1. Evolutionary Biology

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
https://doi.org/10.7554/eLife.62765
Share this article
Cite this article
  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
  2. Download BibTeX
  3. Download .RIS

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

  • 2,032
    views
  • 290
    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. 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

Categories and tags

Further reading

    1. Evolutionary Biology
    2. Genetics and Genomics

    Insights into early animal evolution form the genome of the xenacoelomorph worm Xenoturbella bocki

    Philipp H Schiffer, Paschalis Natsidis ... Maximilian J Telford
    Research Article

    The evolutionary origins of Bilateria remain enigmatic. One of the more enduring proposals highlights similarities between a cnidarian-like planula larva and simple acoel-like flatworms. This idea is based in part on the view of the Xenacoelomorpha as an outgroup to all other bilaterians which are themselves designated the Nephrozoa (protostomes and deuterostomes). Genome data can provide important comparative data and help to understand the evolution and biology of enigmatic species better. Here we assemble and analyse the genome of the simple, marine xenacoelomorph Xenoturbella bocki, a key species for our understanding of early bilaterian evolution. Our highly contiguous genome assembly of X. bocki has a size of ~111 Mbp in 18 chromosome like scaffolds, with repeat content and intron, exon and intergenic space comparable to other bilaterian invertebrates. We find X. bocki to have a similar number of genes to other bilaterians and to have retained ancestral metazoan synteny. Key bilaterian signalling pathways are also largely complete and most bilaterian miRNAs are present. Overall, we conclude that X. bocki has a complex genome typical of bilaterians, which does not reflect the apparent simplicity of its body plan that has been so important to proposals that the Xenacoelomorpha are the simple sister group of the rest of the Bilateria.

    1. Evolutionary Biology
    2. Microbiology and Infectious Disease

    Recombinant origin and interspecies transmission of a HERV-K(HML-2)-related primate retrovirus with a novel RNA transport element

    Zachary H Williams, Alvaro Dafonte Imedio ... Welkin E Johnson
    Research Article

    HERV-K(HML-2), the youngest clade of human endogenous retroviruses (HERVs), includes many intact or nearly intact proviruses, but no replication competent HML-2 proviruses have been identified in humans. HML-2-related proviruses are present in other primates, including rhesus macaques, but the extent and timing of HML-2 activity in macaques remains unclear. We have identified 145 HML-2-like proviruses in rhesus macaques, including a clade of young, rhesus-specific insertions. Age estimates, intact ORFs, and insertional polymorphism of these insertions are consistent with recent or ongoing infectious activity in macaques. 106 of the proviruses form a clade characterized by an ~750 bp sequence between env and the 3' LTR, derived from an ancient recombination with a HERV-K(HML-8)-related virus. This clade is found in Old World monkeys (OWM), but not great apes, suggesting it originated after the ape/OWM split. We identified similar proviruses in white-cheeked gibbons; the gibbon insertions cluster within the OWM recombinant clade, suggesting interspecies transmission from OWM to gibbons. The LTRs of the youngest proviruses have deletions in U3, which disrupt the Rec Response Element (RcRE), required for nuclear export of unspliced viral RNA. We show that the HML-8 derived region functions as a Rec-independent constitutive transport element (CTE), indicating the ancestral Rec-RcRE export system was replaced by a CTE mechanism.

    1. Evolutionary Biology

    Early evolution of the ecdysozoan body plan

    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.