A genomic timescale for placental mammal evolution.

A genomic timescale for placental mammal evolution.
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DOI:
10.1126/science.abl8189
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发表时间:
2023-04-28
期刊:
Science (New York, N.Y.)
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产生所有现存胎盘哺乳动物的物种形成事件的精确模式和时间仍然存在争议。我们提供了一个全面的系统发育分析的遗传变异在241胎盘哺乳动物基因组组件的对齐,解决以前的问题,有限的基因组采样跨物种。我们使用基于连接和聚结的方法比较了中性全基因组范围内的基因组信号,询问了染色体间的系统发育变异,并分析了广泛的结构变异目录。在不同的数据集和分析方法中,序数间关系表现出相对较低的基因组冲突率。相反,X染色体与常染色体冲突的特点是多个独立的分支,在新生代辐射。基因组时间树揭示了白垩纪-古近纪(K-Pg)界线之前和之后的分支事件的积累,暗示了白垩纪大陆分隔和K-Pg灭绝在胎盘辐射中的重要作用。解决不同的环境力量可能在现代胎盘哺乳动物明显的爆炸性多样化中发挥的作用,对于理解它们现存和灭绝的形态和基因组多样性的进化背景至关重要。有限的全基因组序列比对样本活的哺乳动物生物多样性阻碍了基因组推断,到目前为止,这一直是有限的相对较小,高度约束的序列矩阵往往代表<2%的典型哺乳动物基因组。为了消除这种抽样偏差,我们使用了241个全基因组的比对,以全面识别和严格分析非编码,中性进化序列变异的结合和串联为基础的系统发育框架。这些分析之后,验证与多个类别的遗传信息结构变异。这种方法使得能够为胎盘哺乳动物生成一个强大的时间树,该时间树评估了不受蛋白质编码注释限制的数百个基因组基因座的年龄变化。从数据的多个处理推断出的合并和串联的遗传学是高度一致的,包括支持更高级别的分类分组,将灵长类动物+猫猴与树鼩(Euarchonta),蝙蝠+鲸偶蹄类动物+奇蹄目动物+食肉动物+穿山甲(Scrotifera),不包括蝙蝠的所有scrotiferans(Fereuungulata),以及食肉动物+穿山甲与奇蹄目动物(Zooamata)。然而,因为这些方法推断出一个单一的最佳树,他们掩盖了不完整的血统排序和历史杂交导致的系统发育冲突的签名。因此,我们还从分布在染色体上的数千个非编码基因座中推断出了基因突变,这些基因座具有历史上截然不同的重组率。在整个辐射的现代订单(如啮齿动物,灵长类动物,蝙蝠和食肉动物),我们观察到显着的差异从常染色体和X染色体,一个典型的模式与基因流的物种形成推断轨迹树。我们发现,在许多情况下,以前有争议的系统发育关系可以通过检查分布的冲突系统发育信号沿着染色体与可变的历史重组率来调和。谱系分歧时间估计是非常均匀的基因组位点和强大的广泛的敏感性分析,其中的基础数据,化石的限制,和时钟模型是不同的。在胎盘发育中最早的分支事件与晚白垩世大陆板块的断裂和海平面上升相吻合。这种异域物种形成的特征与大多数超序关系推断的低基因组冲突一致。相比之下,我们观察到的第二个脉冲的多样化后,立即叠加在一个插曲的快速土地出现的灭绝事件的古近纪(K-PG)。更大的地理连续性,加上动荡的气候变化和增加的生态景观,在这个时候提供了更多的机会,哺乳动物的多样化,在化石记录中描述。这些意见吻合增加系统发育的冲突内观察到的分支,在新生代多样化。我们的全基因组分析的多个类别的序列变异提供了最全面的评估胎盘哺乳动物胚胎发育,解决有争议的关系,并澄清哺乳动物多样化的时间。我们认为,白垩纪大陆分裂和谱系隔离的组合,其次是直接和间接的影响,K-Pg灭绝的时候,快速的土地出现,协同促进了加速多样化率的胎盘哺乳动物在新生代早期。胎盘哺乳动物进化的时间。超序数哺乳动物的多样化发生在白垩纪大陆分裂和海平面上升期间,几乎没有基因组不一致(饼图:左,常染色体;右,X染色体),这与异域物种形成一致。相比之下,古近纪托管intraordinal多样化的K-Pg大灭绝事件的后果,当分支表现出较高的基因组不一致与物种形成与基因流和不完整的谱系排序。
The precise pattern and timing of speciation events that gave rise to all living placental mammals remain controversial. We provide a comprehensive phylogenetic analysis of genetic variation across an alignment of 241 placental mammal genome assemblies, addressing prior concerns regarding limited genomic sampling across species. We compared neutral genome-wide phylogenomic signals using concatenation and coalescent-based approaches, interrogated phylogenetic variation across chromosomes, and analyzed extensive catalogs of structural variants. Interordinal relationships exhibit relatively low rates of phylogenomic conflict across diverse datasets and analytical methods. Conversely, X-chromosome versus autosome conflicts characterize multiple independent clades that radiated during the Cenozoic. Genomic time trees reveal an accumulation of cladogenic events before and immediately after the Cretaceous-Paleogene (K-Pg) boundary, implying important roles for Cretaceous continental vicariance and the K-Pg extinction in the placental radiation. Resolving the role that different environmental forces may have played in the apparent explosive diversification of modern placental mammals is crucial to understanding the evolutionary context of their living and extinct morphological and genomic diversity. Limited access to whole-genome sequence alignments that sample living mammalian biodiversity has hampered phylogenomic inference, which until now has been limited to relatively small, highly constrained sequence matrices often representing <2% of a typical mammalian genome. To eliminate this sampling bias, we used an alignment of 241 whole genomes to comprehensively identify and rigorously analyze noncoding, neutrally evolving sequence variation in coalescent and concatenation-based phylogenetic frameworks. These analyses were followed by validation with multiple classes of phylogenetically informative structural variation. This approach enabled the generation of a robust time tree for placental mammals that evaluated age variation across hundreds of genomic loci that are not restricted by protein coding annotations. Coalescent and concatenation phylogenies inferred from multiple treatments of the data were highly congruent, including support for higher-level taxonomic groupings that unite primates+colugos with treeshrews (Euarchonta), bats+cetartiodactyls+perissodactyls+carnivorans+ pangolins (Scrotifera), all scrotiferans excluding bats (Fereuungulata), and carnivorans+pangolins with perissodactyls (Zooamata). However, because these approaches infer a single best tree, they mask signatures of phylogenetic conflict that result from incomplete lineage sorting and historical hybridization. Accordingly, we also inferred phylogenies from thousands of noncoding loci distributed across chromosomes with historically contrasting recombination rates. Throughout the radiation of modern orders (such as rodents, primates, bats, and carnivores), we observed notable differences between locus trees inferred from the autosomes and the X chromosome, a pattern typical of speciation with gene flow. We show that in many cases, previously controversial phylogenetic relationships can be reconciled by examining the distribution of conflicting phylogenetic signals along chromosomes with variable historical recombination rates. Lineage divergence time estimates were notably uniform across genomic loci and robust to extensive sensitivity analyses in which the underlying data, fossil constraints, and clock models were varied. The earliest branching events in the placental phylogeny coincide with the breakup of continental landmasses and rising sea levels in the Late Cretaceous. This signature of allopatric speciation is congruent with the low genomic conflict inferred for most superordinal relationships. By contrast, we observed a second pulse of diversification immediately after the Cretaceous-Paleogene (K-Pg) extinction event superimposed on an episode of rapid land emergence. Greater geographic continuity coupled with tumultuous climatic changes and increased ecological landscape at this time provided enhanced opportunities for mammalian diversification, as depicted in the fossil record. These observations dovetail with increased phylogenetic conflict observed within clades that diversified in the Cenozoic. Our genome-wide analysis of multiple classes of sequence variation provides the most comprehensive assessment of placental mammal phylogeny, resolves controversial relationships, and clarifies the timing of mammalian diversification. We propose that the combination of Cretaceous continental fragmentation and lineage isolation, followed by the direct and indirect effects of the K-Pg extinction at a time of rapid land emergence, synergistically contributed to the accelerated diversification rate of placental mammals during the early Cenozoic. The timing of placental mammal evolution. Superordinal mammalian diversification took place in the Cretaceous during periods of continental fragmentation and sea level rise with little phylogenomic discordance (pie charts: left, autosomes; right, X chromosome), which is consistent with allopatric speciation. By contrast, the Paleogene hosted intraordinal diversification in the aftermath of the K-Pg mass extinction event, when clades exhibited higher phylogenomic discordance consistent with speciation with gene flow and incomplete lineage sorting.
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