Phylogenomics of white-eyes, a 'great speciator', reveals Indonesian archipelago as the center of lineage diversity

  1. Chyi Yin Gwee
  2. Kritika M Garg
  3. Balaji Chattopadhyay
  4. Keren R Sadanandan
  5. Dewi M Prawiradilaga
  6. Martin Irestedt
  7. Fumin Lei
  8. Luke M Bloch
  9. Jessica GH Lee
  10. Mohammad Irham
  11. Tri Haryoko
  12. Malcolm CK Soh
  13. Kelvin S-H Peh
  14. Karen MC Rowe
  15. Teuku Reza Ferasyi
  16. Shaoyuan Wu
  17. Guinevere OU Wogan
  18. Rauri CK Bowie
  19. Frank E Rheindt  Is a corresponding author
  1. National University of Singapore, Singapore
  2. Indonesian Institute of Sciences (LIPI), Indonesia
  3. Swedish Museum of Natural History, Sweden
  4. Institute of Zoology (CAS), China
  5. University of California, Berkeley, United States
  6. Wildlife Reserves Singapore, Singapore
  7. University of Western Australia, Australia
  8. University of Southampton, United Kingdom
  9. Museums Victoria, Australia
  10. Universitas Syiah Kuala, Indonesia
  11. Jiangsu Normal University, China

Abstract

Archipelagoes serve as important 'natural laboratories' which facilitate the study of island radiations and contribute to the understanding of evolutionary processes. The white-eye genus Zosterops is a classical example of a 'great speciator', comprising c. 100 species from across the Old World, most of them insular. We achieved an extensive geographic DNA sampling of Zosterops by using historical specimens and recently collected samples. Using over 700 genome-wide loci in conjunction with coalescent species tree methods and gene flow detection approaches, we untangled the reticulated evolutionary history of Zosterops, which comprises three main clades centered in Indo-Africa, Asia, and Australasia, respectively. Genetic introgression between species permeates the Zosterops phylogeny, regardless of how distantly related species are. Crucially, we identified the Indonesian archipelago, and specifically Borneo, as the major centre of diversity and the only area where all three main clades overlap, attesting to the evolutionary importance of this region.

Data availability

All data generated or analysed during this study are included in Dryad database: https://doi.org/10.5061/dryad.8931zcrmt. Raw FASTQ files of target enriched samples are available on NCBI under BioProject no. PRJNA682287.

The following data sets were generated
The following previously published data sets were used

Article and author information

Author details

  1. Chyi Yin Gwee

    Biological Sciences, National University of Singapore, Singapore, Singapore
    Competing interests
    The authors declare that no competing interests exist.
  2. Kritika M Garg

    Biological Sciences, National University of Singapore, Singapore, Singapore
    Competing interests
    The authors declare that no competing interests exist.
  3. Balaji Chattopadhyay

    Biological Sciences, National University of Singapore, Singapore, Singapore
    Competing interests
    The authors declare that no competing interests exist.
  4. Keren R Sadanandan

    Biological Sciences, National University of Singapore, Singapore, Singapore
    Competing interests
    The authors declare that no competing interests exist.
  5. Dewi M Prawiradilaga

    Division of Zoology, Indonesian Institute of Sciences (LIPI), Jakarta, Indonesia
    Competing interests
    The authors declare that no competing interests exist.
  6. Martin Irestedt

    Department of Bioinformatics and Genetics, Swedish Museum of Natural History, Stockholm, Sweden
    Competing interests
    The authors declare that no competing interests exist.
  7. Fumin Lei

    Key Laboratory of Zoological Systematics and Evolution, Institute of Zoology (CAS), Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  8. Luke M Bloch

    Museum of Vertebrate Zoology and Department of Integrative Biology, University of California, Berkeley, Berkeley, United States
    Competing interests
    The authors declare that no competing interests exist.
  9. Jessica GH Lee

    Conservation, Wildlife Reserves Singapore, Singapore, Singapore
    Competing interests
    The authors declare that no competing interests exist.
  10. Mohammad Irham

    Division of Zoology, Indonesian Institute of Sciences (LIPI), Jakarta, Indonesia
    Competing interests
    The authors declare that no competing interests exist.
  11. Tri Haryoko

    Division of Zoology, Indonesian Institute of Sciences (LIPI), Jakarta, Indonesia
    Competing interests
    The authors declare that no competing interests exist.
  12. Malcolm CK Soh

    School of Biological Sciences, University of Western Australia, Perth, Australia
    Competing interests
    The authors declare that no competing interests exist.
  13. Kelvin S-H Peh

    School of Biological Sciences, University of Southampton, Southampton, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-2921-1341
  14. Karen MC Rowe

    Sciences Department, Museums Victoria, Victoria, Australia
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6131-6418
  15. Teuku Reza Ferasyi

    Faculty of Veterinary Medicine, Universitas Syiah Kuala, Banda Aceh, Indonesia
    Competing interests
    The authors declare that no competing interests exist.
  16. Shaoyuan Wu

    School of Life Sciences, Jiangsu Normal University, Jiangsu, China
    Competing interests
    The authors declare that no competing interests exist.
  17. Guinevere OU Wogan

    Museum of Vertebrate Zoology and Department of Environmental Science, Policy, and Management, University of California, Berkeley, Berkeley, United States
    Competing interests
    The authors declare that no competing interests exist.
  18. Rauri CK Bowie

    Museum of Vertebrate Zoology and Department of Integrative Biology, University of California, Berkeley, Berkeley, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8328-6021
  19. Frank E Rheindt

    Department of Biological Sciences, National University of Singapore, Singapore, Singapore
    For correspondence
    dbsrfe@nus.edu.sg
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8946-7085

Funding

Singapore Ministry of Education (R-154-000-A59-112)

  • Frank E Rheindt

Wildlife Reserved Singapore Conservation Fund (R-154-000-A99-592)

  • Frank E Rheindt

Croeni Foundation (R-154-000-A05-592)

  • Frank E Rheindt

SEABIG (R-154-000-648-646)

  • Balaji Chattopadhyay

SEABIG (R-154-000-648-733)

  • Balaji Chattopadhyay

University of Southampton research grant (511206105)

  • Kelvin S-H Peh

US National Science Foundation grant (DEB-1441652)

  • Rauri CK Bowie

US National Science Foundation grant (DEB-1457845)

  • Rauri CK Bowie

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

Reviewing Editor

  1. Rosalyn Gloag, University of Sidney, Australia

Version history

  1. Received: September 3, 2020
  2. Accepted: December 21, 2020
  3. Accepted Manuscript published: December 22, 2020 (version 1)
  4. Version of Record published: December 31, 2020 (version 2)
  5. Version of Record updated: January 6, 2021 (version 3)

Copyright

© 2020, Gwee 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

  • 1,983
    Page views
  • 285
    Downloads
  • 14
    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. Chyi Yin Gwee
  2. Kritika M Garg
  3. Balaji Chattopadhyay
  4. Keren R Sadanandan
  5. Dewi M Prawiradilaga
  6. Martin Irestedt
  7. Fumin Lei
  8. Luke M Bloch
  9. Jessica GH Lee
  10. Mohammad Irham
  11. Tri Haryoko
  12. Malcolm CK Soh
  13. Kelvin S-H Peh
  14. Karen MC Rowe
  15. Teuku Reza Ferasyi
  16. Shaoyuan Wu
  17. Guinevere OU Wogan
  18. Rauri CK Bowie
  19. Frank E Rheindt
(2020)
Phylogenomics of white-eyes, a 'great speciator', reveals Indonesian archipelago as the center of lineage diversity
eLife 9:e62765.
https://doi.org/10.7554/eLife.62765

Share this article

https://doi.org/10.7554/eLife.62765

Further reading

    1. Evolutionary Biology
    Zhiliang Zhang, Zhifei Zhang ... Guoxiang Li
    Research Article

    Biologically-controlled mineralization producing organic-inorganic composites (hard skeletons) by metazoan biomineralizers has been an evolutionary innovation since the earliest Cambrian. Among them, linguliform brachiopods are one of the key invertebrates that secrete calcium phosphate minerals to build their shells. One of the most distinct shell structures is the organo-phosphatic cylindrical column exclusive to phosphatic-shelled brachiopods, including both crown and stem groups. However, the complexity, diversity, and biomineralization processes of these microscopic columns are far from clear in brachiopod ancestors. Here, exquisitely well-preserved columnar shell ultrastructures are reported for the first time in the earliest eoobolids Latusobolus xiaoyangbaensis gen. et sp. nov. and Eoobolus acutulus sp. nov. from the Cambrian Series 2 Shuijingtuo Formation of South China. The hierarchical shell architectures, epithelial cell moulds, and the shape and size of cylindrical columns are scrutinised in these new species. Their calcium phosphate-based biomineralized shells are mainly composed of stacked sandwich columnar units. The secretion and construction of the stacked sandwich model of columnar architecture, which played a significant role in the evolution of linguliforms, is highly biologically controlled and organic-matrix mediated. Furthermore, a continuous transformation of anatomic features resulting from the growth of diverse columnar shells is revealed between Eoobolidae, Lingulellotretidae, and Acrotretida, shedding new light on the evolutionary growth and adaptive innovation of biomineralized columnar architecture among early phosphatic-shelled brachiopods during the Cambrian explosion.

    1. Developmental Biology
    2. Evolutionary Biology
    Eman Hijaze, Tsvia Gildor ... Smadar Ben-Tabou de-Leon
    Research Article

    Biomineralization had apparently evolved independently in different phyla, using distinct minerals, organic scaffolds, and gene regulatory networks (GRNs). However, diverse eukaryotes from unicellular organisms, through echinoderms to vertebrates, use the actomyosin network during biomineralization. Specifically, the actomyosin remodeling protein, Rho-associated coiled-coil kinase (ROCK) regulates cell differentiation and gene expression in vertebrates’ biomineralizing cells, yet, little is known on ROCK’s role in invertebrates’ biomineralization. Here, we reveal that ROCK controls the formation, growth, and morphology of the calcite spicules in the sea urchin larva. ROCK expression is elevated in the sea urchin skeletogenic cells downstream of the Vascular Endothelial Growth Factor (VEGF) signaling. ROCK inhibition leads to skeletal loss and disrupts skeletogenic gene expression. ROCK inhibition after spicule formation reduces the spicule elongation rate and induces ectopic spicule branching. Similar skeletogenic phenotypes are observed when ROCK is inhibited in a skeletogenic cell culture, indicating that these phenotypes are due to ROCK activity specifically in the skeletogenic cells. Reduced skeletal growth and enhanced branching are also observed under direct perturbations of the actomyosin network. We propose that ROCK and the actomyosin machinery were employed independently, downstream of distinct GRNs, to regulate biomineral growth and morphology in Eukaryotes.