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.

Reviewing Editor

  1. Sonia Sen, Tata Institute for Genetics and Society, India

Version history

  1. Received: September 15, 2022
  2. Accepted: January 18, 2023
  3. Accepted Manuscript published: January 19, 2023 (version 1)
  4. Version of Record published: February 8, 2023 (version 2)

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

  • 802
    views
  • 207
    downloads
  • 4
    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
    Songdou Zhang, Shiheng An
    Insight

    The bacterium responsible for a disease that infects citrus plants across Asia facilitates its own proliferation by increasing the fecundity of its host insect.

    1. Ecology
    2. Evolutionary Biology
    Alexis J Breen, Dominik Deffner
    Research Article

    In the unpredictable Anthropocene, a particularly pressing open question is how certain species invade urban environments. Sex-biased dispersal and learning arguably influence movement ecology, but their joint influence remains unexplored empirically, and might vary by space and time. We assayed reinforcement learning in wild-caught, temporarily captive core-, middle-, or edge-range great-tailed grackles—a bird species undergoing urban-tracking rapid range expansion, led by dispersing males. We show, across populations, both sexes initially perform similarly when learning stimulus-reward pairings, but, when reward contingencies reverse, male—versus female—grackles finish ‘relearning’ faster, making fewer choice-option switches. How do male grackles do this? Bayesian cognitive modelling revealed male grackles’ choice behaviour is governed more strongly by the ‘weight’ of relative differences in recent foraging payoffs—i.e., they show more pronounced risk-sensitive learning. Confirming this mechanism, agent-based forward simulations of reinforcement learning—where we simulate ‘birds’ based on empirical estimates of our grackles’ reinforcement learning—replicate our sex-difference behavioural data. Finally, evolutionary modelling revealed natural selection should favour risk-sensitive learning in hypothesised urban-like environments: stable but stochastic settings. Together, these results imply risk-sensitive learning is a winning strategy for urban-invasion leaders, underscoring the potential for life history and cognition to shape invasion success in human-modified environments.