Variation in Stem Anatomical Characteristics of Campanuloideae Species in Relation to Evolutionary History and Ecological Preferences

Background
The detailed knowledge of plant anatomical characters and their variation among closely related taxa is key to understanding their evolution and function. We examined anatomical variation in 46 herbaceous taxa from the subfamily Campanuloideae (Campanulaceae) to link this information with their phylogeny, ecology and comparative material of 56 woody tropical taxa from the subfamily Lobelioideae. The species studied covered major environmental gradients from Mediterranean to Arctic zones, allowing us to test hypotheses on the evolution of anatomical structure in relation to plant competitive ability and ecological preferences.
Methodology/Principal Findings
To understand the evolution of anatomical diversity, we reconstructed the phylogeny of studied species from nucleotide sequences and examined the distribution of anatomical characters on the resulting phylogenetic tree. Redundancy analysis, with phylogenetic corrections, was used to separate the evolutionary inertia from the adaptation to the environment. A large anatomical diversity exists within the Campanuloideae. Traits connected with the quality of fibres were the most congruent with phylogeny, and the Rapunculus 2 (“phyteumoid”) clade was especially distinguished by a number of characters (absence of fibres, pervasive parenchyma, type of rays) from two other clades (Campanula s. str. and Rapunculus 1) characterized by the dominance of fibres and the absence of parenchyma. Septate fibres are an exclusive trait in the Lobelioideae, separating it clearly from the Campanuloideae where annual rings, pervasive parenchyma and crystals in the phellem are characteristic features.
Conclusions/Significance
Despite clear phylogenetic inertia in the anatomical features studied, the ecological attributes and plant height had a significant effect on anatomical divergence. From all three evolutionary clades, the taller species converged towards similar anatomical structure, characterized by a smaller number of early wood vessels of large diameter, thinner cell-walls and alternate intervessel pits, while the opposite trend was found in small Arctic and alpine taxa. This supports the existing generalization that narrower vessels allow plants to grow in colder places where they can avoid freezing-induced embolism, while taller plants have wider vessels to minimize hydraulic resistance with their greater path lengths.

研究背景
植物解剖特征及其近缘类群间的变异细节，是理解植物演化与功能的核心关键。本研究针对桔梗科（Campanulaceae）桔梗亚科（Campanuloideae）的46个草本类群开展解剖变异分析，并结合来自半边莲亚科（Lobelioideae）的56个木本热带类群的对比材料，将解剖特征信息与其系统发育（phylogeny）、生态特征相关联。所研究的物种覆盖了从地中海气候区到北极圈的主要环境梯度，使我们得以检验关于解剖结构演化与植物竞争能力、生态偏好相关的假说。

研究方法/主要发现
为解析解剖多样性的演化机制，我们基于核苷酸序列（nucleotide sequences）重建了研究物种的系统发育（phylogeny）关系，并在所得系统发育树上分析了解剖特征的分布模式。采用系统发育校正后的冗余分析（redundancy analysis），将演化惯性与环境适应性分离开来。
桔梗亚科内存在丰富的解剖多样性。与纤维品质相关的性状与系统发育（phylogeny）的一致性最高；长柱风铃草2群（"phyteumoid"）演化支（clade）凭借一系列特征（无纤维、普遍存在的薄壁组织（parenchyma）、射线（rays）类型）显著区别于另外两个演化支（clade）——狭义风铃草属（Campanula s. str.）和长柱风铃草1群，后两者以纤维占主导且缺乏薄壁组织（parenchyma）为特征。分隔纤维（septate fibres）是半边莲亚科的独有性状，可将其与桔梗亚科清晰区分；桔梗亚科的典型特征为生长轮、普遍存在的薄壁组织（parenchyma）以及木栓层（phellem）中的晶体。

研究结论/研究意义
尽管所研究的解剖特征存在显著的系统发育（phylogeny）惯性，但生态属性与植物高度对解剖特征分化具有显著影响。三个演化支（clade）中的高大物种均趋同演化出相似的解剖结构：早材导管数量更少、管径更大、细胞壁更薄且管间纹孔为互生型；而小型北极和高山类群则呈现相反的趋势。这一结果支持了现有共识：较窄的导管使植物能够在寒冷环境中生长，避免冻融诱导的栓塞（embolism）；而高大植物则拥有更宽的导管，以降低因输水路径更长带来的水力阻力。