Early evolution of beetles regulated by the end-Permian deforestation

  1. Xianye Zhao
  2. Yilun Yu
  3. Matthew E Clapham
  4. Evgeny Yan
  5. Jun Chen
  6. Edmund A Jarzembowski
  7. Xiangdong Zhao
  8. Bo Wang  Is a corresponding author
  1. Nanjing Institute of Geology and Palaeontology, China
  2. Institute of Vertebrate Paleontology and Paleoanthropology, China
  3. Department of Earth and Planetary Sciences, University of California, Santa Cruz, United States
  4. Palaeontological Institute, Russian Academy of Sciences, Russian Federation
  5. Institute of Geology and Paleontology, Linyi University, China
  6. Chinese Academy of Sciences, China

Abstract

The end-Permian mass extinction (EPME) led to a severe terrestrial ecosystem collapse. However, the ecological response of insects—the most diverse group of organisms on Earth—to the EPME remains poorly understood. Here, we analyse beetle evolutionary history based on taxonomic diversity, morphological disparity, phylogeny, and ecological shifts from the Early Permian to Middle Triassic, using a comprehensive new data set. Permian beetles were dominated by xylophagous stem groups with high diversity and disparity, which probably played an underappreciated role in the Permian carbon cycle. Our suite of analyses shows that Permian xylophagous beetles suffered a severe extinction during the EPME largely due to the collapse of forest ecosystems, resulting in an Early Triassic gap of xylophagous beetles. New xylophagous beetles appeared widely in the early Middle Triassic, which is consistent with the restoration of forest ecosystems. Our results highlight the ecological significance of insects in deep-time terrestrial ecosystems.

Data availability

All source data are available at https://doi.org/10.5061/dryad.7m0cfxpvd. In addition, the source data files (Supplementary Data 1-4) have been provided for figures 2-4 and appendix figures 1-10.

The following data sets were generated

Article and author information

Author details

  1. Xianye Zhao

    Nanjing Institute of Geology and Palaeontology, Nanjing, China
    Competing interests
    The authors declare that no competing interests exist.
  2. Yilun Yu

    Institute of Vertebrate Paleontology and Paleoanthropology, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  3. Matthew E Clapham

    Department of Earth and Planetary Sciences, University of California, Santa Cruz, Santa Cruz, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Evgeny Yan

    Palaeontological Institute, Russian Academy of Sciences, Moscow, Russian Federation
    Competing interests
    The authors declare that no competing interests exist.
  5. Jun Chen

    Institute of Geology and Paleontology, Linyi University, Linyi, China
    Competing interests
    The authors declare that no competing interests exist.
  6. Edmund A Jarzembowski

    State Key Laboratory of Palaeobiology and Stratigraphy, Nanjing Institute of Geology and Palaeontology, Chinese Academy of Sciences, Nanjiing, China
    Competing interests
    The authors declare that no competing interests exist.
  7. Xiangdong Zhao

    Nanjing Institute of Geology and Palaeontology, Nanjing, China
    Competing interests
    The authors declare that no competing interests exist.
  8. Bo Wang

    Nanjing Institute of Geology and Palaeontology, Nanjing, China
    For correspondence
    bowang@nigpas.ac.cn
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8001-9937

Funding

Chinese Academy of Sciences (XDA19050101,XDB26000000)

  • Bo Wang

National Natural Science Foundation of China (42125201,41688103)

  • Bo Wang

Natural Scientific Founation of Shandong Province (ZR2020YQ27)

  • Jun Chen

Russian Science Foundation (21-14-00284)

  • Evgeny Yan

Chinese Academy of Sciences (2020VCA0020)

  • Edmund A Jarzembowski

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

Reviewing Editor

  1. George H Perry, Pennsylvania State University, United States

Version history

  1. Received: August 1, 2021
  2. Preprint posted: October 13, 2021 (view preprint)
  3. Accepted: November 3, 2021
  4. Accepted Manuscript published: November 8, 2021 (version 1)
  5. Version of Record published: November 11, 2021 (version 2)

Copyright

© 2021, Zhao 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

  • 1,891
    views
  • 292
    downloads
  • 19
    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. Xianye Zhao
  2. Yilun Yu
  3. Matthew E Clapham
  4. Evgeny Yan
  5. Jun Chen
  6. Edmund A Jarzembowski
  7. Xiangdong Zhao
  8. Bo Wang
(2021)
Early evolution of beetles regulated by the end-Permian deforestation
eLife 10:e72692.
https://doi.org/10.7554/eLife.72692

Share this article

https://doi.org/10.7554/eLife.72692

Further reading

    1. Evolutionary Biology
    Deng Wang, Yaqin Qiang ... Jian Han
    Research Article

    Extant ecdysozoans (moulting animals) are represented by a great variety of soft-bodied or articulated organisms that may or may not have appendages. However, controversies remain about the vermiform nature (i.e. elongated and tubular) of their ancestral body plan. We describe here Beretella spinosa gen. et sp. nov. a tiny (maximal length 3 mm) ecdysozoan from the lowermost Cambrian, Yanjiahe Formation, South China, characterized by an unusual sack-like appearance, single opening, and spiny ornament. Beretella spinosa gen. et sp. nov has no equivalent among animals, except Saccorhytus coronarius, also from the basal Cambrian. Phylogenetic analyses resolve both fossil species as a sister group (Saccorhytida) to all known Ecdysozoa, thus suggesting that ancestral ecdysozoans may have been non-vermiform animals. Saccorhytids are likely to represent an early off-shot along the stem-line Ecdysozoa. Although it became extinct during the Cambrian, this animal lineage provides precious insight into the early evolution of Ecdysozoa and the nature of the earliest representatives of the group.

    1. Biochemistry and Chemical Biology
    2. Evolutionary Biology
    Foteini Karapanagioti, Úlfur Águst Atlason ... Sebastian Obermaier
    Research Article

    The emergence of new protein functions is crucial for the evolution of organisms. This process has been extensively researched for soluble enzymes, but it is largely unexplored for membrane transporters, even though the ability to acquire new nutrients from a changing environment requires evolvability of transport functions. Here, we demonstrate the importance of environmental pressure in obtaining a new activity or altering a promiscuous activity in members of the amino acid-polyamine-organocation (APC)-type yeast amino acid transporters family. We identify APC members that have broader substrate spectra than previously described. Using in vivo experimental evolution, we evolve two of these transporter genes, AGP1 and PUT4, toward new substrate specificities. Single mutations on these transporters are found to be sufficient for expanding the substrate range of the proteins, while retaining the capacity to transport all original substrates. Nonetheless, each adaptive mutation comes with a distinct effect on the fitness for each of the original substrates, illustrating a trade-off between the ancestral and evolved functions. Collectively, our findings reveal how substrate-adaptive mutations in membrane transporters contribute to fitness and provide insights into how organisms can use transporter evolution to explore new ecological niches.