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Species-wide genomics of kākāpō provides tools to accelerate recovery

Nature Ecology & Evolution volume 7, pages 1693–1705 (2023)Cite this article

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Abstract

The kākāpō is a critically endangered, intensively managed, long-lived nocturnal parrot endemic to Aotearoa New Zealand. We generated and analysed whole-genome sequence data for nearly all individuals living in early 2018 (169 individuals) to generate a high-quality species-wide genetic variant callset. We leverage extensive long-term metadata to quantify genome-wide diversity of the species over time and present new approaches using probabilistic programming, combined with a phenotype dataset spanning five decades, to disentangle phenotypic variance into environmental and genetic effects while quantifying uncertainty in small populations. We find associations for growth, disease susceptibility, clutch size and egg fertility within genic regions previously shown to influence these traits in other species. Finally, we generate breeding values to predict phenotype and illustrate that active management over the past 45 years has maintained both genome-wide diversity and diversity in breeding values and, hence, evolutionary potential. We provide new pathways for informing future conservation management decisions for kākāpō, including prioritizing individuals for translocation and monitoring individuals with poor growth or high disease risk. Overall, by explicitly addressing the challenge of the small sample size, we provide a template for the inclusion of genomic data that will be transformational for species recovery efforts around the globe.

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Fig. 1: Modern and historical spread of kākāpō, and pedigree of assayed individuals.
Fig. 2: Circos plot of kākāpō population genomics.

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Data availability

Genomic reads, variant data and phenotypic data are taonga of Ngāi Tahu and sensitive for the Department of Conservation. Raw and processed data, such as variant files, are available via application to the Aotearoa Genomic Data Repository https://data.agdr.org.nz/.

Code availability

Scripts, workflows, Jupyter notebooks and other methodology resources are available at the GitHub repo for this paper: https://github.com/GenomicsAotearoa/Kakapo or at Zenodo103.

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Acknowledgements

We are grateful to the Kākāpō125+ Project led by the New Zealand Department of Conservation (DOC) in partnership with Te Rūnanga o Ngāi Tahu (TRONT). We acknowledge the incredible long-term support and vision from Ngāi Tahu, DOC staff, including office-based support staff, and the many volunteers, veterinarians and others who have contributed to the conservation of this taonga species. Our thanks to the Genetic Rescue Foundation, University of Otago, New Zealand Genomics Limited, Rockefeller Institute, Duke University, Science Exchange and Experiment.com for the generation and availability of the short-read data used in this study. B.C.R. acknowledges support from the Department of Zoology, University of Otago, for funding sample preparation. We extend many thanks to Genomics Aotearoa for financial support of the project including for J.G., J.W., E.K., N.J.G., T.E.S., A.W.S. and P.K.D. We are very grateful to New Zealand eScience Infrastructure for computational resources and support, especially for assistance with data management, transfer and storage, and development and hosting of the AGDR (https://data.agdr.org.nz/), with particular thanks to Dinindu Senanayake.

Author information

Author notes

  1. These authors jointly supervised this work: Tammy E. Steeves, Anna W. Santure, Peter K. Dearden.

Authors and Affiliations

  1. Genomics Aotearoa, Biochemistry Department, School of Biomedical Sciences, University of Otago, Dunedin, Aotearoa New Zealand

    Joseph Guhlin, Marissa F. Le Lec & Peter K. Dearden

  2. School of Biological Sciences, University of Canterbury, Christchurch, Aotearoa New Zealand

    Jana Wold, Stephanie J. Galla & Tammy E. Steeves

  3. The New Zealand Institute for Plant and Food Research Ltd, Palmerston North, Aotearoa New Zealand

    Emily Koot

  4. School of Natural Sciences, Massey University, Palmerston North, Aotearoa New Zealand

    David Winter, Patrick J. Biggs & Murray P. Cox

  5. School of Veterinary Science, Massey University, Palmerston North, Aotearoa New Zealand

    Patrick J. Biggs

  6. Department of Biological Sciences, Boise State University, Boise, ID, USA

    Stephanie J. Galla

  7. Department of Anatomy, School of Biomedical Sciences, University of Otago, Dunedin, Aotearoa New Zealand

    Lara Urban & Neil J. Gemmell

  8. Helmholtz Pioneer Campus, Helmholtz Zentrum Muenchen, Neuherberg, Germany

    Lara Urban

  9. Helmholtz AI, Helmholtz Zentrum Muenchen, Neuherberg, Germany

    Lara Urban

  10. School of Life Sciences, Technical University of Munich, Freising, Germany

    Lara Urban

  11. Department of Zoology, University of Otago, Dunedin, Aotearoa New Zealand

    Yasmin Foster, Fiona E. Robertson & Bruce C. Robertson

  12. Department of Statistics, University of Auckland, Auckland, Aotearoa New Zealand

    Murray P. Cox

  13. Kākāpō Recovery Programme, Department of Conservation, Invercargill, Aotearoa New Zealand

    Andrew Digby, Lydia R. Uddstrom, Daryl Eason, Deidre Vercoe, Karen Andrew, Lisa Argilla, Karen Arnold, James Bohan, Liam Bolitho, Nichy Brown, Jo Carpenter, Jodie Crane, Margie Grant, Glen Greaves, Brett Halkett, Rory Hannan, Sam Haultain, Bryony Hitchcock, Leigh Joyce, Sara Larcombe, Jo Ledington, Jinty MacTavish, Phil Marsh, Gilbert Mingam, Freya Moore, Lyndsay Murray, Errol Nye, Jake Osborne, Lou Parker, Chris Phillips, Roy Phillips, Brodie Philp, Tim Raemaekers, Jenny Rickett, Rachel Rouse, Rachael Sagar, Alisha Sherriff, Theo Thompson, Jason Van de Wetering, Nicki van Zyl, Jen Waite & Jim Watts

  14. Rakiura Tītī Islands Administering Body, Invercargill, Aotearoa New Zealand

    Tāne Davis

  15. Neurogenetics of Language Lab, The Rockefeller University, New York, NY, USA

    Jason T. Howard

  16. Mirxes, Cambridge, MA, USA

    Jason T. Howard

  17. The Rockefeller University, New York, NY, USA

    Erich D. Jarvis

  18. Howard Hughes Medical Institute, Chevy Chase, MD, USA

    Erich D. Jarvis

  19. School of Biological Sciences, University of Auckland, Auckland, Aotearoa New Zealand

    Anna W. Santure

Authors
  1. Joseph Guhlin
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  2. Marissa F. Le Lec
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  3. Jana Wold
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  4. Emily Koot
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  5. David Winter
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  6. Patrick J. Biggs
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  7. Stephanie J. Galla
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  8. Lara Urban
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  9. Yasmin Foster
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  10. Murray P. Cox
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  11. Andrew Digby
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  12. Lydia R. Uddstrom
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  13. Daryl Eason
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  14. Deidre Vercoe
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  15. Tāne Davis
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  16. Jason T. Howard
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  17. Erich D. Jarvis
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  18. Fiona E. Robertson
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  19. Bruce C. Robertson
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  20. Neil J. Gemmell
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  21. Tammy E. Steeves
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  22. Anna W. Santure
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  23. Peter K. Dearden
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Consortia

Kākāpō Recovery Team

  • Karen Andrew
  • , Lisa Argilla
  • , Karen Arnold
  • , James Bohan
  • , Liam Bolitho
  • , Nichy Brown
  • , Jo Carpenter
  • , Jodie Crane
  • , Andrew Digby
  • , Daryl Eason
  • , Margie Grant
  • , Glen Greaves
  • , Brett Halkett
  • , Rory Hannan
  • , Sam Haultain
  • , Bryony Hitchcock
  • , Leigh Joyce
  • , Sara Larcombe
  • , Jo Ledington
  • , Jinty MacTavish
  • , Phil Marsh
  • , Gilbert Mingam
  • , Freya Moore
  • , Lyndsay Murray
  • , Errol Nye
  • , Jake Osborne
  • , Lou Parker
  • , Chris Phillips
  • , Roy Phillips
  • , Brodie Philp
  • , Tim Raemaekers
  • , Jenny Rickett
  • , Rachel Rouse
  • , Rachael Sagar
  • , Alisha Sherriff
  • , Theo Thompson
  • , Jason Van de Wetering
  • , Nicki van Zyl
  • , Deidre Vercoe
  • , Jen Waite
  •  & Jim Watts

Contributions

Conceptualization: all authors; methodology: J.G., M.F.L.L., E.K., D.W., P.J.B., S.J.G., A.W.S. and J.W.; software and formal analysis: J.G., M.F.L.L., E.K., D.W., P.J.B., S.J.G. and M.P.C.; validation: L.U., Y.F., D.W., P.J.B. and M.P.C.; investigation, resources and data curation: A.D., L.R.U., D.E., D.V., Kākāpō Recovery Team, L.U., B.C.R., F.E.R., D.W., P.J.B., M.P.C. and T.D.; writing—original draft: J.G.; writing—review and editing: J.G., P.K.D., M.F.L.L., A.W.S., L.U., E.D.J., Y.F., T.E.S., E.K., S.J.G., A.D., L.R.U., J.W. and N.J.G; visualization: J.G., E.K., M.F.L.L. and S.J.G.; supervision: T.E.S., A.W.S. and P.K.D.; project administration: J.G. and P.K.D.; funding acquisition: P.K.D., A.W.S., T.E.S., B.C.R., J.T.H. and E.D.J.

Corresponding author

Correspondence to Peter K. Dearden.

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The authors declare no competing interests.

Peer review

Peer review information

Nature Ecology & Evolution thanks Rebecca Taylor, Cock van Oosterhout and the other, anonymous, reviewer(s) for their contribution to the peer review of this work. Peer reviewer reports are available.

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Extended data

Extended Data Fig. 1 Plots of breeding values for Richard Henry lineages vs non Richard Henry lineages.

Violin plot of all calculated Breeding Values for each trait, with individual breeding values represented as points on the left of the distributions. Green points and distributions represent all birds exclusive of Richard Henry and his lineage, while tan represents Richard Henry and lineage scores (n = 8). Aspergillosis Risk is a risk score derived from case-control (see Supplemental Materials: Aspergillosis Susceptibility for details).

Extended Data Table 1 Relevant groupings for population statistics in kākāpō
Full size table

Supplementary information

Supplementary Information

Supplementary text including Supplementary Figs. 1–74.

Reporting Summary

Peer Review File

Supplementary Tables

Supplementary Tables 1–25.

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Guhlin, J., Le Lec, M.F., Wold, J. et al. Species-wide genomics of kākāpō provides tools to accelerate recovery. Nat Ecol Evol 7, 1693–1705 (2023). https://doi.org/10.1038/s41559-023-02165-y

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