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Genetic structure and population history in two critically endangered Kaua‘i honeycreepers

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Abstract

Population sizes of endemic songbirds on Kaua‘i have decreased by an order of magnitude over the past 10–15 years to dangerously low numbers. The primary cause appears to be the ascent of invasive mosquitoes and Plasmodium relictum, the agent of avian malaria, into elevations formerly free of introduced malarial parasites and their vectors. Given that these declines in native bird populations appear to be continuing, last resort measures to save these species from extinction, such as conservation breeding, are being implemented. Using 200–1439 SNPs from across the genome, we assessed kinship among individuals, levels of genetic variation, and extent of population decline in wild birds of the two most critically endangered Kaua‘i endemic species, the ‘akikiki (Oreomystis bairdi) and ‘akeke‘e (Loxops caeruleirostris). We found relatively high genomic diversity within individuals and little evidence of spatial population genetic structure. Populations displayed genomic signatures of declining population size, but individual inbreeding coefficients were universally negative, likely indicating inbreeding avoidance. Diversity within the founding conservation breeding population largely mirrored that in the wild, indicating that genetic variation in the conservation breeding population is representative of the wild population and suggesting that the current breeding program captures existing variation. Thus, although existing genetic diversity is likely lower than in historical populations, contemporary variation has been retained through high gene flow and inbreeding avoidance. Nonetheless, current effective population size for both species was estimated at fewer than 20 individuals, highlighting the urgency of management actions to protect these species.

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Availability of data and materials

Sequence reads have been published on GenBank as individual fastq files for each individual under BioProject PRJNA527134.

Code availability

All software is publicly and freely available, and all custom scripts are published on GitHub.

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Acknowledgements

Blood samples from individuals in the conservation breeding population were collected following San Diego Zoo Wildlife Alliance IACUC 18-022. We are thankful to Carter Atkinson, U.S. Geological Survey, Pacific Island Ecosystems Research Center, for sharing blood samples collected in the Alaka‘i during the 1990s and to Katy Parise for DNA extractions. We are grateful to the Kaua‘i Forest Bird Recovery Project field crews and the San Diego Zoo Wildlife Alliance crews for their tremendous dedication to catching all the wild birds and to finding, collecting, and hatching the eggs. The establishment of the conservation breeding population was funded by the U.S. Fish and Wildlife Service, State of Hawai‘i, San Diego Zoo Wildlife Alliance, and the Mohamed Bin Zayed Species Conservation Fund. Funding to collect samples from wild individuals and for genetic analysis was in part provided by the U.S. Fish and Wildlife Service, the State of Hawai‘i, NSF DEB-1547168, Ann Beeson, and Friends of the National Zoo’s Small Grant program. We appreciate comments on the manuscript from the @CrawLab and Cadena Lab at Universidad de los Andes and from two anonymous reviewers. Any use of trade, product, or firm names is for descriptive purposes only and does not imply endorsement by the U.S. Government.

Funding

U.S. Fish and Wildlife Service, State of Hawai‘i, San Diego Zoo Wildlife Alliance, Mohamed Bin Zayed Species Conservation Fund, Friends of the National Zoo.

Author information

Author notes

  1. Loren Cassin-Sackett

    Present address: Department of Biology, University of Louisiana, Lafayette, LA, USA

Authors and Affiliations

  1. Center for Conservation Genomics, Smithsonian Conservation Biology Institute, Washington, DC, USA

    Loren Cassin-Sackett, Michael G. Campana, Nancy Rotzel McInerney, Haw Chuan Lim, Natalia A. S. Przelomska & Robert C. Fleischer

  2. Department of Biology, George Mason University, Fairfax, VA, USA

    Haw Chuan Lim

  3. Department of Anthropology, National Museum of Natural History, Washington, DC, USA

    Natalia A. S. Przelomska

  4. Comparative Plant and Fungal Biology, Royal Botanic Gardens, Kew, Richmond, UK

    Natalia A. S. Przelomska

  5. Conservation Science and Wildlife Health, San Diego Zoo Wildlife Alliance, Volcano, HI, USA

    Bryce Masuda

  6. U.S. Geological Survey, Eastern Ecological Science Center, Laurel, MD, USA

    R. Terry Chesser

  7. Department of Vertebrate Zoology, National Museum of Natural History, Washington, DC, USA

    R. Terry Chesser

  8. U.S. Geological Survey Pacific Island Ecosystems Research Center, Hawai‘i National Park, HI, USA

    Eben H. Paxton

  9. Pathogen and Microbiome Institute, Northern Arizona University, Flagstaff, AZ, USA

    Jeffrey T. Foster

  10. Kaua‘i Forest Bird Recovery Project, Pacific Cooperative Studies Unit, Hanapepe, HI, USA

    Lisa H. Crampton

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Contributions

This study was conceived and designed by LHC, BM, EHP, RCF, LCS and MGC. Material preparation, data collection, and data analysis were performed by LCS, MGC, NRM, HCL, NASP, BM, RTC, EHP, JTF, LHC and RCF. The first draft of the manuscript was written by LCS with MGC and RCF, and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Loren Cassin-Sackett.

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All authors participated in the project and have seen this manuscript.

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Ethical approval

Blood sample collection protocols from individuals in the conservation breeding population were approved by San Diego Zoo Wildlife Alliance IACUC 18-022.

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Cassin-Sackett, L., Campana, M.G., McInerney, N.R. et al. Genetic structure and population history in two critically endangered Kaua‘i honeycreepers. Conserv Genet 22, 601–614 (2021). https://doi.org/10.1007/s10592-021-01382-x

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  • DOI: https://doi.org/10.1007/s10592-021-01382-x

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