Publications by authors named "Vladimir Gross"

13 Publications

  • Page 1 of 1

Organization of the central nervous system and innervation of cephalic sensory structures in the water bear Echiniscus testudo (Tardigrada: Heterotardigrada) revisited.

J Morphol 2021 Jun 15. Epub 2021 Jun 15.

Department of Zoology, Institute of Biology, University of Kassel, Kassel, Germany.

The tardigrade brain has been the topic of several neuroanatomical studies, as it is key to understanding the evolution of the central nervous systems in Panarthropoda (Tardigrada + Onychophora + Arthropoda). The gross morphology of the brain seems to be well conserved across tardigrades despite often disparate morphologies of their heads and cephalic sensory structures. As such, the general shape of the brain and its major connections to the rest of the central nervous system have been mapped out already by early tardigradologists. Despite subsequent investigations primarily based on transmission electron microscopy or immunohistochemistry, characterization of the different regions of the tardigrade brain has progressed relatively slowly and open questions remain. In an attempt to improve our understanding of different brain regions, we reinvestigated the central nervous system of the heterotardigrade Echiniscus testudo using anti-synapsin and anti-acetylated α-tubulin immunohistochemistry in order to visualize the number and position of tracts, commissures, and neuropils. Our data revealed five major synapsin-immunoreactive domains along the body: a large unitary, horseshoe-shaped neuropil in the head and four neuropils in the trunk ganglia, supporting the hypothesis that the dorsal brain is serially homologous with the ventral trunk ganglia. At the same time, the pattern of anti-synapsin and anti-tubulin immunoreactivity differs between the ganglia, adding to the existing evidence that each of the four trunk ganglia is unique in its morphology. Anti-tubulin labeling further revealed two commissures within the central brain neuropil, one of which is forked, and additional sets of extracerebral cephalic commissures associated with the stomodeal nervous system and the ventral cell cluster. Furthermore, our results showing the innervation of each of the cephalic sensilla in E. testudo support the homology of subsets of these structures with the sensory fields of eutardigrades.
View Article and Find Full Text PDF

Download full-text PDF

Source
http://dx.doi.org/10.1002/jmor.21386DOI Listing
June 2021

Cellular morphology of leg musculature in the water bear (Tardigrada) unravels serial homologies.

R Soc Open Sci 2019 Oct 16;6(10):191159. Epub 2019 Oct 16.

Department of Zoology, Institute of Biology, University of Kassel, Heinrich-Plett-Straße 40, 34132 Kassel, Germany.

Tardigrades (water bears) are microscopic, segmented ecdysozoans with four pairs of legs. Lobopodous limbs that are similar to those seen in tardigrades are hypothesized to represent the ancestral state of Panarthropoda (Tardigrada + Onychophora + Arthropoda), and their evolutionary history is important to our understanding of ecdysozoan evolution. Equally important is our understanding of the functional morphology of these legs, which requires knowledge of their musculature. Tardigrade musculature is well documented but open questions remain. For example, while the muscular organization of each trunk segment and its legs is unique, three of the four trunk segments are nevertheless relatively homonomous. To what extent, then, do leg muscles show segmental patterns? Specifically, which leg muscles are serially repeated and which are unique? The present study addresses these questions using a combination of techniques intended to visualize both the overall layout and fine structure of leg muscles in the eutardigrade . In doing so, we propose serial homologies for all leg muscles in each of the four legs and reveal new details of their cellular structure and attachment sites. We compare our results to those of previous studies and address the functional implications of specialized muscle cell morphologies.
View Article and Find Full Text PDF

Download full-text PDF

Source
http://dx.doi.org/10.1098/rsos.191159DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6837179PMC
October 2019

X-ray imaging of a water bear offers a new look at tardigrade internal anatomy.

Zoological Lett 2019 11;5:14. Epub 2019 May 11.

2Department of Physics and Munich School of BioEngineering, Technical University of Munich, 85748 Garching, Germany.

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.
View Article and Find Full Text PDF

Download full-text PDF

Source
http://dx.doi.org/10.1186/s40851-019-0130-6DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6511223PMC
May 2019

Miniaturization of tardigrades (water bears): Morphological and genomic perspectives.

Arthropod Struct Dev 2019 Jan 3;48:12-19. Epub 2018 Dec 3.

Department of Zoology, Institute of Biology, University of Kassel, Heinrich-Plett-Straße 40, Kassel, D-34132, Germany. Electronic address:

Tardigrades form a monophyletic group of microscopic ecdysozoans best known for surviving extreme environmental conditions. Due to their key phylogenetic position as a subgroup of the Panarthropoda, understanding tardigrade biology is important for comparative studies with related groups like Arthropoda. Panarthropods - and Ecdysozoa as a whole - likely evolved from macroscopic ancestors, with several taxa becoming secondarily miniaturized. Morphological and genomic evidence likewise points to a miniaturized tardigrade ancestor. The five-segmented tardigrade body typically measures less than 1 mm in length and consists of only about 1000 cells. Most organs comprise a relatively small number of cells, with the highest proportion belonging to the central nervous system, while muscles are reduced to a single cell each. Similarly, fully sequenced genomes of three tardigrade species - together with Hox gene expression data - point to extensive modifications, rearrangements, and major losses of genes and even a large body region. Parallels are evident with related ecdysozoans that may have also undergone genomic reductions, such as the nematode Caenorhabditis elegans. We interpret these data together as evidence of miniaturization in the tardigrade lineage, while cautioning that the effects of miniaturization may manifest in different ways depending on the organ or organ system under examination.
View Article and Find Full Text PDF

Download full-text PDF

Source
http://dx.doi.org/10.1016/j.asd.2018.11.006DOI Listing
January 2019

Evaluation of contrasting techniques for X-ray imaging of velvet worms (Onychophora).

J Microsc 2018 06 22;270(3):343-358. Epub 2018 Feb 22.

Institute of Materials Research, Helmholtz-Zentrum Geesthacht, Geesthacht, Germany.

Non-invasive imaging techniques like X-ray computed tomography have become very popular in zoology, as they allow for simultaneous imaging of the internal and external morphology of organisms. Nevertheless, the effect of different staining approaches required for this method on samples lacking mineralized tissues, such as soft-bodied invertebrates, remains understudied. Herein, we used synchrotron radiation-based X-ray micro-computed tomography to compare the effects of commonly used contrasting approaches on onychophorans - soft-bodied invertebrates important for studying animal evolution. Representatives of Euperipatoides rowelli were stained with osmium tetroxide (vapour or solution), ruthenium red, phosphotungstic acid, or iodine. Unstained specimens were imaged using both standard attenuation-based and differential phase-contrast setups to simulate analyses with museum material. Our comparative qualitative analyses of several tissue types demonstrate that osmium tetroxide provides the best overall tissue contrast in onychophorans, whereas the remaining staining agents rather favour the visualisation of specific tissues and/or structures. Quantitative analyses using signal-to-noise ratio measurements show that the level of image noise may vary according to the staining agent and scanning medium selected. Furthermore, box-and-whisker plots revealed substantial overlap in grey values among structures in all datasets, suggesting that a combination of semiautomatic and manual segmentation of structures is required for comprehensive 3D reconstructions of Onychophora, irrespective of the approach selected. Our results show that X-ray micro-computed tomography is a promising technique for studying onychophorans and, despite the benefits and disadvantages of different staining agents for specific tissues/structures, this method retrieves informative data that may eventually help address evolutionary questions long associated with Onychophora.
View Article and Find Full Text PDF

Download full-text PDF

Source
http://dx.doi.org/10.1111/jmi.12688DOI Listing
June 2018

The nervous and visual systems of onychophorans and tardigrades: learning about arthropod evolution from their closest relatives.

J Comp Physiol A Neuroethol Sens Neural Behav Physiol 2017 Aug 9;203(8):565-590. Epub 2017 Jun 9.

Department of Zoology, University of Kassel, Heinrich-Plett-Str. 40, 34132, Kassel, Germany.

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.
View Article and Find Full Text PDF

Download full-text PDF

Source
http://dx.doi.org/10.1007/s00359-017-1186-4DOI Listing
August 2017

External morphogenesis of the tardigrade Hypsibius dujardini as revealed by scanning electron microscopy.

J Morphol 2017 04 6;278(4):563-573. Epub 2017 Feb 6.

Department of Zoology, Institute of Biology, University of Kassel, Heinrich-Plett-Straße 40, D-34132, Kassel, Germany.

Tardigrada, commonly called water bears, is a taxon of microscopic panarthropods with five-segmented bodies and four pairs of walking legs. Although tardigrades have been known to science for several centuries, questions remain regarding many aspects of their biology, such as embryogenesis. Herein, we used scanning electron microscopy to document the external changes that occur during embryonic development in the tardigrade Hypsibius dujardini (Eutardigrada, Parachela, Hypsibiidae). Our results show an accelerated development of external features, with approximately 30 hrs separating the point at which external structures first become recognizable and a fully formed embryo. All segments appear to arise simultaneously between ∼20 and 25 hrs of development, and no differences in the degree of development could be detected between the limb buds at any stage. Claws emerge shortly after the limb buds and are morphologically similar to those of adults. The origin of the claws is concurrent with that of the sclerotized parts of the mouth, suggesting that all cuticular structures arise simultaneously at ∼30 hrs. The mouth arises as an invagination in the terminal region of the head at ∼25 hrs, closes later in development, and opens again shortly before hatching. The anlagen of the peribuccal lobes arise as one dorsal and one ventral row, each consisting of three lobes, and later form a ring in the late embryo, whereas there is no indication of a labrum anlage at any point during development. Furthermore, we describe limited postembryonic development in the form of cuticular pores that are absent in juveniles but present in adults. This study represents the first scanning electron micrographs of tardigrade embryos, demonstrating the utility of this technique for studying embryogenesis in tardigrades. This work further adds an external morphological perspective to the developmental data already available for H. dujardini, facilitating future comparisons to related panarthropod taxa. J. Morphol. 278:563-573, 2017. © 2017 Wiley Periodicals, Inc.
View Article and Find Full Text PDF

Download full-text PDF

Source
http://dx.doi.org/10.1002/jmor.20654DOI Listing
April 2017

Assessing segmental versus non-segmental features in the ventral nervous system of onychophorans (velvet worms).

BMC Evol Biol 2017 01 3;17(1). Epub 2017 Jan 3.

Department of Zoology, University of Kassel, Heinrich-Plett-Str. 40, D-34132, Kassel, Germany.

Background: Due 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.

Results: To 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.

Conclusions: We 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.
View Article and Find Full Text PDF

Download full-text PDF

Source
http://dx.doi.org/10.1186/s12862-016-0853-3DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5209844PMC
January 2017

Earliest Onychophoran in Amber Reveals Gondwanan Migration Patterns.

Curr Biol 2016 10 29;26(19):2594-2601. Epub 2016 Sep 29.

Department of Zoology, Institute of Biology, University of Kassel, Heinrich-Plett-Straße 40, 34132 Kassel, Germany.

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.
View Article and Find Full Text PDF

Download full-text PDF

Source
http://dx.doi.org/10.1016/j.cub.2016.07.023DOI Listing
October 2016

Neural development in the tardigrade Hypsibius dujardini based on anti-acetylated α-tubulin immunolabeling.

Evodevo 2015 25;6:12. Epub 2015 Apr 25.

Department of Zoology, Institute of Biology, University of Kassel, Heinrich-Plett-Str. 40, D-34132 Kassel, Germany.

Background: The 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.

Results: An 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.

Conclusions: The 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.
View Article and Find Full Text PDF

Download full-text PDF

Source
http://dx.doi.org/10.1186/s13227-015-0008-4DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4458024PMC
June 2015

Latest anomalocaridid affinities challenged.

Nature 2014 Dec;516(7530):E1-2

Animal Evolution and Development, University of Leipzig, Talstraße 33, 04103 Leipzig, Germany.

View Article and Find Full Text PDF

Download full-text PDF

Source
http://dx.doi.org/10.1038/nature13860DOI Listing
December 2014

A new tardigrade, Mutaparadoxipus duodigifinis gen. nov., sp. nov. (Heterotardigrada: Arthrotardigrada), from the Southeastern United States.

Zootaxa 2014 Jul 10;3835(2):263-72. Epub 2014 Jul 10.

Department of Biological Sciences, University of Massachusetts Lowell, One University Avenue, Lowell, MA 01854, USA.; Email:

A new genus and species of Arthrotardigrada is described from Florida, USA based on its unique adhesive pad/claw combinations. Mutaparadoxipus duodigifinis gen. nov., sp. nov., is characterized by well-developed, ventral secondary clavae that are adjacent to the mouth, pointed lateral and caudal alae, seminal receptacles with coiled ducts opening lateral to the gonopore, and all legs with digits bearing proximal adhesive pads. Distal claws are present on digits I-III of legs I-III, but are missing from digit IV. On leg IV, distal claws are present only on digits II & III. A single accessory point is present on claws II & III only. This is the fourth species discovered to date with proximal adhesive pads, increasing support for a clade of adhesive-padded arthrotardigrades, and is likely the sister taxon of Paradoxipus orzeliscoides. The incomplete set of claws may represent an evolutionary step in a progressive loss of claws hypothesized to have occurred within the Halechiniscidae. The subfamily Orzeliscinae is amended as a result.
View Article and Find Full Text PDF

Download full-text PDF

Source
http://dx.doi.org/10.11646/zootaxa.3835.2.6DOI Listing
July 2014

A new species of sublittoral marine gastrotrich, Lepidodasys ligni sp. n. (Macrodasyida, Lepidodasyidae), from the Atlantic coast of Florida.

Zookeys 2013 12(289):1-12. Epub 2013 Apr 12.

University of Massachusetts Lowell, One University Avenue, Lowell, MA 01854 USA, 01.978.934.2885.

A new species of Lepidodasys is described from sublittoral sandy sediments off the Atlantic coast of Florida. Lepidodasys ligni sp. n. is a small species (≤ 450 µm) with a crossed-helical pattern of small, non-keeled, non-imbricated scales on the dorsal and lateral body surfaces, two columns of ventral, interciliary scales that form a herringbone pattern, and a series of anterior, lateral, dorsal and posterior adhesive tubes. Similar to Lepidodasys castoroides from the Faroe Islands, the new species possesses a caudal constriction that demarcates the posterior end containing the caudal organ. The frontal organ lies within the posterior constriction, which is heavily invested with somatic circular muscles. These muscles are also present throughout the trunk and represent a novel condition for species of Lepidodasys,which were previously considered to lack somatic circular muscles. Posterior of the caudal constriction is a large, barrel-shaped caudal organ that is wrapped in a series of interdigitating, spindle-shaped, incomplete circular muscle fibers. The caudal organ contains a sclerotized central canal, but the absence of distal cuticular endpieces distinguishes the new species from its morphologically similar congener, Lepidodasys castoroides.
View Article and Find Full Text PDF

Download full-text PDF

Source
http://dx.doi.org/10.3897/zookeys.289.4764DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3677386PMC
June 2013