Comparative myoanatomy of Tardigrada: new insights from the heterotardigrades Actinarctus doryphorus (Tanarctidae) and Echiniscoides sigismundi (Echiniscoididae)

Abstract

BackgroundTardigrada is a group of microscopic invertebrates distributed worldwide in permanent and temporal aquatic habitats. Famous for their extreme stress tolerance, tardigrades are also of interest due to their close relationship with Arthropoda and Cycloneuralia. Despite recent efforts in analyzing the musculature of a number of tardigrade species, data on the class Heterotardigrada remain scarce. Aiming to expand the current morphological framework, and to promote the use of muscular body plans in elucidating tardigrade phylogeny, the myoanatomy of two heterotardigrades, Actinarctus doryphorus and Echiniscoides sigismundi, was analyzed by cytochemistry, scanning electron and confocal laser scanning microscopy and 3D imaging. We discuss our findings with reference to other tardigrades and internal phylogenetic relationships of the phylum.ResultsWe focus our analyses on the somatic musculature, which in tardigrades includes muscle groups spanning dorsal, ventral, and lateral body regions, with the legs being musculated by fibers belonging to all three groups. A pronounced reduction of the trunk musculature is seen in the dorsoventrally compressed A. doryphorus, a species that generally has fewer cuticle attachment sites as compared to E. sigismundi and members of the class Eutardigrada. Interestingly, F-actin positive signals were found in the head appendages of A. doryphorus. Our analyses further indicate that cross-striation is a feature common to the somatic muscles of heterotardigrades and that E. sigismundi—as previously proposed for other echiniscoidean heterotardigrades—has relatively thick somatic muscle fibers.ConclusionsWe provide new insights into the myoanatomical differences that characterize distinct evolutionary lineages within Tardigrada, highlighting characters that potentially can be informative in future phylogenetic analyses. We focus our current analyses on the ventral trunk musculature. Our observations suggest that seven paired ventromedian attachment sites anchoring a large number of muscles can be regarded as part of the ground pattern of Tardigrada and that fusion and reduction of cuticular attachment sites is a derived condition. Specifically, the pattern of these sites differs in particular details between tardigrade taxa. In the future, a deeper understanding of the tardigrade myoanatomical ground pattern will require more investigations in order to include all major tardigrade lineages.

Thermotolerance experiments on active and desiccated states of Ramazzottius varieornatus emphasize that tardigrades are sensitive to high temperatures

“…Tardigrades survive extreme conditions by entering cryptobiosis -a state of extreme dormancy, where metabolism comes to a reversible stop. Cryptobiotic survival in turn depends on the organism sustaining structural integrity and our investigations indicate that actin filaments are crucial for stabilizing the three-dimensional structure of the anhydrobiotic state 22,25,61 . In effect, we propose that ATP dependent "rigor mortis" ensure tardigrade structure during anhydrobiosis.…”

Musculature of an Early Cambrian cycloneuralian animal

“…diagonal ones in platyhelminthes [ 32 ]. There may be exceptions to this generalization; for example, nematodes [ 33 ], nematomorphs [ 34 ], tardigrades [ 35 , 36 ], arthropods [ 2 , 37 ] and some polychaete annelids [ 38 ] lack body-wall circular muscles, most likely due to secondary loss. The Early Cambrian lobopodian Tritonychus has an outer layer of longitudinal, a middle layer of oblique and an inner layer of circular muscles [ 21 ].…”

New records on the rich loriciferan fauna of Trezen ar Skoden (Roscoff, France): Description of two new species of Nanaloricus and the new genus Scutiloricus

“…This is exemplified by the description of and current research on the Roscoff worm, Symsagittifera roscoffensis (Graff, 1891) (see e.g. [1,2]) and by investigations into the diversity and adaptations of tardigrades [3][4][5][6][7]. Notably, the phylum Loricifera was described in 1983 from the study of the first representative specimens found off the coast of Roscoff [8].…”