Protein feeding mediates sex pheromone biosynthesis in an insect

  1. Shiyu Gui
  2. Boaz Yuval
  3. Tobias Engl
  4. Yongyue Lu
  5. Daifeng Cheng  Is a corresponding author
  1. South China Agricultural University, China
  2. Hebrew University of Jerusalem, Israel
  3. Max Planck Institute for Chemical Ecology, Germany

Abstract

Protein feeding is critical for male reproductive success in many insect species. However, how protein affects the reproduction remains largely unknown. Using Bactrocera dorsalis as the study model, we investigated how protein feeding regulated sex pheromone synthesis. We show that protein ingestion is essential for sex pheromone synthesis in male. While protein feeding or deprivation did not affect Bacillus abundance, transcriptome analysis revealed that sarcosine dehydrogenase (Sardh) in protein-fed males regulates the biosynthesis of sex pheromones by increasing glycine and threonine (sex pheromone precursors) contents. RNAi-mediated loss-of-function of Sardh decreases glycine, threonine and sex pheromone contents and results in decreased mating ability in males. The study links male feeding behavior with discrete patterns of gene expression that plays role in sex pheromone synthesis, which in turn translate to successful copulatory behavior of the males.

Data availability

All data needed to evaluate the conclusions in the paper are present in the paper and/or the Supplementary Materials. RNA-sequencing and 16S rRNA amplicon sequencing data have been deposited in the Genome Sequence Read Archive Database of the National Genomics Data Center (BioProject PRJCA010569, PRJCA010560 and PRJCA010555).

The following data sets were generated

Article and author information

Author details

  1. Shiyu Gui

    Department of Entomology, South China Agricultural University, Guanghzou, China
    Competing interests
    The authors declare that no competing interests exist.
  2. Boaz Yuval

    Department of Entomology, Hebrew University of Jerusalem, Rehovot, Israel
    Competing interests
    The authors declare that no competing interests exist.
  3. Tobias Engl

    Department of Insect Symbiosis, Max Planck Institute for Chemical Ecology, Jena, Germany
    Competing interests
    The authors declare that no competing interests exist.
  4. Yongyue Lu

    Department of Entomology, South China Agricultural University, Guanghzou, China
    Competing interests
    The authors declare that no competing interests exist.
  5. Daifeng Cheng

    Department of Entomology, South China Agricultural University, Guanghzou, China
    For correspondence
    chengdaifeng@scau.edu.cn
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0918-5913

Funding

The national natural science foundation of China (3212200346)

  • Daifeng Cheng

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

Copyright

© 2023, Gui 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

  • 1,094
    views
  • 262
    downloads
  • 10
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

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. Shiyu Gui
  2. Boaz Yuval
  3. Tobias Engl
  4. Yongyue Lu
  5. Daifeng Cheng
(2023)
Protein feeding mediates sex pheromone biosynthesis in an insect
eLife 12:e83469.
https://doi.org/10.7554/eLife.83469

Share this article

https://doi.org/10.7554/eLife.83469

Further reading

    1. Ecology
    2. Evolutionary Biology
    Rebecca D Tarvin, Jeffrey L Coleman ... Richard W Fitch
    Research Article

    Understanding the origins of novel, complex phenotypes is a major goal in evolutionary biology. Poison frogs of the family Dendrobatidae have evolved the novel ability to acquire alkaloids from their diet for chemical defense at least three times. However, taxon sampling for alkaloids has been biased towards colorful species, without similar attention paid to inconspicuous ones that are often assumed to be undefended. As a result, our understanding of how chemical defense evolved in this group is incomplete. Here, we provide new data showing that, in contrast to previous studies, species from each undefended poison frog clade have measurable yet low amounts of alkaloids. We confirm that undefended dendrobatids regularly consume mites and ants, which are known sources of alkaloids. Thus, our data suggest that diet is insufficient to explain the defended phenotype. Our data support the existence of a phenotypic intermediate between toxin consumption and sequestration — passive accumulation — that differs from sequestration in that it involves no derived forms of transport and storage mechanisms yet results in low levels of toxin accumulation. We discuss the concept of passive accumulation and its potential role in the origin of chemical defenses in poison frogs and other toxin-sequestering organisms. In light of ideas from pharmacokinetics, we incorporate new and old data from poison frogs into an evolutionary model that could help explain the origins of acquired chemical defenses in animals and provide insight into the molecular processes that govern the fate of ingested toxins.

    1. Ecology
    Mercury Shitindo
    Insight

    Tracking wild pigs with GPS devices reveals how their social interactions could influence the spread of disease, offering new strategies for protecting agriculture, wildlife, and human health.