Neuroanatomy of Halobiotus crispae (Eutardigrada: Hypsibiidae): Tardigrade brain structure supports the clade panarthropoda

Abstract

The position of Tardigrada in the animal tree of life is a subject that has received much attention, but still remains controversial. Whereas some think tardigrades should be categorized as cycloneuralians, most authors argue in favor of a phylogenetic position within Panarthropoda as a sister group to Arthropoda or Arthropoda + Onychophora. Thus far, neither molecular nor morphological investigations have provided conclusive results as to the tardigrade sister group relationships. In this article, we present a detailed description of the nervous system of the eutardigrade Halobiotus crispae, using immunostainings, confocal laser scanning microscopy, and computer-aided three-dimensional reconstructions supported by transmission electron microscopy. We report details regarding the structure of the brain as well as the ganglia of the ventral nerve cord. In contrast to the newest investigation, we find transverse commissures in the ventral ganglia, and our data suggest that the brain is partitioned into at least three lobes. Additionally, we can confirm the existence of a subpharyngeal ganglion previously called subesophagal ganglion. According to our results, the original suggestion of a brain comprised of at least three parts cannot be rejected, and the data presented supports a sister group relationship of Tardigrada to 1) Arthropoda or 2) Onychophora or 3) Arthropoda + Onychophora.

Selective neuronal staining in tardigrades and onychophorans provides insights into the evolution of segmental ganglia in panarthropods

“…However, our immunocytochemical and electron microscopic data clearly show contralateral fibres and bundles of neurites in all four trunk ganglia in specimens of Macrobiotus cf. harmsworthi , Paramacrobiotus richtersi and Hypsibius dujardini , thus confirming previous findings from other tardigrade species, including Macrobiotus hufelandi [22,23,25,34]. Therefore, contrary to this previous assumption [33], the occurrence of contralateral fibres and commissures in the ventral nervous system does not support the proposed sister group relationship of Onychophora and Arthropoda, as these structures also occur in the tardigrade ganglia and, therefore, were most likely present in the last common ancestor of Panarthropoda.…”

“…Moreover, our data revealed an anteriorly shifted position of trunk ganglia with respect to each leg pair in the three tardigrade species studied, which is also seen in the illustrations of other tardigrade species [22,23,25,29-32,36,37]. Notably, a corresponding anterior shift in position of ganglia occurs in representatives of all major arthropod groups [38], which might be due to the embryonic origin of ganglia.…”

Neuronal tracing of oral nerves in a velvet worm—Implications for the evolution of the ecdysozoan brain

“…Among the three panarthropod clades (Figure 1), tardigrades also show a typical dorsal brain, although there is some controversy regarding the number of segmental regions involved (Persson et al, 2012, 2013; Mayer et al, 2013a,b; Schulze et al, 2013). Hence, the last common ancestor of Panarthropoda most likely possessed a bilaterally symmetric, dorsal, ganglionic brain rather than a circumoral/circumpharyngeal, collar-shaped brain, which is a characteristic feature of cycloneuralians, including priapulids, loriciferans, kinorhynchs, nematodes and nematomorphs (Bullock and Horridge, 1965; Nielsen, 2012).…”

Neural Markers Reveal a One-Segmented Head in Tardigrades (Water Bears)

“…The typical arthropod head is a composite structure consisting of several segments, which might have been added successively in the course of arthropod evolution [3]–[5]. The homology of the cephalic segments has been clarified recently in arthropods and onychophorans [6], [7], but the contradictory data from tardigrades [8]–[10] currently do not allow an adequate comparison with these two animal groups.…”