From Gondwana to the Yellow Sea, evolutionary diversifications of true toads Bufo sp. in the Eastern Palearctic and a revisit of species boundaries for Asian lineages

  1. Siti N Othman
  2. Spartak N Litvinchuk
  3. Irina Maslova
  4. Hollis Dahn
  5. Kevin R Messenger
  6. Desiree Andersen
  7. Michael J Jowers
  8. Yosuke Kojima
  9. Dmitry V Skorinov
  10. Kiyomi Yasumiba
  11. Ming-Feng Chuang
  12. Yi-Huey Chen
  13. Yoonhyuk Bae
  14. Jennifer Hoti
  15. Yikweon Jang  Is a corresponding author
  16. Amaël Borzée  Is a corresponding author
  1. Ewha Womans University, Republic of Korea
  2. Russian Academy of Sciences, Russian Federation
  3. Federal Scientific Center of the East Asia Terrestrial Biodiversity Far Eastern Branch of Russian Academy of Sciences, Russian Federation
  4. University of Toronto, Canada
  5. Nanjing Forestry University, China
  6. Universidade do Porto, Portugal
  7. Kyoto University, Japan
  8. Tokyo University of Agriculture and Technology, Japan
  9. National Chung Hsing University, Taiwan
  10. Chinese Culture University, Taiwan

Abstract

Taxa with vast distribution ranges often display unresolved phylogeographic structures and unclear taxonomic boundaries resulting into hidden diversity. This hypothesis-driven study reveals the evolutionary history of Bufonidae, covering the phylogeographic patterns found in Holarctic bufonids from the West Gondwana to the phylogenetic taxonomy of Asiatic true toads in the Eastern Palearctic. We used an integrative approach relying on fossilised birth-death calibrations, population dynamic, gene-flow, species distribution and species delimitation modelling to resolve the biogeography of the clade and highlight cryptic lineages. We verified the near-simultaneous Miocene radiations within Western and Eastern Palearctic Bufo, c. 14.49 - 10.00 Mya, temporally matching with the maximum dust outflows in Central Asian deserts. Contrary to earlier studies, we demonstrated that the combined impacts of long dispersal and ice-age refugia equally contributed to the current genetic structure of Bufo in East Asia. Our findings reveal a climate-driven adaptation in septentrional Eastern Asian Bufo, explained its range shifts towards northern latitudes. We resolve species boundaries within the Eastern Palearctic Bufo, and redefine the taxonomic and conservation units of the northeastern species: B. sachalinensis and its subspecies.

Data availability

All data generated or analysed during this study are either included in the manuscript and supporting files, or submitted online depositories. All Sequences generated in present study deposited to the Genbank database [https://www.ncbi.nlm.nih.gov/ 927 genbank/] under the accession number MW081664- MW081847 (CR), MW467646-MW467777 (ND2), MW489915-MW489964 (POMC), MW489986-MW490035 (RAG-1), MW507752-MW507780 (Rho). Input files in the form of BEAST XML generated for all molecular dating analyses and species delimitation modelling are available from the Mendeley Data repository http://dx.doi.org/10.17632/wdtw6kn2t4.1 (Othman et al., 2021).

The following data sets were generated

Article and author information

Author details

  1. Siti N Othman

    Department of Life Sciences, Ewha Womans University, Seoul, Republic of Korea
    Competing interests
    The authors declare that no competing interests exist.
  2. Spartak N Litvinchuk

    Institute of Cytology, Russian Academy of Sciences, St. Petersburg, Russian Federation
    Competing interests
    The authors declare that no competing interests exist.
  3. Irina Maslova

    Federal Scientific Center of the East Asia Terrestrial Biodiversity Far Eastern Branch of Russian Academy of Sciences, Vladivostok, Russian Federation
    Competing interests
    The authors declare that no competing interests exist.
  4. Hollis Dahn

    Department of Ecology and Evolutionary Biology, University of Toronto, Toronto, Canada
    Competing interests
    The authors declare that no competing interests exist.
  5. Kevin R Messenger

    Herpetology and Applied Conservation Laboratory, Nanjing Forestry University, Nanjing, China
    Competing interests
    The authors declare that no competing interests exist.
  6. Desiree Andersen

    Department of Life Sciences, Ewha Womans University, Seoul, Republic of Korea
    Competing interests
    The authors declare that no competing interests exist.
  7. Michael J Jowers

    Universidade do Porto, Vairão, Portugal
    Competing interests
    The authors declare that no competing interests exist.
  8. Yosuke Kojima

    Graduate School of Human and Environmental Studies, Kyoto University, Kyoto, Japan
    Competing interests
    The authors declare that no competing interests exist.
  9. Dmitry V Skorinov

    Institute of Cytology, Russian Academy of Sciences, St. Petersburg, Russian Federation
    Competing interests
    The authors declare that no competing interests exist.
  10. Kiyomi Yasumiba

    Tokyo University of Agriculture and Technology, Tokyo, Japan
    Competing interests
    The authors declare that no competing interests exist.
  11. Ming-Feng Chuang

    Department of Life Sciences, National Chung Hsing University, Taipei, Taiwan
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7328-2577
  12. Yi-Huey Chen

    Department of Life Science, Chinese Culture University, Taipei, Taiwan
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0987-2385
  13. Yoonhyuk Bae

    Department of Life Sciences, Ewha Womans University, Seoul, Republic of Korea
    Competing interests
    The authors declare that no competing interests exist.
  14. Jennifer Hoti

    Department of Life Sciences, Ewha Womans University, Seoul, Republic of Korea
    Competing interests
    The authors declare that no competing interests exist.
  15. Yikweon Jang

    Department of Life Sciences, Ewha Womans University, Seoul, Republic of Korea
    For correspondence
    jangy@ewha.ac.kr
    Competing interests
    The authors declare that no competing interests exist.
  16. Amaël Borzée

    Laboratory of Animal Behaviour and Conservation, Nanjing Forestry University, Nanjing, China
    For correspondence
    amaelborzee@gmail.com
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-1093-677X

Funding

Korean Environmental Industry and Technology Institute (KEITI 2017002270003)

  • Yikweon Jang

Foreign Youth Talent Program (QN2021014013L)

  • Amaël Borzée

Russian Foundation of Basic Research (20-04-00918)

  • Spartak N Litvinchuk

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 Donoso, Escuela Politécnica Nacional, Ecuador

Ethics

Animal experimentation: Sampling in the Republic of Korea were collected in 2017 under the Ministerial authorisation number 2017-16, and the samples from Jirisan National Park were collected under the Ministerial authorisation number 2019-01. Samples from the People's Republic of China were collected under the authorisation provided by Nanjing Forestry University. IACUC permit is not required for the in-situ experiment in this study, in accord to the rules of Ewha Woman's University Institutional Biosafety Committee

Version history

  1. Received: May 18, 2021
  2. Accepted: January 27, 2022
  3. Accepted Manuscript published: January 28, 2022 (version 1)
  4. Version of Record published: March 14, 2022 (version 2)

Copyright

© 2022, Othman 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

  • 1,520
    views
  • 313
    downloads
  • 18
    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. Siti N Othman
  2. Spartak N Litvinchuk
  3. Irina Maslova
  4. Hollis Dahn
  5. Kevin R Messenger
  6. Desiree Andersen
  7. Michael J Jowers
  8. Yosuke Kojima
  9. Dmitry V Skorinov
  10. Kiyomi Yasumiba
  11. Ming-Feng Chuang
  12. Yi-Huey Chen
  13. Yoonhyuk Bae
  14. Jennifer Hoti
  15. Yikweon Jang
  16. Amaël Borzée
(2022)
From Gondwana to the Yellow Sea, evolutionary diversifications of true toads Bufo sp. in the Eastern Palearctic and a revisit of species boundaries for Asian lineages
eLife 11:e70494.
https://doi.org/10.7554/eLife.70494

Share this article

https://doi.org/10.7554/eLife.70494

Further reading

    1. Computational and Systems Biology
    2. Ecology
    Kazushi Tsutsui, Ryoya Tanaka ... Keisuke Fujii
    Research Article

    Collaborative hunting, in which predators play different and complementary roles to capture prey, has been traditionally believed to be an advanced hunting strategy requiring large brains that involve high-level cognition. However, recent findings that collaborative hunting has also been documented in smaller-brained vertebrates have placed this previous belief under strain. Here, using computational multi-agent simulations based on deep reinforcement learning, we demonstrate that decisions underlying collaborative hunts do not necessarily rely on sophisticated cognitive processes. We found that apparently elaborate coordination can be achieved through a relatively simple decision process of mapping between states and actions related to distance-dependent internal representations formed by prior experience. Furthermore, we confirmed that this decision rule of predators is robust against unknown prey controlled by humans. Our computational ecological results emphasize that collaborative hunting can emerge in various intra- and inter-specific interactions in nature, and provide insights into the evolution of sociality.

    1. Ecology
    2. Evolutionary Biology
    Théo Constant, F Stephen Dobson ... Sylvain Giroud
    Research Article

    Seasonal animal dormancy is widely interpreted as a physiological response for surviving energetic challenges during the harshest times of the year (the physiological constraint hypothesis). However, there are other mutually non-exclusive hypotheses to explain the timing of animal dormancy, that is, entry into and emergence from hibernation (i.e. dormancy phenology). Survival advantages of dormancy that have been proposed are reduced risks of predation and competition (the ‘life-history’ hypothesis), but comparative tests across animal species are few. Using the phylogenetic comparative method applied to more than 20 hibernating mammalian species, we found support for both hypotheses as explanations for the phenology of dormancy. In accordance with the life-history hypotheses, sex differences in hibernation emergence and immergence were favored by the sex difference in reproductive effort. In addition, physiological constraint may influence the trade-off between survival and reproduction such that low temperatures and precipitation, as well as smaller body mass, influence sex differences in phenology. We also compiled initial evidence that ectotherm dormancy may be (1) less temperature dependent than previously thought and (2) associated with trade-offs consistent with the life-history hypothesis. Thus, dormancy during non-life-threatening periods that are unfavorable for reproduction may be more widespread than previously thought.