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.

摘要 研究背景：解析种群对数量下降的微观进化响应，是进化生物学与保护生物学领域的核心研究目标之一。在小型种群中，遗传漂变（genetic drift）会导致有害突变（deleterious mutations）的累积，进而提升种群灭绝风险。然而，种群在经历极端数量下降后仍可实现恢复，这表明即便在极端小型的种群中，自然选择仍可能清除有害突变。
查塔姆岛黑知更鸟（Petroica traversi）无疑是全球近交程度最高的鸟类。该物种在20世纪80年代初避免了迫在眉睫的灭绝：从仅存的一对个体实现显著恢复后，研究人员建立了第二个种群，自此两个现存种群便处于完全隔离的进化状态。本研究对52份现代与历史基因组进行分析，以解析此次极端种群瓶颈及后续种群易地转移事件带来的基因组层面影响。
研究结果：我们发现现代基因组的杂合度较历史样本下降了50%（即两倍降幅），近交程度提升了3至4倍。此外，研究结果部分支持有害变异总负荷随时间推移有所降低这一假说。与之形成对比的是，相较于历史基因组，现代基因组的实际突变负荷显著更高，这反映出近交程度随时间的提升。此外，此次种群易地转移仅对有害等位基因（deleterious alleles）的频率造成了小幅改变，绝大多数有害变异在两个种群间均存在共享。
研究结论：我们的研究结果揭示了一种从灭绝边缘恢复的物种的突变负荷动态，并表明突变负荷随时间的变化幅度相当有限。我们提出假说：数千代以来，多个岛屿上的种群碎片化与隔离状态可能促进了祖先种群的突变清除（ancestral purging），且早在人类抵达该群岛并引入外来害虫之前，这类清除便已大幅降低了绝大多数高度有害的突变负荷。两个现代种群间共享绝大多数已固定的有害变异，但通过转移携带低突变负荷的个体，或可缓解高频有害变异的进一步固定。