1. Evolutionary Biology
  2. Genetics and Genomics
Download icon

Reproduction: How flies turn food into progeny

  1. Thomas Flatt  Is a corresponding author
  1. University of Fribourg, Switzerland
Insight
  • Cited 1
  • Views 1,063
  • Annotations
Cite this article as: eLife 2019;8:e51289 doi: 10.7554/eLife.51289

Abstract

Sex-optimal diets have different effects on gene expression in female and male flies.

Main text

Females and males have evolved different strategies to achieve the same goal: making babies. For example, males usually produce a large number of cheap sperm cells and often display traits that help to maximize the number of successful matings. Females, on the other hand, tend to 'go for quality' by producing a small number of relatively large eggs (each of which requires a lot of energy to produce), and exhibit traits that help them maximize their 'return on investment’. It is thus not surprising that females and males require different diets to maximize their progeny. In various insects, for instance, females rely mainly on protein intake to fuel egg production, whereas males use a higher proportion of carbohydrates to optimize their Darwinian fitness (Lee et al., 2008; Maklakov et al., 2008; Jensen et al., 2015; Camus et al., 2017).

A growing body of work is dedicated to studying the specific dietary requirements that maximize reproductive success of each sex, but the underlying molecular and physiological mechanisms remain poorly understood, especially in males. Now, in eLife, Florencia Camus and Max Reuter from University College London, and Matthew Piper from Monash University, report the results of experiments on the fruit fly Drosophila melanogaster which show that male and female flies modify the expression of certain genes differently in response to changes in their diet (Camus et al., 2019).

Camus et al. fed the flies a diet that was reproductively optimal either for their own sex or for the other sex, and then sequenced the RNA of these flies. Comparing the results for female and male flies revealed that different genes had distinct responses to the two diets (Figure 1). Many metabolic or ‘core’ genes had similar expression patterns in female and male flies. However, several smaller groups of genes had transcriptional responses that were sex-specific. These groups include genes that only respond to changes in diet in one sex, and genes that exhibit opposite (antagonistic) responses to the same dietary change in male and female flies.

Gene expression responses to changes in diet in female and male fruit flies.

Camus et al. examined gene expression in female and male flies given a protein-rich diet (which is optimal for egg production) and a carbohydrate-rich diet (which is optimal for sperm production). Many metabolic genes (‘core genes’) displayed similar responses to diet in both female and male flies (bottom left). A smaller group of genes – including a number of reproductive genes – showed clear-cut differences in expression for each diet depending on sex, with some exhibiting antagonistic behaviors in the two sexes (bottom right). Further analyses revealed that this sex-opposite regulation occurs within the IIS/TOR signaling network.

Among the genes that responded to diet in just one sex, Camus et al. identified genes involved in egg production and hormonal regulation in females, and genes responsible for sperm function in males. One prominent example in this category is doublesex, a well-known regulator of sexual differentiation and sex-specific behavior, which showed higher expression in females fed a high-protein diet. Genes with antagonistic responses in males and females include fit (female-specific independent of transformer), a gene that is upregulated in male flies during courtship and mating. Moreover, the transcripts that showed antagonistic responses between the sexes were enriched for GATA transcription factors which have previously been implicated in nutritional responses (including dietary restriction) and reproductive physiology.

Comparing these results to previously published datasets (Tiebe et al., 2015; Graze et al., 2018) provided compelling bioinformatic evidence that the IIS/TOR signaling network (short for the insulin/insulin-like growth factor signaling/target of rapamycin signaling network) is involved in reproduction. This is particularly interesting given growing evidence that IIS/TOR signaling plays an important role in regulating traits and processes that vary between the sexes. For example, using transcriptional profiling of virgin flies, it has been shown that reducing insulin signaling increases the differences in expression of IIS core pathway genes between the sexes (Graze et al., 2018). The work by Camus et al. makes a significant advance in this area by establishing profound connections between sex-specific dietary optima for reproduction and sex-specific expression changes in IIS/TOR.

To further corroborate the IIS/TOR connection, Camus et al. inhibited TOR signaling with the antagonist rapamycin, leading to disproportionately deleterious effects on reproductive performance when male or female flies were fed their sex-optimal diet. This suggests that TOR signaling is required for the increased reproductive performance conferred by the different diets. These results are consistent with the idea that nutrient-sensing signals mediated by IIS/TOR signaling are somehow inverted between females and males. It will be a fascinating task for future work to uncover how the nutritional signaling inputs into the IIS/TOR network are modulated in a sex-specific way to optimize each sex's reproductive performance.

Together, the results reported by Camus et al. provide fertile ground for future experiments to dissect the mechanisms that underpin sex-specific links between diet, nutrient sensing, metabolism and reproduction.

References

Article and author information

Author details

  1. Thomas Flatt

    Thomas Flatt is in the Department of Biology, University of Fribourg, Fribourg, Switzerland

    For correspondence
    thomas.flatt@unifr.ch
    Competing interests
    No competing interests declared
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5990-1503

Publication history

  1. Version of Record published: October 1, 2019 (version 1)

Copyright

© 2019, Flatt

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

Metrics

  • 1,063
    Page views
  • 86
    Downloads
  • 1
    Citations

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

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)

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

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

Further reading

    1. Evolutionary Biology
    2. Neuroscience
    Lucia L Prieto-Godino et al.
    Research Article

    Olfactory receptor repertoires exhibit remarkable functional diversity, but how these proteins have evolved is poorly understood. Through analysis of extant and ancestrally-reconstructed drosophilid olfactory receptors from the Ionotropic receptor (Ir) family, we investigated evolution of two organic acid-sensing receptors, Ir75a and Ir75b. Despite their low amino acid identity, we identify a common 'hotspot' in their ligand-binding pocket that has a major effect on changing the specificity of both Irs, as well as at least two distinct functional transitions in Ir75a during evolution. Moreover, we show that odor specificity is refined by changes in additional, receptor-specific sites, including those outside the ligand-binding pocket. Our work reveals how a core, common determinant of ligand-tuning acts within epistatic and allosteric networks of substitutions to lead to functional evolution of olfactory receptors.

    1. Evolutionary Biology
    Chenlu Di et al.
    Research Article Updated

    Advances in genome sequencing have improved our understanding of the genetic basis of human diseases, and thousands of human genes have been associated with different diseases. Recent genomic adaptation at disease genes has not been well characterized. Here, we compare the rate of strong recent adaptation in the form of selective sweeps between mendelian, non-infectious disease genes and non-disease genes across distinct human populations from the 1000 Genomes Project. We find that mendelian disease genes have experienced far less selective sweeps compared to non-disease genes especially in Africa. Investigating further the possible causes of the sweep deficit at disease genes, we find that this deficit is very strong at disease genes with both low recombination rates and with high numbers of associated disease variants, but is almost non-existent at disease genes with higher recombination rates or lower numbers of associated disease variants. Because segregating recessive deleterious variants have the ability to interfere with adaptive ones, these observations strongly suggest that adaptation has been slowed down by the presence of interfering recessive deleterious variants at disease genes. These results suggest that disease genes suffer from a transient inability to adapt as fast as the rest of the genome.