Kaji Tomonari, Song Chihong, Murata Kazuyoshi, Nonaka Shigenori, Ogawa Kota, Kondo Yusuke, Ohtsuka Susumu, Palmer A Richard
1Department of Biological Sciences, University of Alberta, Edmonton, AB T6G 2E9 Canada.
2Allgemeine & Spezielle Zoologie, Institut fur Biowissenschaften, Universität Rostock, 18055 Rostock, Germany.
Front Zool. 2019 Aug 22;16:35. doi: 10.1186/s12983-019-0308-y. eCollection 2019.
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 (), one derived and specialized carnivore (), and two intermediate taxa ( and ). 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 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 . They also highlight the value of interactive 3D animations for understanding evolutionary transformations of complex, multicomponent morphological systems.
新的摄食适应性通常会促进适应性辐射和多样化。但是，如果这些摄食适应性需要多个组成部分协调变化，那么其进化起源可能会令人困惑。海洋异足桡足类（哲水蚤目）表现出多样的摄食行为，从简单的颗粒摄食到涉及穿刺口器（可能注射毒液）的高度特化的肉食性形式。我们回顾了异足桡足类的进化历史，并对与这一显著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三维解剖分析。
我们研究了四种具有不同摄食模式的异足桡足类：一种原始的颗粒摄食者（），一种衍生的特化肉食者（），以及两个中间分类群（和）。我们使用了两种先进的高分辨率显微镜技术——连续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观察口器形态和内部解剖结构。交互式三维图形可视化使我们能够自信地识别肌肉和腺细胞的假定同源物，并追踪从颗粒摄食到穿刺肉食性的进化转变。显著变化包括：a）新腺细胞的增加，b）一些（产毒液的？）腺体的扩大，c）与下颌空心穿刺齿相关的腺体开口的重新定位，d）一些下颌肌肉功能的重新利用，包括挤压腺体，以及e）仅在最特化的穿刺物种中添加可能有助于毒液注射的新肌肉。此外，对所有四个物种的实时视频记录显示，下颌刀片的运动与连接到食道的一些肌肉的周期性收缩有关。这些行为和三维形态学观察揭示了与穿刺（注入毒液？）肉食性相关的一种新的注射系统。
总体而言，这些结果表明，下颌齿形态、肌肉和腺体形态及位置的细微变化促进了一种新的穿刺摄食模式的进化，加速了该属的多样化。它们还强调了交互式三维动画对于理解复杂的多组分形态系统进化转变的价值。
