Genomic signatures of inbreeding depression for a threatened Aotearoa New Zealand passerine

• Published in: Molecular ecology 2023-04, Vol.32 (8), p.1893-1907
• Main Authors: Duntsch, Laura, Whibley, Annabel, Villemereuil, Pierre, Brekke, Patricia, Bailey, Sarah, Ewen, John G., Santure, Anna W.
• Format: Article
• Language: English
• Subjects: Animal reproduction; Animals; Breeding; Breeding success; conservation genomics; Fitness; Genome-Wide Association Study; Genomes; genomic inbreeding; Genomics; Habitat loss; Homozygote; Humans; Inbreeding; Inbreeding Depression; New Zealand; Notiomystis cincta; Nucleotides; Passeriformes; Polymorphism; Polymorphism, Single Nucleotide - genetics; Reproduction; Reproductive fitness; runs of homozygosity; Single-nucleotide polymorphism; SNP array; Success; Survival; Threatened species; Translocation
• ISSN: 0962-1083; 1365-294X
• DOI: 10.1111/mec.16855

For small and isolated populations, the increased chance of mating between related individuals can result in a substantial reduction in individual and population fitness. Despite the increasing availability of genomic data to measure inbreeding accurately across the genome, inbreeding depression studies for threatened species are still scarce due to the difficulty of measuring fitness in the wild. Here, we investigate inbreeding and inbreeding depression for the extensively monitored Tiritiri Mātangi island population of a threatened Aotearoa New Zealand passerine, the hihi (Notiomystis cincta). First, using a custom 45 k single nucleotide polymorphism (SNP) array, we explore genomic inbreeding patterns by inferring homozygous segments across the genome. Although all individuals have similar levels of ancient inbreeding, highly inbred individuals are affected by recent inbreeding, which can probably be explained by bottleneck effects such as habitat loss after European arrival and their translocation to the island in the 1990s. Second, we investigate genomic inbreeding effects on fitness, measured as lifetime reproductive success, and its three components, juvenile survival, adult annual survival and annual reproductive success, in 363 hihi. We find that global inbreeding significantly affects juvenile survival but none of the remaining fitness traits. Finally, we employ a genome‐wide association approach to test the locus‐specific effects of inbreeding on fitness, and identify 13 SNPs significantly associated with lifetime reproductive success. Our findings suggest that inbreeding depression does impact hihi, but at different genomic scales for different traits, and that purging has therefore failed to remove all variants with deleterious effects from this population of conservation concern.