Temporal loss of genome-wide and immunogenetic diversity in a near-extinct parrot

Abstract

Loss of genetic diversity threatens a species adaptive potential and long-term resilience. Predicted to be extinct by 2038, the orange-bellied parrot (Neophema chrysogaster) is a Critically Endangered migratory bird threatened by numerous viral, bacterial and fungal diseases. The species has undergone multiple population crashes, reaching a low of three wild-born females and 13 males in 2016 and is now represented by only a single wild population and individuals in the captive breeding program. Here we used our high-quality long-read reference genome, and contemporary and historical resequenced genomes from as early as 1829, to track the long-term genomic erosion and immunogenetic diversity decline in this species. 62% of genomic diversity was lost between historical (mean autosomal heterozygosity = 0.00149 {+/-} 0.000699 SD) and contemporary (0.00057 {+/-} 0.000026) parrots. A greater number and length of runs of homozygosity in contemporary samples was also observed. A temporal reduction of the number of alleles at Toll-like receptor genes was found (historical average alleles = 5.78 {+/-} 2.73; contemporary = 3.89 {+/-} 2.10), potentially exacerbating disease susceptibility in the contemporary population. Of particular concern is the new threat of avian influenza strain (HPAI) to Australia. We discuss the conservation implications of our findings and propose that hybridization and synthetic biology may be required to address the catastrophic loss of genetic diversity that has occurred this species in order to prevent extinction. Significance statementOrange-bellied parrots (Neophema chrysogaster) face a dire future, with extinction predicted by 2038 due to severe genetic diversity loss. This Critically Endangered species, now reduced to a single wild population and a captive breeding program, has lost 62% of its genomic diversity since 1829. Contemporary samples show a decline in immunogenetic diversity and signs of very recent inbreeding. Meaning birds today are more susceptible to disease events than birds a hundred years ago. Conservation efforts must consider hybridization and synthetic biology to counteract the catastrophic loss of genetic diversity to ensure the species survival. Our study underscores the urgent need for innovative strategies to preserve the adaptive potential and resilience of the orange-bellied parrot and other species in similar situations.