Sex-specific transcriptomic responses to changes in the nutritional environment

  1. M Florencia Camus  Is a corresponding author
  2. Matthew DW Piper
  3. Max Reuter
  1. University College London, United Kingdom
  2. Monash University, Australia

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

Article and author information

Author details

  1. 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.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0626-6865
  2. Matthew DW Piper

    School of Biological Sciences, Monash University, Melbourne, Australia
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-3245-7219
  3. 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.
    ORCID icon "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.

Reviewing Editor

  1. Laurent Keller, University of Lausanne, Switzerland

Publication history

  1. Received: March 29, 2019
  2. Accepted: August 21, 2019
  3. Accepted Manuscript published: August 22, 2019 (version 1)
  4. Version of Record published: October 1, 2019 (version 2)

Copyright

© 2019, Camus et al.

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.

Metrics

  • 3,338
    Page views
  • 455
    Downloads
  • 21
    Citations

Article citation count generated by polling the highest count across the following sources: Crossref, Scopus, PubMed Central.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. M Florencia Camus
  2. Matthew DW Piper
  3. Max Reuter
(2019)
Sex-specific transcriptomic responses to changes in the nutritional environment
eLife 8:e47262.
https://doi.org/10.7554/eLife.47262

Further reading

    1. Evolutionary Biology
    Milo S Johnson, Michael M Desai
    Research Article Updated

    As an adapting population traverses the fitness landscape, its local neighborhood (i.e., the collection of fitness effects of single-step mutations) can change shape because of interactions with mutations acquired during evolution. These changes to the distribution of fitness effects can affect both the rate of adaptation and the accumulation of deleterious mutations. However, while numerous models of fitness landscapes have been proposed in the literature, empirical data on how this distribution changes during evolution remains limited. In this study, we directly measure how the fitness landscape neighborhood changes during laboratory adaptation. Using a barcode-based mutagenesis system, we measure the fitness effects of 91 specific gene disruption mutations in genetic backgrounds spanning 8000–10,000 generations of evolution in two constant environments. We find that the mean of the distribution of fitness effects decreases in one environment, indicating a reduction in mutational robustness, but does not change in the other. We show that these distribution-level patterns result from differences in the relative frequency of certain patterns of epistasis at the level of individual mutations, including fitness-correlated and idiosyncratic epistasis.

    1. Evolutionary Biology
    2. Genetics and Genomics
    Henrike Indrischek et al.
    Research Article Updated

    Despite decades of research, knowledge about the genes that are important for development and function of the mammalian eye and are involved in human eye disorders remains incomplete. During mammalian evolution, mammals that naturally exhibit poor vision or regressive eye phenotypes have independently lost many eye-related genes. This provides an opportunity to predict novel eye-related genes based on specific evolutionary gene loss signatures. Building on these observations, we performed a genome-wide screen across 49 mammals for functionally uncharacterized genes that are preferentially lost in species exhibiting lower visual acuity values. The screen uncovered several genes, including SERPINE3, a putative serine proteinase inhibitor. A detailed investigation of 381 additional mammals revealed that SERPINE3 is independently lost in 18 lineages that typically do not primarily rely on vision, predicting a vision-related function for this gene. To test this, we show that SERPINE3 has the highest expression in eyes of zebrafish and mouse. In the zebrafish retina, serpine3 is expressed in Müller glia cells, a cell type essential for survival and maintenance of the retina. A CRISPR-mediated knockout of serpine3 in zebrafish resulted in alterations in eye shape and defects in retinal layering. Furthermore, two human polymorphisms that are in linkage with SERPINE3 are associated with eye-related traits. Together, these results suggest that SERPINE3 has a role in vertebrate eyes. More generally, by integrating comparative genomics with experiments in model organisms, we show that screens for specific phenotype-associated gene signatures can predict functions of uncharacterized genes.