The prothoracic repellent glands of stick and leaf insects: Reconstructing the morphological and chemical evolution of an elaborate arthropod defensive system

为了避免捕食，动物一直处于强势选择之下，因此捕食者-猎物之间的相互作用是进化的主要驱动力，并产生了大量有效的防御策略。颜色可以说是主要防御中最明显的，可能会增强密码，以减少检测或警告捕食者猎物的不适性或毒性。这两种策略都可以在枝叶昆虫(Phasmatodea)中找到，这是一种大型陆地食草性节肢动物的中间多样性谱系，以其非凡的伪装能力而闻名。大多数物种是夜间活动的，白天保持不动，通过模仿树枝、树叶和树皮来伪装神秘。相比之下，少数物种表现出惊人的无融合现象(警示颜色)，暗示它们使用了有效的前胸腺。从这些腺体喷洒化学物质只是食肉动物众多次级防御机制中的一种(即捕食者攻击时启动的机制)，包括惊吓显示、防御性突击、死亡或逃脱、肢体自切或通过重型Armend腿进行反击。虽然大多数物种在很大程度上依靠隐蔽的外表来躲避捕食者的发现，但它们的二级防御系统相当复杂，原胸腺中的厌恶腺体被认为在现存物种中广泛存在，实际上构成了所有节肢动物的衍生地面模式特征(自形)。在所描述的3.000多个分类群中，这种强大的防御机制所涉及的化学物质只有12个物种已知，到目前为止还没有关于一些主要和关键谱系的信息。本项目的目标是(I)为前胸腺的存在和解剖多样性建立一个丰富的信息库，包括100种棒虫和叶昆虫的广泛和有代表性的分类样本，(Ii)确定所涉及的化学物质，以及(Iii)在系统发育框架内重建这一复杂防御系统的逐步解剖和化学进化。所获得的信息将与被检查物种的身体形状和大小、骨架、颜色和行为观察的现有数据相结合，以揭示关键特征的相关性和变化，并发现可能对多样化速度产生影响并塑造棍虫和叶虫进化的关键创新。由于迄今报道的为数不多的几种驱避物质在不同类群之间表现出出人意料的巨大多样性，表现出高度特异性的特征，如气味或引起皮肤刺激(如人类感知的)，并包括一些以前未报道的天然产物，我们也希望我们的项目能够证明棍虫和叶虫作为新的生物活性化合物来源的价值。

Animals are permanently under strong selection to avoid predation, therefore predator-prey interactions are major driving forces of evolution and have given rise to a plethora of effective defensive strategies. Colouration is arguably the most obvious among primary defenses and might enhance crypsis to reduce detection or warn predators of the prey’s unpalatability or toxicity. Both strategies can be found in stick and leaf insects (Phasmatodea), a mesodiverse lineage of large terrestrial herbivorous arthropods well known for their remarkable capability to camouflage themselves as plant parts. Most species are nocturnal, remain motionless during the day and exhibit masquerade crypsis by mimicking twigs, leaves and bark. In contrast, a minority of species displays striking forms of aposematism (warning colouration) insinuating the use of their efficient prothoracic repellent glands. Chemical spraying from these glands is just one of numerous secondary defensive mechanisms in phasmatodeans (i.e., those initiated when a predator attacks), comprising startle display, defensive stridulation, thanatosis or escape by flight, limb autotomy or counterattack via heavily armend legs. Although most species largely rely on cryptic appearance to avoid predator detection, their secondary defensive system is quite elaborate, and repugnatorial glands in the prothorax are supposed to be widely present among extant species, in fact constituting a derived ground pattern feature (autapomorphy) of all Phasmatodea.The chemical substances involved in this powerful defensive mechanism are known only for a dozen species out of the more than 3.000 described taxa, so far with no information available for some major and pivotal lineages. The goal of the present project is (i) to generate a profound information base for the presence and anatomical diversity of the prothoracic repellent glands across a broad and representative taxon sampling of 100 stick and leaf insect species, (ii) to identify the chemical substances involved, and (iii) to reconstruct the step-wise anatomical and chemical evolution of this elaborate defensive system in a phylogenetic framework. The obtained information will be combined with existing data on body form and size, armature, colouration and behavioural observations of the examined species in order to reveal correlations and transformations of crucial traits and to detect key innovations that might have had an effect on diversification rates and shaped the evolution of stick and leaf insects. Since the few hitherto reported repellent substances show an unexpectedly huge diversity between taxa, exhibiting highly specific characteristics such as odor or causing skin irritations (as perceived by humans), and include some previously unreported natural products, we also expect our project to demonstrate the value of stick and leaf insects as sources of new bioactive compounds.