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Link to original content: https://pubmed.ncbi.nlm.nih.gov/37399417
Cambrian lobopodians shed light on the origin of the tardigrade body plan - PubMed Skip to main page content
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. 2023 Jul 11;120(28):e2211251120.
doi: 10.1073/pnas.2211251120. Epub 2023 Jul 3.

Cambrian lobopodians shed light on the origin of the tardigrade body plan

Ji-Hoon Kihm  1 , Frank W Smith  2 , Sanghee Kim  3 , Hyun Soo Rho  4 , Xingliang Zhang  5 , Jianni Liu  5 , Tae-Yoon S Park  1   6
Affiliations

Cambrian lobopodians shed light on the origin of the tardigrade body plan

Ji-Hoon Kihm et al. Proc Natl Acad Sci U S A. .

Abstract

Phylum Tardigrada (water bears), well known for their cryptobiosis, includes small invertebrates with four paired limbs and is divided into two classes: Eutardigrada and Heterotardigrada. The evolutionary origin of Tardigrada is known to lie within the lobopodians, which are extinct soft-bodied worms with lobopodous limbs mostly discovered at sites of exceptionally well-preserved fossils. Contrary to their closest relatives, onychophorans and euarthropods, the origin of morphological characters of tardigrades remains unclear, and detailed comparison with the lobopodians has not been well explored. Here, we present detailed morphological comparison between tardigrades and Cambrian lobopodians, with a phylogenetic analysis encompassing most of the lobopodians and three panarthropod phyla. The results indicate that the ancestral tardigrades likely had a Cambrian lobopodian-like morphology and shared most recent ancestry with the luolishaniids. Internal relationships within Tardigrada indicate that the ancestral tardigrade had a vermiform body shape without segmental plates, but possessed cuticular structures surrounding the mouth opening, and lobopodous legs terminating with claws, but without digits. This finding is in contrast to the long-standing stygarctid-like ancestor hypothesis. The highly compact and miniaturized body plan of tardigrades evolved after the tardigrade lineage diverged from an ancient shared ancestor with the luolishaniids.

Keywords: Cambrian explosion; Panarthropoda; Tardigrada; lobopodia; morphological evolution.

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Conflict of interest statement

The authors declare no competing interest.

Figures

Fig. 1.
Fig. 1.
Images of tardigrades and lobopodians. (A) Apochelan Milnesium sp., DIC image. (B) Arthrotardigrade Parastygarctus sp., DIC image (image courtesy of Shinta Fujimoto). (C) ROM 52707, Cambrian lobopodian Ovatiovermis cribratus (image courtesy of Jean-Bernard Caron). (D) Schematic drawing of the anterior part of Milnesium. (E) Mouth and COS structures of Macrobiotus sp., SEM image. (F) Extracted bucco-pharyngeal apparatus of parachelan tardigrade Dactylobiotus ovimutans, SEM image. (G) Echiniscoidean tardigrade Echiniscus testudo, SEM image. (H) SP-2018-43, mouth of Cambrian lobopodian Pambdelurion whittingtoni, PTM image. Abbreviations: an, anus; atr, anterior tooth row; bl, buccal lobe; bt, buccal tube; cA, cirrus A; cp, cephalic papilla; e, eye; ec, external cirrus; ic, internal cirrus; m, mouth; mc, median cirrus; pc, primary clava; ph, pharynx; pl, peribuccal lamella; pp, peribuccal papilla; pt, pharyngeal teeth; ptr, posterior tooth row; tp, triangular plate; tr, transverse ridge; sc, secondary clava; and st, stylet. Asterisk indicates the dorsal peribuccal lamella.
Fig. 2.
Fig. 2.
The foregut, dorsolateral paired structures, and claws of tardigrades and lobopodians. (A) Bucco-pharyngeal apparatus in place of parachelan tardigrade Dactylobiotus ovimutans, DIC image. (B) Backwardly retracted bucco-pharyngeal apparatus of D. ovimutans, DIC image. (C) ML0020A-2, Cambrian lobopodian Luolishania longicruris. (D) Claw of echiniscoidean tardigrade Cornechiniscus holmeni, SEM image. (E–G) JS0001A, Cambrian lobopodian Onychodictyon ferox and its claws, digital camera images. The scale bars in (F) and (G) are 0.5 mm in length. Abbreviations: atr, anterior tooth row; bl, buccal lobe; bt, buccal tube; mp, macroplacoid; ph, pharynx; pl, peribuccal lamella; ptr, posterior tooth row; and tr, transverse ridge.
Fig. 3.
Fig. 3.
Panarthropod phylogeny. (A) Summary tree showing relationships inferred under Bayesian, maximum likelihood, and maximum parsimony methods. (B) A simplified tree obtained from the Bayesian inference (BI). (C) A simplified tree obtained from the maximum likelihood analysis (ML). (D) A simplified tree obtained from the maximum parsimony strict consensus (MP). See SI Appendix, Figs. S3 and S4 for full tree topologies.
Fig. 4.
Fig. 4.
Comparison of general body plan between luolishaniid lobopodians and tardigrades. A hypothetical luolishaniid lobopodian exhibiting five anterior limb pairs and six posterior limb pairs. A hypothetical tardigrade combining eutardigrade Milnesium (left side) and heterotardigrade Coronarctus (right side). Dark colored parts in the trunk and limb of the luolishaniid lobopodian (Left) are absent in the tardigrade (Right). The anterior regions in the red color represent COS (circumoral sensory field) (see text).
See this image and copyright information in PMC

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