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.

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

  • 4,576
    views
  • 675
    downloads
  • 17
    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
    2. Evolutionary Biology
    Vendula Bohlen Šlechtová, Tomáš Dvořák ... Joerg Bohlen
    Research Article

    Eurasia has undergone substantial tectonic, geological, and climatic changes throughout the Cenozoic, primarily associated with tectonic plate collisions and a global cooling trend. The evolution of present-day biodiversity unfolded in this dynamic environment, characterised by intricate interactions of abiotic factors. However, comprehensive, large-scale reconstructions illustrating the extent of these influences are lacking. We reconstructed the evolutionary history of the freshwater fish family Nemacheilidae across Eurasia and spanning most of the Cenozoic on the base of 471 specimens representing 279 species and 37 genera plus outgroup samples. Molecular phylogeny using six genes uncovered six major clades within the family, along with numerous unresolved taxonomic issues. Dating of cladogenetic events and ancestral range estimation traced the origin of Nemacheilidae to Indochina around 48 mya. Subsequently, one branch of Nemacheilidae colonised eastern, central, and northern Asia, as well as Europe, while another branch expanded into the Burmese region, the Indian subcontinent, the Near East, and northeast Africa. These expansions were facilitated by tectonic connections, favourable climatic conditions, and orogenic processes. Conversely, aridification emerged as the primary cause of extinction events. Our study marks the first comprehensive reconstruction of the evolution of Eurasian freshwater biodiversity on a continental scale and across deep geological time.

    1. Ecology
    2. Neuroscience
    Kathleen T Quach, Gillian A Hughes, Sreekanth H Chalasani
    Research Article

    Prey must balance predator avoidance with feeding, a central dilemma in prey refuge theory. Additionally, prey must assess predatory imminence—how close threats are in space and time. Predatory imminence theory classifies defensive behaviors into three defense modes: pre-encounter, post-encounter, and circa-strike, corresponding to increasing levels of threat—–suspecting, detecting, and contacting a predator. Although predatory risk often varies in spatial distribution and imminence, how these factors intersect to influence defensive behaviors is poorly understood. Integrating these factors into a naturalistic environment enables comprehensive analysis of multiple defense modes in consistent conditions. Here, we combine prey refuge and predatory imminence theories to develop a model system of nematode defensive behaviors, with Caenorhabditis elegans as prey and Pristionchus pacificus as predator. In a foraging environment comprised of a food-rich, high-risk patch and a food-poor, low-risk refuge, C. elegans innately exhibits circa-strike behaviors. With experience, it learns post- and pre-encounter behaviors that proactively anticipate threats. These defense modes intensify with predator lethality, with only life-threatening predators capable of eliciting all three modes. SEB-3 receptors and NLP-49 peptides, key stress regulators, vary in their impact and interdependence across defense modes. Overall, our model system reveals fine-grained insights into how stress-related signaling regulates defensive behaviors.