Tardigrada

Panarthropoda (coined by Claus Nielsen in 1995) is the crown-group superclade within Ecdysozoa that unites three living phyla of segmented, legged molting animals: Arthropoda (insects, crustaceans, myriapods, and chelicerates), Onychophora (the terrestrial velvet worms), and Tardigrada (the microscopic water bears or moss piglets). Together with their extinct stem-group relatives—the soft-bodied and armored Cambrian lobopodians (Hallucigenia, Microdictyon, Aysheaia, and Kerygmachela) and the radiodont anomalocaridids (Anomalocaris, Opabinia)—panarthropods are defined by a segmented body bearing paired ventrolateral appendages terminated by hardened claws, a chitinous cuticle shed periodically via 20-hydroxyecdysone signaling, a dorsal ostiate heart, and a spacious open blood cavity (hemocoel or mixocoel) derived from the embryonic fusion of segmental coelomic pouches with the blastocoel.

Exceptionally preserved Konservat-Lagerstätten from the Early and Middle Cambrian Explosion (the Chengjiang biota at ~518 Ma, Sirius Passet at ~518 Ma, and the Burgess Shale at ~508 Ma) preserve the step-by-step anatomical assembly of the panarthropod body plan from unjointed "lobopod" legs to sclerotized, pivot-jointed arthropod limbs (arthropodization):

1. Basal Xenusiid Lobopodians (Aysheaia, Hallucigenia, Luolishania): Possessed an annulated, flexible cuticular trunk supported by paired, unjointed, telescopic hydrostatically inflated lobopodia ending in curved chitinous claws. In 2014–2015, Martin R. Smith and Jean-Bernard Caron used electron microscopy of Burgess Shale Hallucigenia sparsa fossils to show that its stacked conical claws match the nested internal jaw-and-claw structure of modern Onychophora, whereas other Cambrian lobopodians sit on the total-group stem of Panarthropoda.
2. Gilled Lobopodians and Radiodonts (Kerygmachela, Pambdelurion, Opabinia, Anomalocaris): Evolved lateral swimming flaps alongside ventral lobopods, stalked compound eyes, and—in radiodonts like Anomalocaris canadensis—a pair of fully arthropodized, sclerotized frontal raptorial appendages hinged by flexible arthrodial membranes before the trunk body wall or walking legs became sclerotized (arthrodization).
3. Euarthropoda: Completed sclerotization of the dorsal tergites, ventral sternites, and biramous/uniramous trunk limbs, coupled with segment fusion into specialized functional tagmata (head/cephalon, thorax, and abdomen).

Living Onychophora (velvet worms, divided into equatorial Peripatidae and temperate Gondwanan Peripatopsidae) are nocturnal ambush predators of humid leaf litter and rotting logs whose lineage has remained terrestrially bound since the Carboniferous (~300 Ma). Despite their soft, velvety, water-permeable cuticle (which lacks a waterproof epicuticular wax layer and bears thousands of unclosable tracheal spiracles, restricting them to high-humidity microhabitats), velvet worms capture fast-moving crickets, termites, and spiders using a remarkable biomechanical weapon:

• Oscillating Slime Jets and Shear-Induced Protein Gelation: Modified nephridial glands on the third head segment (oral papillae) squirt twin jets of liquid proteinaceous slime at speeds of 3–5 m/s over distances up to 30 cm. Driven by microfluidic pressure, the flexible papilla tips whip back and forth at 30–60 Hz via elastic fluid-structure instability, coating the prey in a disordered net. As the prey struggles, mechanical extensional shear forces cause globular, high-molecular-weight proline-rich intrinsicaly disordered slime proteins and nanoglobular lipid-protein complexes to assemble instantly into stiff β-sheet amyloid-like fibers (Young's modulus ~4 GPa when dry), immobilizing the insect within seconds; once the velvet worm consumes its meal, it eats its own dried slime threads to recycle the nitrogen.
• Resolving the Arthropod Head Problem: Embryological expression of the segment-polarity gene engrailed and Hox genes in onychophorans (Euperipatoides) by Graham E. Budd, Georg Mayer, and Maximilian J. Telford proved that the sensory "antennae" of velvet worms arise from the first (protocerebral/ocular) brain neuromere, whereas their chitinous jaws arise from the second (deutocerebral) neuromere—demonstrating that onychophoran antennae are not homologous to the deutocerebral antennae of insects/crustaceans (nor to chelicerae), which instead correspond to the velvet worm's second-segment jaws.

Tardigrada (discovered by Johann August Ephraim Goeze in 1773 as kleiner Wasserbär, "little water bear," and named Tardigrada, "slow stepper," by Lazzaro Spallanzani in 1776) are microscopic aquatic-film animals inhabiting mosses, lichens, marine sediments, and cryoconite glacier holes worldwide.

1. Loss of the Intermediate Trunk (Antp–Ubx–abd-A Deletion): Comparative genomics of the tardigrades Hypsibius exemplaris and Ramazzottius varieornatus (Smith et al., 2016; Yoshida et al., 2017) revealed why tardigrades have only four leg-bearing segments: the tardigrade ancestor underwent radical body-plan miniaturization, deleting the entire mid-trunk region along with the five intermediate Hox genes (Scr, ftz, Antp, Ubx, and abd-A) that specify the thorax and anterior abdomen in arthropods and annelids. Consequently, the entire four-legged trunk of a tardigrade is anatomically homologous to the anterior head region of an arthropod!
2. Anhydrobiosis and Cytoplasmic Vitrification (CAHS, SAHS, and Dsup Proteins): When a moss cushion dries out, terrestrial tardigrades retract their eight legs and contract longitudinally into a barrel-shaped tun, losing >97% of their intracellular free water and reducing metabolic oxygen consumption to undetectable levels (cryptobiosis). In the tun state, tardigrades survive temperatures from 1 K (−272 °C) to +151 °C, pressures of 600 MPa (six times the Mariana Trench), the hard vacuum and solar UV of low-Earth orbit (ESA FOTON-M3 mission, 2007), and 4,000 to 5,000 Gray (Gy) of ionizing gamma or X-ray radiation (1,000× the lethal human dose).
   • Tardigrade-Specific Disordered Proteins (TDPs): Whereas brine shrimp (Artemia) and nematodes accumulate up to 15% dry weight of the disaccharide trehalose to replace water hydrogen bonds, many tardigrades synthesize virtually no trehalose. Instead, Thomas Boothby, Bob Goldstein, and colleagues (2017) demonstrated that desiccation induces massive expression of Cytoplasmic Abundant Heat-Soluble (CAHS) proteins—intrinsically disordered proteins that self-assemble into reversible coiled-coil hydrogels and vitrify into a non-crystalline bioglass upon drying, mechanically locking cellular membranes and enzymes against unfolding.
   • Damage Suppressor (Dsup) Nucleosome Shield: Discovered by Takuma Hashimoto, Takekazu Kunieda, and colleagues (2016) in Ramazzottius varieornatus, the tardigrade-unique nuclear protein Dsup (Damage suppressor) uses a positively charged, disordered C-terminal domain (homologous to HMGN nucleosome-binding motifs) to bind directly to nucleosomes, forming a physical and electrostatic cloud over chromosomal DNA that quenches hydroxyl radicals (•OH) generated by X-ray radiolysis of water and cuts DNA double-strand breaks by ~40%–50% even when expressed in human cells.

Are Tardigrada the sister group of Arthropoda ("Tactopoda") or of Nematoida?

In concatenated phylogenomic supermatrices, fast-evolving tardigrades sometimes cluster artificially with nematodes due to long-branch attraction. However, five independent lines of evidence—(1) site-heterogeneous CAT-GTR and Dayhoff-recoded matrices, (2) rare microRNA family gains, (3) shared Engrailed/Pax3/7 segment-polarity expression, (4) paired ventrolateral clawed appendages, and (5) sub-domain partitioned phylogenomics separating folded Pfam cores from disordered SLiMs—confirm that Tardigrada belongs firmly inside Panarthropoda, where Onychophora + Arthropoda (or Tardigrada + Arthropoda, the Tactopoda hypothesis) form the legged crown group.

Did tardigrades acquire 17% of their genome from bacteria by horizontal gene transfer?

No. In 2015, a preliminary assembly of the Hypsibius exemplaris genome claimed that ~17.5% of tardigrade genes were bacterial horizontal transfers, sparking media speculation that horizontal gene transfer explained cryptobiosis. Within months, Georgios Koutsovoulos, Mark Blaxter, and colleagues (2016) proved that the vast majority of those bacterial contigs were unfiltered microbiome contaminants from the tardigrade's culture medium and gut. Clean, re-sequenced genomes of H. exemplaris and R. varieornatus show a true horizontal gene transfer level of only ~0.7% to 1.2% (including a bacterial catalase gene), while the primary radiation/desiccation protectants (CAHS, SAHS, MAHS, and Dsup) are lineage-specific tardigrade inventions.

1. Smith, M. R., & Caron, J. B. (2015). *Hallucigenia*'s head and the pharyngeal armature of early ecdysozoans. Nature, 523(7558), 75–78. doi:10.1038/nature14573
2. Smith, F. W., Boothby, T. C., Giovannini, I., Rebecchi, L., Jockusch, E. L., & Goldstein, B. (2016). The compact body plan of tardigrades evolved by the loss of a large body region. Current Biology, 26(2), 224–229. doi:10.1016/j.cub.2015.11.059
3. Hashimoto, T., Horikawa, D. D., Saito, Y., Kuwahara, H., Kozuka-Hata, H., Shin-I, T., ... & Kunieda, T. (2016). Extremotolerant tardigrade genome and improved radiotolerance of human cultured cells by tardigrade-unique protein. Nature Communications, 7(1), 12808. doi:10.1038/ncomms12808
4. Boothby, T. C., Tapia, H., Brozena, A. H., Piszkiewicz, S., Smith, A. E., Giovannini, I., ... & Goldstein, B. (2017). Tardigrades use intrinsically disordered proteins to survive desiccation. Molecular Cell, 65(6), 975–984. doi:10.1016/j.molcel.2017.02.018
5. Yoshida, Y., Koutsovoulos, G., Laetsch, D. R., Stevens, L., Kumar, S., Horikawa, D. D., ... & Blaxter, M. (2017). Comparative genomics of the tardigrades Hypsibius dujardini and Ramazzottius varieornatus. PLoS Biology, 15(7), e2002266. doi:10.1371/journal.pbio.2002266