Kearns Anna M, Campana Michael G, Slikas Beth, Berry Lainie, Saitoh Takema, Graves Gary R, Cibois Alice, Fleischer Robert C
Center for Conservation Genomics, Smithsonian's National Zoo and Conservation Biology Institute, Washington, DC, United States.
Australian National Wildlife Collection, CSIRO National Research Collections Australia, Canberra, Australia.
Evolution. 2024 Dec 2;78(12):1900-1915. doi: 10.1093/evolut/qpae136.
Island radiations, such as those of the Australo-Pacific, offer unique insight into diversification, extinction, and early speciation processes. Yet, their speciation and colonization histories are often obscured by conflicting genomic signals from incomplete lineage sorting (ILS) or hybridization. Here, we integrated mitogenomes and genome-wide SNPs to unravel the evolutionary history of one of the world's most geographically widespread island radiations. The Australo-Pacific reed warblers (Acrocephalus luscinius complex) are a speciose lineage including five species that have become extinct since the 19th century and ten additional species of conservation concern. The radiation spans over 10,000 km across Australo-Papua, Micronesia and Polynesia, including the Mariana, Hawaii and Pitcairn Island archipelagos. Earlier mtDNA studies suggested a stepping-stone colonization process, resulting in archipelago-level secondary sympatry of divergent mtDNA lineages in the Mariana Islands and Marquesas. These studies hypothesized that morphologically similar species on neighboring islands arose from ecological convergence. Using DNA from historical museum specimens and modern genetic samples, we show that ILS and/or gene flow have shaped the radiation of Australo-Pacific reed warblers rather than secondary sympatry. The nuclear genome reconstructs a simpler biogeographic history than mtDNA, showing close relationships between species in the Mariana Islands and Marquesas despite their paraphyletic mtDNA lineages. Gene flow likely involved early and late colonizing waves of the radiation before the loss of ancestral dispersive ability. Our results highlight how collection genomics can elucidate evolutionary history and inform conservation efforts for threatened species.
岛屿辐射，如澳大拉西亚 - 太平洋地区的辐射，为多样化、灭绝和早期物种形成过程提供了独特的见解。然而，它们的物种形成和殖民历史常常被不完全谱系分选（ILS）或杂交产生的相互冲突的基因组信号所掩盖。在这里，我们整合了线粒体基因组和全基因组单核苷酸多态性（SNP），以揭示世界上地理分布最广的岛屿辐射之一的进化历史。澳大拉西亚 - 太平洋苇莺（Acrocephalus luscinius复合体）是一个物种丰富的谱系，包括自19世纪以来灭绝的5个物种以及另外10个受保护关注的物种。这种辐射跨越澳大拉西亚 - 巴布亚、密克罗尼西亚和波利尼西亚超过10000公里的区域，包括马里亚纳、夏威夷和皮特凯恩群岛。早期的线粒体DNA研究表明是一种踏脚石式的殖民过程，导致马里亚纳群岛和马克萨斯群岛中不同线粒体DNA谱系在群岛层面的次生同域分布。这些研究推测相邻岛屿上形态相似的物种是由生态趋同产生的。利用历史博物馆标本和现代遗传样本的DNA，我们表明ILS和/或基因流塑造了澳大拉西亚 - 太平洋苇莺的辐射，而非次生同域分布。核基因组重建的生物地理历史比线粒体DNA更简单，显示出马里亚纳群岛和马克萨斯群岛的物种之间存在密切关系，尽管它们的线粒体DNA谱系是并系的。基因流可能涉及在祖先扩散能力丧失之前该辐射早期和晚期的殖民浪潮。我们的结果突出了采集基因组学如何能够阐明进化历史并为受威胁物种的保护工作提供信息。
