Genetic purging in an island-endemic pigeon recovering from the brink of extinction

Abstract

In many endangered species with increased homozygosity, population recovery is limited by expressed deleterious mutations. In contrast, the critically endangered red-headed wood pigeon, endemic to an isolated oceanic archipelago of ~100 km², experienced a dramatic population increase three years after the removal of introduced predators, despite being nearly extinct in the 2000s. To understand the reason for this recovery, we sequenced and analysed its genome. We find that over 80% of the genome is homozygous due to centuries of inbreeding, yet the frequency of highly deleterious mutations is lower than in widespread conspecifics. Linkage disequilibrium-based analysis suggests that the effective population size declined from several thousand to fewer than a hundred in the early 20th century due to human impacts. Gradual inbreeding in a historically small population before human impact may have purged part of the mutation load, facilitating the recovery. Our study highlights the role of historical demography in the persistence of bottlenecked populations, with implications for biological conservation.

Fig. 1. Distribution and population history of the critically endangered red-headed wood pigeon (Columba janthina nitens) and the widespread Japanese wood pigeon (C. j. janthina).

The distribution area was redrawn from Seki et al.. The plot of effective population size (N_e) from 0.01 to 1 million years ago (Mya) was redrawn based on PSMC results presented in Tsujimoto et al. to illustrate contrasting demographic histories between the two subspecies.

Fig. 2. Inbreeding and deleterious mutations in wild and captive red-headed wood pigeons and Japanese wood pigeons.

a Distribution of runs of homozygosity (ROH) longer than 1 Mb and nonsense single nucleotide polymorphisms (SNPs) on the genome. Each line represents an individual (e.g., NA030). For clarity, only the 10 largest autosomes are shown here; the analysis covered all 38 autosomes. b Individual inbreeding coefficients (F_ROH), calculated as the fraction of the genome in ROH regions longer than 0.1, 1, or 10 Mb. c Allele frequency of each nonsense SNP. Grey lines connect six SNPs found in all three populations. d Proportion of nonsense effects relative to silent effects of derived alleles for each sample.

Fig. 3. Relationship between inbreeding coefficient and log-transformed longevity (days) in 119 captive red-headed wood pigeons.

The solid line represents the fitted linear regression model (F_1,117 = 2.73, p = 0.101). The estimated slope was β = 3.75 (95% CI: −0.70 to 8.19).

Fig. 4. Recent changes in effective population size (N_e) of red-headed wood pigeons.

N_e was estimated from linkage disequilibrium on macrochromosomes of 8 individuals sampled between 2001 and 2021. The orange ribbon represents the 95% confidence interval based on 100 bootstrap replicates, and the orange line shows the geometric mean. Estimates were repeated assuming average recombination rates of 1 and 2 cM/Mb on macrochromosomes. The black line represents changes in the human population of the Ogasawara Islands. The generation time of 3.58 years was used to convert generations into years. Note that estimates during the sampling period can be less accurate.