Phylogenomic analyses of 2,786 genes in 158 lineages support a root of the eukaryotic tree of life between opisthokonts and all other lineages

Advances in phylogenetic methods and high-throughput sequencing have allowed the reconstruction of deep phylogenetic relationships in the evolutionary history of eukaryotes. Yet, the root of the eukaryotic tree of life remains elusive. The most 'popular' (i.e. in textbooks and reviews) hypothesis for the root is between Unikonta (Opisthokonta + Amoebozoa) and Bikonta (all other eukaryotes), which emerged from analyses of a single gene fusion and a limited sampling of eukaryotic lineages. Subsequent highly-cited studies based on concatenation of genes supported this hypothesis with some variations or proposed a root within the Excavata. However, concatenation of genes neither considers phylogenetically-informative events (i.e. gene duplications and losses) nor provides an estimate of the root. A more recent study using gene tree-species tree reconciliation methods suggested the root lies between Opisthokonta and all other eukaryotes, but only including 59 taxa and 20 genes. Here we apply a gene tree – species tree reconciliation approach to a gene-rich and taxon-rich dataset (i.e. 2,786 gene families from two sets of ~158 diverse eukaryotic lineages) to assess the root, and we iterate each analysis 100 times to quantify tree space uncertainty. Our results estimate a root between Fungi and all other eukaryotes, or between Opisthokonta and all other eukaryotes, and reject alternative popular roots from the literature. Based on further analysis of genome size, we propose Opisthokonta + others as the most likely root. Finding the root of the eukaryotic tree of life is critical for the field of comparative biology as it allows us to understand the timing and mode of evolution of characters across the evolutionary history of eukaryotes.

系统发育方法与高通量测序技术的进步，使得重构真核生物演化历史中的深层系统发育关系成为可能。然而，真核生物生命之树的根部位置至今仍不明确。目前教科书中与综述文献里最“流行”的根部假说，认为其位于单鞭毛生物（Unikonta，包含后鞭毛生物Opisthokonta与变形虫类Amoebozoa）和双鞭毛生物（Bikonta，其余所有真核生物类群）之间，该假说源自对单一基因融合事件的分析，且仅对有限的真核生物演化支进行了取样。后续基于基因串联分析的高引用研究，要么在部分修正后支持这一假说，要么提出根部位于古虫界（Excavata）内部。然而，基因串联分析既未考虑具有系统发育信息的演化事件（如基因重复与丢失），也无法对根部位置进行估算。近期一项采用基因树-物种树调和分析（gene tree-species tree reconciliation）的研究提出，根部位于后鞭毛生物与其余所有真核生物之间，但该研究仅纳入了59个类群与20个基因家族。本研究将基因树-物种树调和分析方法应用于类群与基因均较为丰富的数据集（即取自两组约158个多样化真核生物类群的2786个基因家族），以评估真核生物生命之树的根部位置；同时将每项分析重复100次，以量化树空间不确定性。研究结果将根部位置估算为真菌界与其余所有真核生物之间，或后鞭毛生物与其余所有真核生物之间，并推翻了文献中其他主流的根部假说。基于对基因组大小的进一步分析，我们提出后鞭毛生物与其余类群的分界为最可信的根部位置。确定真核生物生命之树的根部位置，对于比较生物学领域至关重要，因其能够帮助我们理解真核生物演化历史中各类性状出现的时间与演化模式。