The genetic basis of the kākāpō structural color polymorphism suggests balancing selection by an extinct apex predator

Urban, Lara, Santure, Anna W., Uddstrom, Lydia, Digby, Andrew, Vercoe, Deidre, Eason, Daryl, Crane, Jodie, Wylie, Matthew J., Davis, Tāne, LeLec, Marissa F., Guhlin, Joseph, Poulton, Simon, Slate, Jon, Alexander, Alana, Fuentes-Cross, Patricia, Dearden, Peter K., Gemmell, Neil J., Azeem, Farhan, Weyland, Marvin, Schwefel, Harald G. L., van Oosterhout, Cock ORCID: https://orcid.org/0000-0002-5653-738X and Morales, Hernán E. and Kākāpō Recovery Team (2024) The genetic basis of the kākāpō structural color polymorphism suggests balancing selection by an extinct apex predator. PLoS Biology, 22 (9). ISSN 1544-9173

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Abstract

AU The:information Pleaseconfirmthatallheadinglevelsarerepresentedcorrectly contained in population genomic data can tell : us much about the past ecology and evolution of species. We leveraged detailed phenotypic and genomic data of nearly all living kākāpō to understand the evolution of its feather color polymorphism. The kākāpō is an endangered and culturally significant parrot endemic to Aotearoa New Zealand, and the green and olive feather colorations are present at similar frequencies in the population. The presence of such a neatly balanced color polymorphism is remarkable because the entire population currently numbers less than 250 birds, which means it has been exposed to severe genetic drift. We dissected the color phenotype, demonstrating that the two colors differ in their light reflectance patterns due to differential feather structure. We used quantitative genomics methods to identify two genetic variants whose epistatic interaction can fully explain the species’ color phenotype. Our genomic forward simulations show that balancing selection might have been pivotal to establish the polymorphism in the ancestrally large population, and to maintain it during population declines that involved a severe bottleneck. We hypothesize that an extinct apex predator was the likely agent of balancing selection, making the color polymorphism in the kākāpō a “ghost of selection past.”

Item Type: Article
Additional Information: Funding Information: The Alexander von Humboldt Foundation (grant number DEU 1209620 FLF-P) provided financial support of LU for study design, data collection and analysis, and preparation of the manuscript. The European Research Council (ERODE, grant number 101078303) provided financial support of HEM for data analysis and preparation of the manuscript. Genomics Aotearoa (https://www.genomics-aotearoa.org.nz/) provided financial support for the project including for AWS, JG, PKD and NJG for study design, data collection and analysis, and preparation of the manuscript. The funders did not play any role in the study design, data collection and analysis, decision to publish, or preparation of the manuscript. Views and opinions expressed are those of the authors only and do not necessarily reflect those of the European Union or the European Research Council; neither the European Union nor the granting authority can be held responsible for them. This work has arisen from a partnership between Ng\u0101i Tahu and the Aotearoa New Zealand Department of Conservation Te Papa Atawhai (DOC), the K\u0101k\u0101p\u014D Recovery Programme, and the involved researchers. We thank the K\u0101k\u0101p\u014D125+ Project led by DOC in partnership with Ng\u0101i Tahu, 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 data used in this study. Thanks for their support with technical challenges and sample/data access goes to Elizabeth Girvan from the SEM facility, University of Otago, the University of Otago Physics Department, the Dodd-Walls Centre for Photonic and Quantum Technologies, Paul Scofield from the Canterbury Museum (also for the lovely tour), and Nic Dussex from the Swedish Museum of Natural History. Thanks for their support with computational analyses goes to the New Zealand eScience Infrastructure (NeSI), especially Dinindu Senanayake, and to Mirte Bosse, Ren\u00E9 Malenfant, Lars Ronnegard, Christiaan de Leeuw, and Fran\u00E7oise Thibaud-Nissen. We thank the K\u0101k\u0101p\u014D Recovery team: Karen Andrew, James Bohan, Nichy Brown, Jodie Crane, Galen Davitt, Andrew Digby, Daryl Eason, Liz Friend, Glen Greaves, Erica Hansen, Petrus Hedman, Bryony Hitchcock, Bronwyn Jeynes, Leigh Joyce, Sara Larcombe, Scott Latimer, Kate Lawrence, Sarah Little, Sarah Manktelow, Phil Marsh, Guy McDonald, Tommy McKerras, Servanne Kiss, Michael Mitchell, Ricki Ann Mitchell, Jake Osborne, Brodie Philp, Louise Porter, Tim Raemaekers, Jenny Rickett, Rachael Sagar, Alyssa Salton, Alisha Sherriff, Theo Thompson, Lydia Uddstrom, Lisa van Beek, Jason Van de Wetering, Maddie van de Wetering, Deidre Vercoe, Jen Waite, Richard Walle, Nia Weinzweig, Daniella Whitaker, and Maddy Whittaker Genomic data were collected as part of a previous study. Phenotypic data were collected for this study as part of the standard and ongoing management of the population by taking pictures and analyzing shed feathers, ensuring that no individual was subjected to any additional handling, treatment, or disturbance. Every step of the project was conducted in consultation with M\u0101ori iwi, in direct partnership with Ng\u0101i Tahu, and with the Aotearoa New Zealand Department of Conservation Te Papa Atawhai and its K\u0101k\u0101p\u014D Recovery Programme. Publisher Copyright: © 2024 Urban et al.
Uncontrolled Keywords: neuroscience(all),biochemistry, genetics and molecular biology(all),immunology and microbiology(all),agricultural and biological sciences(all) ,/dk/atira/pure/subjectarea/asjc/2800
Faculty \ School: Faculty of Science > School of Biological Sciences
Faculty of Science > School of Environmental Sciences
UEA Research Groups: Faculty of Science > Research Centres > Centre for Ecology, Evolution and Conservation
Related URLs:
Depositing User: LivePure Connector
Date Deposited: 30 Sep 2024 15:30
Last Modified: 19 Oct 2024 00:05
URI: https://ueaeprints.uea.ac.uk/id/eprint/96836
DOI: 10.1371/journal.pbio.3002755

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