Brain anatomy of the marine tardigrade actinarctus doryphorus (arthrotardigrada)

Abstract

Knowledge of tardigrade brain structure is important for resolving the phylogenetic relationships of Tardigrada. Here, we present new insight into the morphology of the brain in a marine arthrotardigrade, Actinarctus doryphorus, based on transmission electron microscopy, supported by scanning electron microscopy, conventional light microscopy as well as confocal laser scanning microscopy. Arthrotardigrades contain a large number of plesiomorphic characters and likely represent ancestral tardigrades. They often have segmented body outlines and each trunk segment, with its paired set of legs, may have up to five sensory appendages. Noticeably, the head carries numerous cephalic appendages that are structurally equivalent to the sensory appendages of the trunk segments. Our data reveal that the brain of A. doryphorus is partitioned into three paired lobes, and that these lobes exhibit a more pronounced separation as compared to that of eutardigrades. The first brain lobe in A. doryphorus is located anteriodorsally, with the second lobe just below it in an anterioventral position. Both of these two paired lobes are located anterior to the buccal tube. The third pair of brain lobes are situated posterioventrally to the first two lobes, and flank the buccal tube. In addition, A. doryphorus possesses a subpharyngeal ganglion, which is connected with the first of the four ventral trunk ganglia. The first and second brain lobes in A. doryphorus innervate the clavae and cirri of the head. The innervations of these structures indicate a homology between, respectively, the clavae and cirri of A. doryphorus and the temporalia and papilla cephalica of eutardigrades. The third brain lobes innervate the buccal lamella and the stylets as described for eutardigrades. Collectively, these findings suggest that the head region of extant tardigrades is the result of cephalization of multiple segments. Our results on the brain anatomy of Actinarctus doryphorus support the monophyly of Panarthropoda.

The metameric pattern of Hypsibius dujardini(Eutardigrada) and its relationship to that of other panarthropods

“…Extant tardigrade species inhabit marine, freshwater, and terrestrial habitats [10,11]. The metameric pattern of tardigrades consists of a head, housing a multilobed brain [12][13][14][15][16][17][18], and four segments bearing lobopodal legs [10,11,19,20]. Based on morphological similarities, a close relationship of Tardigrada with two other ancient lineages, Onychophora and Arthropoda, has long been acknowledged; the taxon Panarthropoda was erected in recognition of this relationship [10,12,[20][21][22][23].…”

“…This debate stems in part from disagreements concerning the relationship of the tardigrade brain to the arthropod brain. In the tripartite hypothesis of tardigrade brain composition, paired outer, inner, and ventral brain lobes are considered to be serially homologous to segmental ganglia [17][18][19][20]34]. This is based on similarities in structure between lobes and ganglia, such as the presence of commissures.…”

“…This is based on similarities in structure between lobes and ganglia, such as the presence of commissures. Under this hypothesis, there is direct homology between tardigrade brain lobes and the three segments of the arthropod brain [17][18][19][20]34]. Generally, the inner lobe of the tardigrade brain is aligned with the protocerebrum, the outer lobe with the deuterocerebrum, and the ventral lobe with the tritocerebrum [20,34].…”

“…Proponents of the tripartite hypothesis have presented confocal microscopy investigations of Halobiotus crispae (Eutardigrada) [17] and Actinarctus doryphorus (Heterotardigrada) [18]. The above studies are generally in agreement that tardigrades possess a multilobed brain, but how many lobes are present in the brain and the relationship of brain lobes across Tardigrada are not well resolved.…”

“…By contrast, under the protocerebral hypothesis, there is no subesophogeal ganglion, because its existence would require the brain to be composed of at least two ganglia. A subesophageal ganglion was included in the brain anatomy interpretations of several studies [13,17,18,20,34]. However, most recent studies of tardigrade brain anatomy have not identified a subesophogeal ganglion [15,[35][36][37].…”