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BackgroundThe tardigrades (water bears) are a cosmopolitan group of microscopic ecdysozoans found in a variety of aquatic and temporarily wet environments. They are members of the Panarthropoda (Tardigrada + Onychophora + Arthropoda), although their exact position within this group remains contested. Studies of embryonic development in tardigrades have been scarce and have yielded contradictory data. Therefore, we investigated the development of the nervous system in embryos of the tardigrade Hypsibius dujardini using immunohistochemical techniques in conjunction with confocal laser scanning microscopy in an effort to gain insight into the evolution of the nervous system in panarthropods.ResultsAn antiserum against acetylated α-tubulin was used to visualize the axonal processes and general neuroanatomy in whole-mount embryos of the eutardigrade H. dujardini. Our data reveal that the tardigrade nervous system develops in an anterior-to-posterior gradient, beginning with the neural structures of the head. The brain develops as a dorsal, bilaterally symmetric structure and contains a single developing central neuropil. The stomodeal nervous system develops separately and includes at least four separate, ring-like commissures. A circumbuccal nerve ring arises late in development and innervates the circumoral sensory field. The segmental trunk ganglia likewise arise from anterior to posterior and establish links with each other via individual pioneering axons. Each hemiganglion is associated with a number of peripheral nerves, including a pair of leg nerves and a branched, dorsolateral nerve.ConclusionsThe revealed pattern of brain development supports a single-segmented brain in tardigrades and challenges previous assignments of homology between tardigrade brain lobes and arthropod brain segments. Likewise, the tardigrade circumbuccal nerve ring cannot be homologized with the arthropod ‘circumoral’ nerve ring, suggesting that this structure is unique to tardigrades. Finally, we propose that the segmental ganglia of tardigrades and arthropods are homologous and, based on these data, favor a hypothesis that supports tardigrades as the sister group of arthropods.Electronic supplementary materialThe online version of this article (doi:10.1186/s13227-015-0008-4) contains supplementary material, which is available to authorized users.
The anomalous occurrence of supposedly Gondwanan taxa in Laurasian-derived regions remains an intriguing chapter of paleobiogeographical history. Representatives of Peripatidae, a major subgroup of velvet worms (Onychophora), show a disjointed distribution in the neotropics, tropical Africa, and Southeast Asia, the latter being the only landmass previously associated with Laurasia [1, 2]. The arrival of these animals in Southeast Asia is explained by two alternative, albeit not mutually exclusive, hypotheses: an early migration via Europe before continental drift (Eurogondwana hypothesis) or transportation via insular India during the Cretaceous and Paleogene ("out-of-India" hypothesis) [3-6]. The latter hypothesis is based on a single extant species of Peripatidae, Typhloperipatus williamsoni, in India. †Cretoperipatus burmiticus from Myanmar is the oldest fossil onychophoran found in amber [7], dating to sometime between the two proposed scenarios, and hence crucial for clarifying how Gondwanan lineages of these low-vagility animals reached Southeast Asia (see also Supplemental Information). Based on the anatomical reconstruction of †C. burmiticus using synchrotron radiation-based X-ray microtomography (SRμCT) and comparisons with extant taxa, we resolved this fossil species within Onychophora, particularly within Peripatidae, with T. williamsoni as its closest extant relative. This suggests that an early Eurogondwanan migration of peripatids was the most likely event, as Burmese amber is too old to be compatible with the out-of-India hypothesis. Moreover, peripatids probably colonized India only recently from Myanmar, refuting the putative Gondwanan relict status of Indian onychophorans. Finally, preservation artifacts identified in the novel amber material might have a major impact on studies of onychophoran stem and/or crown groups.
Understanding the origin and evolution of arthropods requires examining their closest outgroups, the tardigrades (water bears) and onychophorans (velvet worms). Despite the rise of molecular techniques, the phylogenetic positions of tardigrades and onychophorans in the panarthropod tree (onychophorans + tardigrades + arthropods) remain unresolved. Hence, these methods alone are currently insufficient for clarifying the panarthropod topology. Therefore, the evolution of different morphological traits, such as one of the most intriguing features of panarthropods-their nervous system-becomes essential for shedding light on the origin and evolution of arthropods and their relatives within the Panarthropoda. In this review, we summarise current knowledge of the evolution of panarthropod nervous and visual systems. In particular, we focus on the evolution of segmental ganglia, the segmental identity of brain regions, and the visual system from morphological and developmental perspectives. In so doing, we address some of the many controversies surrounding these topics, such as the homology of the onychophoran eyes to those of arthropods as well as the segmentation of the tardigrade brain. Finally, we attempt to reconstruct the most likely state of these systems in the last common ancestors of arthropods and panarthropods based on what is currently known about tardigrades and onychophorans.
BackgroundDue to their phylogenetic position as one of the closest arthropod relatives, studies of the organisation of the nervous system in onychophorans play a key role for understanding the evolution of body segmentation in arthropods. Previous studies revealed that, in contrast to the arthropods, segmentally repeated ganglia are not present within the onychophoran ventral nerve cords, suggesting that segmentation is either reduced or might be incomplete in the onychophoran ventral nervous system.ResultsTo assess segmental versus non-segmental features in the ventral nervous system of onychophorans, we screened the nerve cords for various markers, including synapsin, serotonin, gamma-aminobutyric acid, RFamide, dopamine, tyramine and octopamine. In addition, we performed retrograde fills of serially repeated commissures and leg nerves to localise the position of neuronal somata supplying those. Our data revealed a mixture of segmental and non-segmental elements within the onychophoran nervous system.ConclusionsWe suggest that the segmental ganglia of arthropods evolved by a gradual condensation of subsets of neurons either in the arthropod or the arthropod-tardigrade lineage. These findings are in line with the hypothesis of gradual evolution of segmentation in panarthropods and thus contradict a loss of ancestral segmentation within the onychophoran lineage.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-016-0853-3) contains supplementary material, which is available to authorized users.
Background Tardigrades (water bears) are microscopic invertebrates of which the anatomy has been well studied using traditional techniques, but a comprehensive three-dimensional reconstruction has never been performed. In order to close this gap, we employed X-ray computed tomography (CT), a technique that is becoming increasingly popular in zoology for producing high-resolution, three-dimensional (3D) scans of whole specimens. While CT has long been used to scan larger samples, its use in some microscopic animals can be problematic, as they are often too small for conventional CT yet too large for high-resolution, optics-based soft X-ray microscopy. This size gap continues to be narrowed with advancements in technology, with high-resolution imaging now being possible using both large synchrotron devices and, more recently, laboratory-based instruments. Results Here we use a recently developed prototype lab-based nano-computed tomography device to image a 152 μm-long tardigrade at high resolution (200–270 nm pixel size). The resulting dataset allowed us to visualize the anatomy of the tardigrade in 3D and analyze the spatial relationships of the internal structures. Segmentation of the major structures of the body enabled the direct measurement of their respective volumes. Furthermore, we segmented every storage cell individually and quantified their volume distribution. We compare our measurements to those from published studies in which other techniques were used. Conclusions The data presented herein demonstrate the utility of CT imaging as a powerful supplementary tool for studies of tardigrade anatomy, especially for quantitative volume measurements. This nanoCT study represents the smallest complete animal ever imaged using CT, and offers new 3D insights into the spatial relationships of the internal organs of water bears. Electronic supplementary material The online version of this article (10.1186/s40851-019-0130-6) contains supplementary material, which is available to authorized users.
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