Stabilized morphological evolution of spiders despite mosaic changes in foraging ecology

A prominent question in animal research is how the evolution of morphology and ecology interact in the generation of phenotypic diversity. Spiders are some of the most abundant arthropod predators in terrestrial ecosystems and exhibit a diversity of foraging styles. It remains unclear how spider body size and proportions relate to foraging style, and if the use of webs as prey capture devices correlates with changes in body characteristics. Here we present the most extensive dataset to date of morphometric and ecological traits in spiders. We used this dataset to estimate the change in spider body sizes and shapes over deep time and to test if and how spider phenotypes are correlated with their behavioural ecology. We found that phylogenetic variation of most traits best fitted an Ornstein-Uhlenbeck model, which is a model of stabilizing selection. A prominent exception was body length, whose evolutionary dynamics were best explained with a Brownian Motion (free trait diffusion) model. This was most expressed in the araneoid clade (ecribellate orb-weaving spiders and allies) that showed bimodal trends towards either miniaturization or gigantism. Only few traits differed significantly between ecological guilds, most prominently leg length and thickness, and although a multivariate framework found general differences in traits among ecological guilds, it was not possible to unequivocally associate a set of morphometric traits with the relative ecological mode. Long, thin legs have often evolved with aerial webs and a hanging (suspended) locomotion style, but this trend is not general. Eye size and fang length did not differ between ecological guilds, rejecting the hypothesis that webs reduce the need for visual cue recognition and prey immobilization. For the inference of the ecology of species with unknown behaviours, we propose not to use morphometric traits, but rather consult (micro-)morphological characters, such as the presence of certain podal structures. These results suggest that, in contrast to insects, the evolution of body proportions in spiders is unusually stabilized, and ecological adaptations are dominantly realized by behavioural traits and extended phenotypes in this group of predators. This work demonstrates the power of combining recent advances in phylogenomics with trait-based approaches to better understand global functional diversity patterns through space and time.

在动物研究领域，形态学和生态学如何相互作用以产生表型多样性，是一个引人注目的课题。蜘蛛作为陆地生态系统中数量最丰富的节肢动物捕食者之一，展现了多样的觅食风格。蜘蛛的身体大小和比例与觅食风格之间的关系，以及使用蛛网作为捕食工具与身体特征变化的相关性，至今仍不明确。在此，我们呈现了迄今为止最全面的蜘蛛形态学特性和生态学特性数据集。利用该数据集，我们估算了蜘蛛身体大小和形状在漫长地质年代中的变化，并检验了蜘蛛表型与它们行为生态学之间的相关性。我们发现，大多数性状的谱系变异最适合奥恩斯坦-乌尔班克模型，这是一个稳定选择的模型。一个显著的例外是身体长度，其进化动态最好用布朗运动（自由性状扩散）模型来解释。这一现象在蛛形纲（无丝蛛类和其盟友）中最为明显，该类群表现出向微型化或巨大型发展的双峰趋势。只有少数性状在生态群中存在显著差异，最突出的是腿长和腿粗，尽管多元框架发现生态群之间的性状存在普遍差异，但无法明确地将一组形态学性状与相对生态模式联系起来。长而细的腿通常与空中蛛网和悬挂（悬挂）的移动风格相伴而生，但这种趋势并非普遍现象。眼大小和螫针长度在生态群之间没有差异，这一发现反驳了蛛网减少了视觉线索识别和猎物固定需求的假设。对于推断具有未知行为的物种的生态学，我们建议不要使用形态学性状，而应咨询（微观）形态学特征，例如某些足部结构的存在。这些结果表明，与昆虫相比，蜘蛛身体比例的进化异常稳定，生态适应主要通过行为特性和扩展表型在这一类捕食者群体中实现。这项工作展示了将谱系基因组学的最新进展与基于性状的方法相结合，以更好地理解空间和时间上的全球功能多样性模式的力量。