Phylogenomic discordance suggests polytomies along the backbone of the large genus Solanum

Premise of the study: Evolutionary studies require solid phylogenetic frameworks, but increased volumes of phylogenomic data have revealed incongruent topologies among gene trees in many organisms both between and within genomes. Some of these incongruences indicate polytomies that may remain impossible to resolve. Here we investigate the degree of gene-tree discordance in Solanum, one of the largest flowering plant genera that includes the cultivated potato, tomato, and eggplant, as well as 24 minor crop plants.

Methods: A densely sampled species-level phylogeny of Solanum is built using unpublished and publicly available Sanger sequences comprising 60% of all accepted species (742 spp.) and nine regions (ITS, waxy, and seven plastid markers). The robustness of this topology is tested by examining a full plastome dataset with 140 species and a nuclear target-capture dataset with 39 species of Solanum (Angiosperms353 probe set).

Key results: While the taxonomic framework of Solanum remained stable, gene tree conflicts and discordance between phylogenetic trees generated from the target-capture and plastome datasets were observed. The latter correspond to regions with short internodal branches, and network analysis and polytomy tests suggest the backbone is composed of three polytomies found at different evolutionary depths. The strongest area of discordance, near the crown node of Solanum, could potentially represent a hard polytomy.

Conclusions: We argue that incomplete lineage sorting due to rapid diversification is the most likely cause for these polytomies, and that embracing the uncertainty that underlies them is crucial to understand the evolution of large and rapidly radiating lineages.

研究背景：进化生物学研究依赖可靠的系统发育框架，但随着系统基因组学数据体量的快速增长，诸多生物类群的基因组内与基因组间的基因树拓扑结构均呈现出不一致现象。其中部分不一致现象指向了迄今仍无法解析的多歧支（polytomy）。本研究以茄属（Solanum）为研究对象，该属是开花植物中最大的类群之一，涵盖栽培马铃薯、番茄、茄子以及24种次要作物，旨在量化该类群中的基因树冲突程度。
研究方法：本研究整合未发表及公开可得的桑格（Sanger）序列，构建了茄属物种级高密度系统发育树，覆盖60%的已确认物种（共计742种），涉及9个分子标记区域：内部转录间隔区（ITS）、蜡质（waxy）基因以及7个质体标记。为验证该拓扑结构的稳健性，本研究分别采用包含140个茄属物种的全质体基因组（plastome）数据集，以及采用被子植物353探针套装（Angiosperms353 probe set）构建的、包含39个茄属物种的核基因组目标捕获（target-capture）数据集进行验证。
主要结果：尽管茄属的分类框架整体保持稳定，但本研究仍观察到基于目标捕获数据集与质体基因组数据集构建的系统发育树存在基因树冲突与拓扑不一致现象。这类不一致集中出现在节间分支较短的区域；网络分析与多歧支检验结果显示，茄属系统发育主干由三个处于不同演化深度的多歧支构成。其中冲突最显著的区域位于茄属冠节点附近，极有可能为硬多歧支（hard polytomy）。
研究结论：本研究认为，快速辐射演化引发的不完全谱系分选是导致上述多歧支现象的最可能成因；正视这类多歧支背后的不确定性，对于解析大型快速辐射演化类群的演化历程至关重要。