Molecular basis of wax-based color change and UV reflection in dragonflies

  1. Ryo Futahashi  Is a corresponding author
  2. Yumi Yamahama
  3. Migaku Kawaguchi
  4. Naoki Mori
  5. Daisuke Ishii
  6. Genta Okude
  7. Yuji Hirai
  8. Ryouka Kawahara-Miki
  9. Kazutoshi Yoshitake
  10. Shunsuke Yajima
  11. Takahiko Hariyama
  12. Takema Fukatsu
  1. National Institute of Advanced Industrial Science and Technology (AIST), Japan
  2. Hamamatsu University School of Medicine, Japan
  3. National Institute of Advanced Industrial Science and Technology (AIST), Japan
  4. Kyoto University, Japan
  5. Nagoya Institute of Technology, Japan
  6. Chitose Institute of Science and Technology, Japan
  7. Tokyo University of Agriculture, Japan
  8. University of Tokyo, Japan

Abstract

Many animals change their body color for visual signaling and environmental adaptation. Some dragonflies show wax-based color change and ultraviolet (UV) reflection, but biochemical properties underlying the phenomena are totally unknown. Here we investigated the UV-reflective abdominal wax of dragonflies, thereby identifying very long-chain methyl ketones and aldehydes as unique and major wax components. Although little wax was detected on young adults, dense wax secretion was mainly found on the dorsal abdomen in mature males of Orthetrum albistylum and O. melania, while pruinose wax secretion was identified on the ventral abdomen in mature females of O. albistylum and Sympetrum darwinianum. Comparative transcriptomics demonstrated drastic upregulation of ELOVL17 gene, a member of the fatty acid elongase family, whose expression reflected the distribution of very long-chain methyl ketones. Synthetic 2-pentacosanone, the major component of dragonfly's wax, spontaneously formed light-scattering scale-like fine structures with strong UV reflection, suggesting its potential utility for biomimetics.

Data availability

The sequences reported in this paper have been deposited in the DNAData Bank Japan Read Archive, www.ddbj.nig.ac.jp (accession nos. BR001497-BR001513, LC416747-LC416767, DRA001687, DRA001690, DRA001693-DRA001694, DRA001697-DRA001698, DRA001700-DRA001701, DRA001703-DRA001704, DRA001706-DRA001707, DRA001709-DRA001710, DRA001712-DRA001713, DRA001716-DRA001717, DRA007015-DRA007018).All data generated or analysed during this study are included in the manuscript and supporting files. Source data files have been provided for Figures 2,6I-L,7I-N, and Figure S1.

The following previously published data sets were used

Article and author information

Author details

  1. Ryo Futahashi

    Bioproduction Research Institute, National Institute of Advanced Industrial Science and Technology (AIST), Tsukuba, Japan
    For correspondence
    ryo-futahashi@aist.go.jp
    Competing interests
    Ryo Futahashi, An international patent on the synthesis method and application of very long chain methyl ketones and aldehydes was applied as PCT/JP2018/019559.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4791-7054
  2. Yumi Yamahama

    Department of Biology, Hamamatsu University School of Medicine, Hamamatsu, Japan
    Competing interests
    Yumi Yamahama, An international patent on the synthesis method and application of very long chain methyl ketones and aldehydes was applied as PCT/JP2018/019559.
  3. Migaku Kawaguchi

    National Metrology Institute of Japan, National Institute of Advanced Industrial Science and Technology (AIST), Tsukuba, Japan
    Competing interests
    Migaku Kawaguchi, An international patent on the synthesis method and application of very long chain methyl ketones and aldehydes was applied as PCT/JP2018/019559.
  4. Naoki Mori

    Division of Applied Life Sciences, Graduate School of Agriculture, Kyoto University, Kyoto, Japan
    Competing interests
    No competing interests declared.
  5. Daisuke Ishii

    Department of Life Science and Applied Chemistry, Graduate School of Engineering, Nagoya Institute of Technology, Nagoya, Japan
    Competing interests
    Daisuke Ishii, An international patent on the synthesis method and application of very long chain methyl ketones and aldehydes was applied as PCT/JP2018/019559.
  6. Genta Okude

    Bioproduction Research Institute, National Institute of Advanced Industrial Science and Technology (AIST), Tsukuba, Japan
    Competing interests
    No competing interests declared.
  7. Yuji Hirai

    Applied Chemistry and Bioscience, Chitose Institute of Science and Technology, Chitose, Japan
    Competing interests
    No competing interests declared.
  8. Ryouka Kawahara-Miki

    NODAI Genome Research Center, Tokyo University of Agriculture, Tokyo, Japan
    Competing interests
    Ryouka Kawahara-Miki, An international patent on the synthesis method and application of very long chain methyl ketones and aldehydes was applied as PCT/JP2018/019559.
  9. Kazutoshi Yoshitake

    Graduate School of Agricultural and Life Sciences, University of Tokyo, Tokyo, Japan
    Competing interests
    No competing interests declared.
  10. Shunsuke Yajima

    NODAI Genome Research Center, Tokyo University of Agriculture, Tokyo, Japan
    Competing interests
    Shunsuke Yajima, An international patent on the synthesis method and application of very long chain methyl ketones and aldehydes was applied as PCT/JP2018/019559.
  11. Takahiko Hariyama

    Department of Biology, Hamamatsu University School of Medicine, Hamamatsu, Japan
    Competing interests
    Takahiko Hariyama, An international patent on the synthesis method and application of very long chain methyl ketones and aldehydes was applied as PCT/JP2018/019559.
  12. Takema Fukatsu

    Bioproduction Research Institute, National Institute of Advanced Industrial Science and Technology (AIST), Tsukuba, Japan
    Competing interests
    No competing interests declared.

Funding

Japan Society for the Promotion of Science (JP26660276)

  • Ryo Futahashi

Genome research for BioResource NODAI Genome Research Center

  • Ryo Futahashi
  • Ryouka Kawahara-Miki
  • Shunsuke Yajima

Japan Society for the Promotion of Science (JP18H02491)

  • Ryo Futahashi

Japan Society for the Promotion of Science (JP18H04893)

  • Ryo Futahashi

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

Reviewing Editor

  1. David Lentink, Stanford University, United States

Version history

  1. Received: October 22, 2018
  2. Accepted: January 7, 2019
  3. Accepted Manuscript published: January 15, 2019 (version 1)
  4. Version of Record published: January 30, 2019 (version 2)
  5. Version of Record updated: February 1, 2019 (version 3)

Copyright

© 2019, Futahashi 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

  • 4,345
    views
  • 641
    downloads
  • 15
    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. Ryo Futahashi
  2. Yumi Yamahama
  3. Migaku Kawaguchi
  4. Naoki Mori
  5. Daisuke Ishii
  6. Genta Okude
  7. Yuji Hirai
  8. Ryouka Kawahara-Miki
  9. Kazutoshi Yoshitake
  10. Shunsuke Yajima
  11. Takahiko Hariyama
  12. Takema Fukatsu
(2019)
Molecular basis of wax-based color change and UV reflection in dragonflies
eLife 8:e43045.
https://doi.org/10.7554/eLife.43045

Share this article

https://doi.org/10.7554/eLife.43045

Further reading

    1. Ecology
    Yang Ruan, Ning Ling ... Zhibiao Nan
    Research Article

    Warming and precipitation anomalies affect terrestrial carbon balance partly through altering microbial eco-physiological processes (e.g., growth and death) in soil. However, little is known about how such processes responds to simultaneous regime shifts in temperature and precipitation. We used the 18O-water quantitative stable isotope probing approach to estimate bacterial growth in alpine meadow soils of the Tibetan Plateau after a decade of warming and altered precipitation manipulation. Our results showed that the growth of major taxa was suppressed by the single and combined effects of temperature and precipitation, eliciting 40–90% of growth reduction of whole community. The antagonistic interactions of warming and altered precipitation on population growth were common (~70% taxa), represented by the weak antagonistic interactions of warming and drought, and the neutralizing effects of warming and wet. The members in Solirubrobacter and Pseudonocardia genera had high growth rates under changed climate regimes. These results are important to understand and predict the soil microbial dynamics in alpine meadow ecosystems suffering from multiple climate change factors.

    1. Ecology
    Anna L Erdei, Aneth B David ... Teun Dekker
    Research Article Updated

    Over two decades ago, an intercropping strategy was developed that received critical acclaim for synergizing food security with ecosystem resilience in smallholder farming. The push–pull strategy reportedly suppresses lepidopteran pests in maize through a combination of a repellent intercrop (push), commonly Desmodium spp., and an attractive, border crop (pull). Key in the system is the intercrop’s constitutive release of volatile terpenoids that repel herbivores. However, the earlier described volatile terpenoids were not detectable in the headspace of Desmodium, and only minimally upon herbivory. This was independent of soil type, microbiome composition, and whether collections were made in the laboratory or in the field. Furthermore, in oviposition choice tests in a wind tunnel, maize with or without an odor background of Desmodium was equally attractive for the invasive pest Spodoptera frugiperda. In search of an alternative mechanism, we found that neonate larvae strongly preferred Desmodium over maize. However, their development stagnated and no larva survived. In addition, older larvae were frequently seen impaled and immobilized by the dense network of silica-fortified, non-glandular trichomes. Thus, our data suggest that Desmodium may act through intercepting and decimating dispersing larval offspring rather than adult deterrence. As a hallmark of sustainable pest control, maize–Desmodium push–pull intercropping has inspired countless efforts to emulate stimulo-deterrent diversion in other cropping systems. However, detailed knowledge of the actual mechanisms is required to rationally improve the strategy, and translate the concept to other cropping systems.