Dryad Digital Repository, doi:10.5061/dryad.2q1301v.

https://dx.doi.org/10.5061/dryad.2q1301v

Article and author information

Author details

M Florencia Camus

Research Department of Genetics, Evolution and Environment, University College London, London, United Kingdom

For correspondence
f.camus@ucl.ac.uk

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0003-0626-6865
Matthew DW Piper

School of Biological Sciences, Monash University, Melbourne, Australia

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0003-3245-7219
Max Reuter

Research Department of Genetics, Evolution and Environment, University College London, London, United Kingdom

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0001-9554-0795

Funding

European Commission (#708362)

M Florencia Camus

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Copyright

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.