No abstract
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.
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