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.

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

  • 2,071
    views
  • 296
    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. 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. Ecology
    2. Evolutionary Biology
    Zhixian Zhang, Jianying Li ... Songdou Zhang
    Research Article

    Seasonal polyphenism enables organisms to adapt to environmental challenges by increasing phenotypic diversity. Cacopsylla chinensis exhibits remarkable seasonal polyphenism, specifically in the form of summer-form and winter-form, which have distinct morphological phenotypes. Previous research has shown that low temperature and the temperature receptor CcTRPM regulate the transition from summer-form to winter-form in C. chinensis by impacting cuticle content and thickness. However, the underling neuroendocrine regulatory mechanism remains largely unknown. Bursicon, also known as the tanning hormone, is responsible for the hardening and darkening of the insect cuticle. In this study, we report for the first time on the novel function of Bursicon and its receptor in the transition from summer-form to winter-form in C. chinensis. Firstly, we identified CcBurs-α and CcBurs-β as two typical subunits of Bursicon in C. chinensis, which were regulated by low temperature (10 °C) and CcTRPM. Subsequently, CcBurs-α and CcBurs-β formed a heterodimer that mediated the transition from summer-form to winter-form by influencing the cuticle chitin contents and cuticle thickness. Furthermore, we demonstrated that CcBurs-R acts as the Bursicon receptor and plays a critical role in the up-stream signaling of the chitin biosynthesis pathway, regulating the transition from summer-form to winter-form. Finally, we discovered that miR-6012 directly targets CcBurs-R, contributing to the regulation of Bursicon signaling in the seasonal polyphenism of C. chinensis. In summary, these findings reveal the novel function of the neuroendocrine regulatory mechanism underlying seasonal polyphenism and provide critical insights into the insect Bursicon and its receptor.

    1. Evolutionary Biology
    2. Genetics and Genomics
    Giulia Ferraretti, Paolo Abondio ... Marco Sazzini
    Research Article

    It is well established that several Homo sapiens populations experienced admixture with extinct human species during their evolutionary history. Sometimes, such a gene flow could have played a role in modulating their capability to cope with a variety of selective pressures, thus resulting in archaic adaptive introgression events. A paradigmatic example of this evolutionary mechanism is offered by the EPAS1 gene, whose most frequent haplotype in Himalayan highlanders was proved to reduce their susceptibility to chronic mountain sickness and to be introduced in the gene pool of their ancestors by admixture with Denisovans. In this study, we aimed at further expanding the investigation of the impact of archaic introgression on more complex adaptive responses to hypobaric hypoxia evolved by populations of Tibetan/Sherpa ancestry, which have been plausibly mediated by soft selective sweeps and/or polygenic adaptations rather than by hard selective sweeps. For this purpose, we used a combination of composite-likelihood and gene network-based methods to detect adaptive loci in introgressed chromosomal segments from Tibetan WGS data and to shortlist those presenting Denisovan-like derived alleles that participate to the same functional pathways and are absent in populations of African ancestry, which are supposed to do not have experienced Denisovan admixture. According to this approach, we identified multiple genes putatively involved in archaic introgression events and that, especially as regards TBC1D1, RASGRF2, PRKAG2, and KRAS, have plausibly contributed to shape the adaptive modulation of angiogenesis and of certain cardiovascular traits in high-altitude Himalayan peoples. These findings provided unprecedented evidence about the complexity of the adaptive phenotype evolved by these human groups to cope with challenges imposed by hypobaric hypoxia, offering new insights into the tangled interplay of genetic determinants that mediates the physiological adjustments crucial for human adaptation to the high-altitude environment.