Genome-wide diversity in the California condor tracks its prehistoric abundance and decline

Jacqueline A Robinson; Rauri C K Bowie; Olga Dudchenko; Erez Lieberman Aiden; Sher L Hendrickson; Cynthia C Steiner; Oliver A Ryder; David P Mindell; Jeffrey D Wall

doi:10.1016/j.cub.2021.04.035

Genome-wide diversity in the California condor tracks its prehistoric abundance and decline

Curr Biol. 2021 Jul 12;31(13):2939-2946.e5. doi: 10.1016/j.cub.2021.04.035. Epub 2021 May 13.

Authors

Jacqueline A Robinson¹, Rauri C K Bowie², Olga Dudchenko³, Erez Lieberman Aiden⁴, Sher L Hendrickson⁵, Cynthia C Steiner⁶, Oliver A Ryder⁷, David P Mindell⁸, Jeffrey D Wall⁹

Affiliations

¹ Institute for Human Genetics, University of California, San Francisco, San Francisco, CA, USA. Electronic address: jacqueline.robinson@ucsf.edu.
² Department of Integrative Biology, University of California, Berkeley, Berkeley, CA, USA; Museum of Vertebrate Zoology, University of California, Berkeley, Berkeley, CA, USA.
³ The Center for Genome Architecture, Department of Molecular and Human Genetics, Baylor College of Medicine, Houston, TX, USA; Center for Theoretical and Biological Physics, Rice University, Houston, TX, USA.
⁴ The Center for Genome Architecture, Department of Molecular and Human Genetics, Baylor College of Medicine, Houston, TX, USA; Center for Theoretical and Biological Physics, Rice University, Houston, TX, USA; Shanghai Institute for Advanced Immunochemical Studies, ShanghaiTech, Pudong, China; Faculty of Science, UWA School of Agriculture and Environment, University of Western Australia, Perth, WA, Australia.
⁵ Department of Biology, Shepherd University, Shepherdstown, WV, USA.
⁶ San Diego Zoo Wildlife Alliance, Beckman Center for Conservation Research, Escondido, CA, USA.
⁷ San Diego Zoo Wildlife Alliance, Beckman Center for Conservation Research, Escondido, CA, USA; Department of Evolution, Behavior, and Ecology, University of California, San Diego, San Diego, CA, USA.
⁸ Museum of Vertebrate Zoology, University of California, Berkeley, Berkeley, CA, USA.
⁹ Institute for Human Genetics, University of California, San Francisco, San Francisco, CA, USA. Electronic address: jeff.wall@ucsf.edu.

PMID: 33989525
DOI: 10.1016/j.cub.2021.04.035

Abstract

Due to their small population sizes, threatened and endangered species frequently suffer from a lack of genetic diversity, potentially leading to inbreeding depression and reduced adaptability.¹ During the latter half of the twentieth century, North America's largest soaring bird,² the California condor (Gymnogyps californianus; Critically Endangered³), briefly went extinct in the wild. Though condors once ranged throughout North America, by 1982 only 22 individuals remained. Following decades of captive breeding and release efforts, there are now >300 free-flying wild condors and ∼200 in captivity. The condor's recent near-extinction from lead poisoning, poaching, and loss of habitat is well documented,⁴ but much about its history remains obscure. To fill this gap and aid future management of the species, we produced a high-quality chromosome-length genome assembly for the California condor and analyzed its genome-wide diversity. For comparison, we also examined the genomes of two close relatives: the Andean condor (Vultur gryphus; Vulnerable³) and the turkey vulture (Cathartes aura; Least Concern³). The genomes of all three species show evidence of historic population declines. Interestingly, the California condor genome retains a high degree of variation, which our analyses reveal is a legacy of its historically high abundance. Correlations between genome-wide diversity and recombination rate further suggest a history of purifying selection against linked deleterious alleles, boding well for future restoration. We show how both long-term evolutionary forces and recent inbreeding have shaped the genome of the California condor, and provide crucial genomic resources to enable future research and conservation.

Keywords: conservation; demographic history; extinction; genomics; inbreeding.

Publication types

Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

Animals
Ecosystem
Endangered Species*
Falconiformes / classification*
Falconiformes / genetics*
Female
Genome / genetics*
Genomics
Population Density

Grants and funding

UM1 HG009375/HG/NHGRI NIH HHS/United States