Desiccation resistance differences in Drosophila species can be largely explained by variations in cuticular hydrocarbons

  1. Zinan Wang  Is a corresponding author
  2. Joseph P Receveur
  3. Jian Pu
  4. Haosu Cong
  5. Cole Richards
  6. Muxuan Liang
  7. Henry Chung  Is a corresponding author
  1. Michigan State University, United States
  2. University of Florida, United States

Abstract

Maintaining water balance is a universal challenge for organisms living in terrestrial environments, especially for insects, which have essential roles in our ecosystem. Although the high surface area to volume ratio in insects makes them vulnerable to water loss, insects have evolved different levels of desiccation resistance to adapt to diverse environments. To withstand desiccation, insects use a lipid layer called cuticular hydrocarbons (CHCs) to reduce water evaporation from the body surface. It has long been hypothesized that the waterproofing capability of this CHC layer, which can confer different levels of desiccation resistance, depends on its chemical composition. However, it is unknown which CHC components are important contributors to desiccation resistance and how these components can determine differences in desiccation resistance. In this study, we used machine learning algorithms, correlation analyses, and synthetic CHCs to investigate how different CHC components affect desiccation resistance in 50 Drosophila and related species. We showed that desiccation resistance differences across these species can be largely explained by variation in CHC composition. In particular, length variation in a subset of CHCs, the methyl-branched CHCs (mbCHCs), is a key determinant of desiccation resistance. There is also a significant correlation between the evolution of longer mbCHCs and higher desiccation resistance in these species. Given that CHCs are almost ubiquitous in insects, we suggest that evolutionary changes in insect CHC components can be a general mechanism for the evolution of desiccation resistance and adaptation to diverse and changing environments.

Data availability

All data generated or analyzed during this study are included in the manuscript and supporting source data file. Code used is uploaded as source code 1-3.

Article and author information

Author details

  1. Zinan Wang

    Department of Entomology, Michigan State University, East Lansing, United States
    For correspondence
    wangzina@msu.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0509-4902
  2. Joseph P Receveur

    Department of Entomology, Michigan State University, East Lansing, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Jian Pu

    Department of Entomology, Michigan State University, East Lansing, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Haosu Cong

    Department of Entomology, Michigan State University, East Lansing, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Cole Richards

    Department of Entomology, Michigan State University, East Lansing, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Muxuan Liang

    Department of Biostatistics, University of Florida, Gainsville, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. Henry Chung

    Department of Entomology, Michigan State University, East Lansing, United States
    For correspondence
    hwchung@msu.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5056-2755

Funding

National Science Foundation (2054773)

  • Henry Chung

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

Reviewing Editor

  1. Lynn M. Riddiford

Version history

  1. Received: June 7, 2022
  2. Preprint posted: June 28, 2022 (view preprint)
  3. Accepted: December 5, 2022
  4. Accepted Manuscript published: December 6, 2022 (version 1)
  5. Version of Record published: December 16, 2022 (version 2)

Copyright

© 2022, Wang 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

  • 1,542
    Page views
  • 291
    Downloads
  • 7
    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)

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. Zinan Wang
  2. Joseph P Receveur
  3. Jian Pu
  4. Haosu Cong
  5. Cole Richards
  6. Muxuan Liang
  7. Henry Chung
(2022)
Desiccation resistance differences in Drosophila species can be largely explained by variations in cuticular hydrocarbons
eLife 11:e80859.
https://doi.org/10.7554/eLife.80859

Share this article

https://doi.org/10.7554/eLife.80859

Further reading

    1. Ecology
    Congnan Sun, Yoel Hassin ... Yossi Yovel
    Research Article

    Covid-19 lockdowns provided ecologists with a rare opportunity to examine how animals behave when humans are absent. Indeed many studies reported various effects of lockdowns on animal activity, especially in urban areas and other human-dominated habitats. We explored how Covid-19 lockdowns in Israel have influenced bird activity in an urban environment by using continuous acoustic recordings to monitor three common bird species that differ in their level of adaptation to the urban ecosystem: (1) the hooded crow, an urban exploiter, which depends heavily on anthropogenic resources; (2) the rose-ringed parakeet, an invasive alien species that has adapted to exploit human resources; and (3) the graceful prinia, an urban adapter, which is relatively shy of humans and can be found in urban habitats with shrubs and prairies. Acoustic recordings provided continuous monitoring of bird activity without an effect of the observer on the animal. We performed dense sampling of a 1.3 square km area in northern Tel-Aviv by placing 17 recorders for more than a month in different micro-habitats within this region including roads, residential areas and urban parks. We monitored both lockdown and no-lockdown periods. We portray a complex dynamic system where the activity of specific bird species depended on many environmental parameters and decreases or increases in a habitat-dependent manner during lockdown. Specifically, urban exploiter species decreased their activity in most urban habitats during lockdown, while human adapter species increased their activity during lockdown especially in parks where humans were absent. Our results also demonstrate the value of different habitats within urban environments for animal activity, specifically highlighting the importance of urban parks. These species- and habitat-specific changes in activity might explain the contradicting results reported by others who have not performed a habitat specific analysis.

    1. Ecology
    2. Plant Biology
    Daniel Fuks, Yoel Melamed ... Ehud Weiss
    Research Article Updated

    Global agro-biodiversity has resulted from processes of plant migration and agricultural adoption. Although critically affecting current diversity, crop diffusion from Classical antiquity to the Middle Ages is poorly researched, overshadowed by studies on that of prehistoric periods. A new archaeobotanical dataset from three Negev Highland desert sites demonstrates the first millennium CE’s significance for long-term agricultural change in Southwest Asia. This enables evaluation of the ‘Islamic Green Revolution (IGR)’ thesis compared to ‘Roman Agricultural Diffusion (RAD)’, and both versus crop diffusion during and since the Neolithic. Among the findings, some of the earliest aubergine (Solanum melongena) seeds in the Levant represent the proposed IGR. Several other identified economic plants, including two unprecedented in Levantine archaeobotany—jujube (Ziziphus jujuba/mauritiana) and white lupine (Lupinus albus)—implicate RAD as the greater force for crop migrations. Altogether the evidence supports a gradualist model for Holocene-wide crop diffusion, within which the first millennium CE contributed more to global agricultural diversity than any earlier period.