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Evolutionary transformation of mouthparts from particle-feeding to piercing carnivory in Viper copepods: Review and 3D analyses of a key innovation using advanced imaging techniques
Frontiers in Zoology ( IF 2.6 ) Pub Date : 2019-08-22 , DOI: 10.1186/s12983-019-0308-y
Tomonari Kaji 1, 2 , Chihong Song 3 , Kazuyoshi Murata 3 , Shigenori Nonaka 4 , Kota Ogawa 5 , Yusuke Kondo 6 , Susumu Ohtsuka 6 , A Richard Palmer 1
Affiliation  

Novel feeding adaptations often facilitate adaptive radiation and diversification. But the evolutionary origins of such feeding adaptations can be puzzling if they require concordant change in multiple component parts. Pelagic, heterorhabdid copepods (Calanoida) exhibit diverse feeding behaviors that range from simple particle feeding to a highly specialized form of carnivory involving piercing mouthparts that likely inject venom. We review the evolutionary history of heterorhabdid copepods and add new high-resolution, 3D anatomical analyses of the muscular system, glands and gland openings associated with this remarkable evolutionary transformation. We examined four heterorhabdid copepods with different feeding modes: one primitive particle-feeder (Disseta palumbii), one derived and specialized carnivore (Heterorhabdus subspinifrons), and two intermediate taxa (Mesorhabdus gracilis and Heterostylites longicornis). We used two advanced, high-resolution microscopic techniques — serial block-face scanning electron microscopy and two-photon excitation microscopy — to visualize mouthpart form and internal anatomy at unprecedented nanometer resolution. Interactive 3D graphical visualizations allowed putative homologues of muscles and gland cells to be identified with confidence and traced across the evolutionary transformation from particle feeding to piercing carnivory. Notable changes included: a) addition of new gland cells, b) enlargement of some (venom producing?) glands, c) repositioning of gland openings associated with hollow piercing fangs on the mandibles, d) repurposing of some mandibular-muscle function to include gland-squeezing, and e) addition of new muscles that may aid venom injection exclusively in the most specialized piercing species. In addition, live video recording of all four species revealed mandibular blade movements coupled to cyclic contraction of some muscles connected to the esophagus. These behavioral and 3D morphological observations revealed a novel injection system in H. subspinifrons associated with piercing (envenomating?) carnivory. Collectively, these results suggest that subtle changes in mandibular tooth form, and muscle and gland form and location, facilitated the evolution of a novel, piercing mode of feeding that accelerated diversification of the genus Heterorhabdus. They also highlight the value of interactive 3D animations for understanding evolutionary transformations of complex, multicomponent morphological systems.

中文翻译:


蝰蛇桡足类口器从颗粒进食到刺穿肉食的进化转变:使用先进成像技术对一项关键创新进行回顾和 3D 分析



新颖的喂养适应通常有助于适应性辐射和多样化。但如果这种进食适应需要多个组成部分的一致变化,那么它们的进化起源可能会令人费解。远洋异杆菌桡足类动物(Calanoida)表现出多种摄食行为,从简单的颗粒摄食到高度专业化的食肉动物,包括可能注入毒液的刺穿口器。我们回顾了异杆菌桡足类动物的进化史,并对与这一显着进化转变相关的肌肉系统、腺体和腺体开口进行了新的高分辨率 3D 解剖分析。我们研究了四种具有不同进食模式的异杆菌桡足类动物:一种原始的颗粒进食动物(Disseta palumbii),一种衍生的专门食肉动物(Heterorhabdus subspinifrons),以及两种中间类群(Mesorhabdus gracilis 和 Heterostylites longicornis)。我们使用了两种先进的高分辨率显微技术——串行块面扫描电子显微镜和双光子激发显微镜——以前所未有的纳米分辨率可视化口器形状和内部解剖结构。交互式 3D 图形可视化允许自信地识别肌肉和腺细胞的假定同源物,并追踪从颗粒进食到刺穿肉食的进化转变。显着的变化包括:a)添加新的腺细胞,b)一些(产生毒液?)腺体的扩大,c)重新定位与下颌骨上空心尖牙相关的腺体开口,d)重新调整一些下颌肌肉功能以包括挤压腺体,以及 e) 添加新的肌肉,这可能有助于专门针对最特殊的刺穿物种进行毒液注射。 此外,所有四个物种的现场视频记录显示下颌刀片运动与与食道相连的一些肌肉的周期性收缩相结合。这些行为和 3D 形态学观察揭示了 H. subspinifrons 中与刺穿(毒液?)食肉动物相关的新型注射系统。总的来说,这些结果表明,下颌牙齿形状、肌肉和腺体形状和位置的微妙变化促进了一种新颖的、刺穿性进食模式的进化,从而加速了异杆菌属的多样化。他们还强调了交互式 3D 动画对于理解复杂、多组分形态系统的进化转变的价值。
更新日期:2020-04-22
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