When birds of a feather flock together: Severe genomic erosion and the implications for genetic rescue in an endangered island passerine

IF 3.5 2区 生物学 Q1 EVOLUTIONARY BIOLOGY
Emily L. Cavill, Hernán E. Morales, Xin Sun, Michael V. Westbury, Cock van Oosterhout, Wilna Accouche, Anna Zora, Melissa J. Schulze, Nirmal Shah, Pierre-André Adam, M. de L. Brooke, Paul Sweet, Shyam Gopalakrishnan, M. Thomas P. Gilbert
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Abstract

The Seychelles magpie-robin's (SMR) five island populations exhibit some of the lowest recorded levels of genetic diversity among endangered birds, and high levels of inbreeding. These populations collapsed during the 20th century, and the species was listed as Critically Endangered in the IUCN Red List in 1994. An assisted translocation-for-recovery program initiated in the 1990s increased the number of mature individuals, resulting in its downlisting to Endangered in 2005. Here, we explore the temporal genomic erosion of the SMR based on a dataset of 201 re-sequenced whole genomes that span the past ~150 years. Our sample set includes individuals that predate the bottleneck by up to 100 years, as well as individuals from contemporary populations established during the species recovery program. Despite the SMR's recent demographic recovery, our data reveal a marked increase in both the genetic load and realized load in the extant populations when compared to the historical samples. Conservation management may have reduced the intensity of selection by increasing juvenile survival and relaxing intraspecific competition between individuals, resulting in the accumulation of loss-of-function mutations (i.e. severely deleterious variants) in the rapidly recovering population. In addition, we found a 3-fold decrease in genetic diversity between temporal samples. While the low genetic diversity in modern populations may limit the species' adaptability to future environmental changes, future conservation efforts (including IUCN assessments) may also need to assess the threats posed by their high genetic load. Our computer simulations highlight the value of translocations for genetic rescue and show how this could halt genomic erosion in threatened species such as the SMR.

Abstract Image

物以类聚,人以群分:严重的基因组侵蚀及其对濒危岛屿鸟类基因拯救的影响。
在濒危鸟类中,塞舌尔鹊罗宾(SMR)的五个岛屿种群的遗传多样性水平最低,而且近亲繁殖程度很高。这些种群在 20 世纪崩溃,该物种于 1994 年被世界自然保护联盟(IUCN)红色名录列为极度濒危物种。20 世纪 90 年代启动的辅助迁移恢复计划增加了成熟个体的数量,因此该物种在 2005 年被降级为濒危物种。在此,我们基于过去约 150 年间重新测序的 201 个全基因组数据集,探讨了 SMR 在时间上的基因组侵蚀。我们的样本集包括比瓶颈发生时间早100年的个体,以及在物种恢复计划期间建立的当代种群中的个体。尽管SMR最近在人口方面有所恢复,但我们的数据显示,与历史样本相比,现存种群的遗传负荷和实现负荷都明显增加。保护管理可能通过提高幼体存活率和放松个体间的种内竞争来降低选择强度,从而导致功能缺失变异(即严重有害变异)在快速恢复的种群中积累。此外,我们还发现不同时间样本之间的遗传多样性下降了 3 倍。虽然现代种群的遗传多样性较低可能会限制该物种对未来环境变化的适应能力,但未来的保护工作(包括世界自然保护联盟的评估)可能还需要评估其高遗传负荷所带来的威胁。我们的计算机模拟突显了基因拯救迁移的价值,并展示了如何通过迁移来阻止基因组侵蚀对 SMR 等濒危物种的影响。
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来源期刊
Evolutionary Applications
Evolutionary Applications 生物-进化生物学
CiteScore
8.50
自引率
7.30%
发文量
175
审稿时长
6 months
期刊介绍: Evolutionary Applications is a fully peer reviewed open access journal. It publishes papers that utilize concepts from evolutionary biology to address biological questions of health, social and economic relevance. Papers are expected to employ evolutionary concepts or methods to make contributions to areas such as (but not limited to): medicine, agriculture, forestry, exploitation and management (fisheries and wildlife), aquaculture, conservation biology, environmental sciences (including climate change and invasion biology), microbiology, and toxicology. All taxonomic groups are covered from microbes, fungi, plants and animals. In order to better serve the community, we also now strongly encourage submissions of papers making use of modern molecular and genetic methods (population and functional genomics, transcriptomics, proteomics, epigenetics, quantitative genetics, association and linkage mapping) to address important questions in any of these disciplines and in an applied evolutionary framework. Theoretical, empirical, synthesis or perspective papers are welcome.
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