Genomic trajectories of a near-extinction event in the Chatham Island black robin

Abstract

Background Understanding the micro-­evolutionary response of populations to demographic declines is a major goal in evolutionary and conservation biology. In small populations, genetic drift can lead to an accumulation of deleterious mutations, which will increase the risk of extinction. However, demographic recovery can still occur after extreme declines, suggesting that natural selection may purge deleterious mutations, even in extremely small populations. The Chatham Island black robin (Petroica traversi) is arguably the most inbred bird species in the world. It avoided imminent extinction in the early 1980s and after a remarkable recovery from a single pair, a second population was established and the two extant populations have evolved in complete isolation since then. Here, we analysed 52 modern and historical genomes to examine the genomic consequences of this extreme bottleneck and the subsequent translocation. Results We found evidence for two-fold decline in heterozygosity and three- to four-fold increase in inbreeding in modern genomes. Moreover, there was partial support for temporal reduction in total load for detrimental variation. In contrast, compared to historical genomes, modern genomes showed a significantly higher realised load, reflecting the temporal increase in inbreeding. Furthermore, the translocation induced only small changes in the frequency of deleterious alleles, with the majority of detrimental variation being shared between the two populations. Conclusion Our results highlight the dynamics of mutational load in a species that recovered from the brink of extinction, and show rather limited temporal changes in mutational load. We hypothesise that ancestral purging may have been facilitated by population fragmentation and isolation on several islands for thousands of generations and may have already reduced much of the highly deleterious load well before human arrival and introduction of pests to the archipelago. The majority of fixed deleterious variation was shared between the modern populations, but translocation of individuals with low mutational load could possibly mitigate further fixation of high-frequency deleterious variation.

An empirical test of the estimation of historical effective population size using Drosophila melanogaster

“…The method of Santiago et al (2020) has now been applied to different species, particularly in the last year, including insects, such as honeybees (Sang et al, 2022); birds, such as Black Robin (von Seth et al, 2022); fishes, such as turbot, seabream and seabass (Saura et al, 2021), Baltic herring (Atmore et al, 2022), pikeperch (De Los Ríos-Pérez et al, 2022, coho salmon (Martinez et al, 2022), catfish (Coimbra et al, 2023) and sailfish (Ferrette et al, 2023); wild mammals, such as grey wolf (Pacheco et al, 2022), killer whales (Kardos et al, 2023), sika deer (Iijima et al, 2023), scimitar-horned oryx (Humble et al, 2023) and gorilla (Alvarez-Estape et al, 2023); humans (Bird et al, 2023); domestic species, such as pigs (Krupa et al, 2022), cattle (Jin et al, 2022;Magnier et al, 2022), sheep (Djokic et al, 2023;Drzaic et al, 2022), horse (Criscione et al, 2022) and chicken (Gao et al, 2023;Liu et al, 2023); plants, such as walnut (Ding et al, 2022); crustaceans, such as Daphnia (Wersebe & Weider, 2023) and fungi (Singh et al, 2021). As suggested by Santiago et al (2020), the method is generally reliable for about 200 generations in the past, although…”

“…As suggested by Santiago et al (2020), the method is generally reliable for about 200 generations in the past, although the software provides values up to about 600 generations. The analyses carried out to date have followed this recommendation considering between 20 and 200 generations, or up to 300–400 generations in a couple of studies (Atmore et al, 2022; von Seth et al, 2022) and up to 700–800 in others (Gao et al, 2023; Singh et al, 2021). It is important to note that the linkage disequilibrium signal is diminished over time so that very far events cannot generally be inferred with precision.…”

“…In fact, Reid and Pinsky (2022) showed that the method exhibits ≥90% accuracy for detecting fast severe declines in population size, outperforming other methods. The method has also been applied to different sets of data from different species (Atmore et al, 2022;Bird et al, 2023;Ding et al, 2022;Ferrette et al, 2023;Pacheco et al, 2022;von Seth et al, 2022;Wersebe & Weider, 2023). However, the simulation tests have always a restricted scope, as the models simulated cannot encompass all the complexities of real genomes.…”

Genetic load and adaptive potential of a recovered avian species that narrowly avoided extinction

“…1D). Similar comparisons in different bird species have reported smaller losses in nucleotide diversity: the crested ibis and the Chatham Island black robin with a 1.8 fold loss (Feng et al 2019; von Seth et al 2022), or in heterozygosity levels: the New Zealand Saddleback, 4.16 fold (Taylor et al 2007); the Mangrove Finch: 1.32 fold (Lawson et al 2017); Greater Prairie Chicken: 1.26 fold (Bellinger et al 2003) (Supplementary Table 2). The resulting extremely low genetic diversity in the modern population of the Seychelles paradise flycatcher is considerably lower compared to other threatened bird species (Fig.…”

“…1D). Similar comparisons in different bird species have reported smaller losses in nucleotide diversity: the crested ibis and the Chatham Island black robin with a 1.8 fold loss (Feng et al 2019;von Seth et al 2022), or in heterozygosity levels: the New Zealand Saddleback, 4.16 fold (Taylor et al 2007); the Mangrove Finch: 1.32 fold (Lawson et al 2017);…”