The Compact Body Plan of Tardigrades Evolved by the Loss of a Large Body Region

Abstract

The superphylum Panarthropoda (Arthropoda, Onychophora, and Tardigrada) exhibits a remarkable diversity of segment morphologies, enabling these animals to occupy diverse ecological niches. The molecular identities of these segments are specified by Hox genes and other axis patterning genes during development [1, 2]. Comparisons of molecular segment identities between arthropod and onychophoran species have yielded important insights into the origins and diversification of their body plans [3-9]. However, the relationship of the segments of tardigrades to those of arthropods and onychophorans has remained enigmatic [10, 11], limiting our understanding of early panarthropod body plan diversification. Here, we reveal molecular identities for all of the segments of a tardigrade. Based on our analysis, we conclude that tardigrades have lost a large intermediate region of the body axis-a region corresponding to the entire thorax and most of the abdomen of insects-and that they have lost the Hox genes that originally specified this region. Our data suggest that nearly the entire tardigrade body axis is homologous to just the head region of arthropods. Based on our results, we reconstruct a last common ancestor of Panarthropoda that had a relatively elongate body plan like most arthropods and onychophorans, rather than a compact, tardigrade-like body plan. These results demonstrate that the body plan of an animal phylum can originate by the loss of a large part of the body.

External morphogenesis of the tardigradeHypsibius dujardinias revealed by scanning electron microscopy

“…Tardigrada, also known as water bears, is a monophyletic group of microscopic invertebrates characterized by a body consisting of five segments (Mayer, Kauschke, Rüdiger, & Stevenson, ; Smith et al, ), four of which carry lobopodous walking appendages, and an aquatic or semi‐terrestrial lifestyle (Nelson, Guidetti, & Rebecchi, ). Together with their closest relatives, the Onychophora (velvet worms) and Arthropoda (invertebrates with articulated appendages), they represent a clade of legged ecdysozoans (molting animals) called Panarthropoda (Rota‐Stabelli et al, ).…”

Clustered brachiopod Hox genes are not expressed collinearly and are associated with lophotrochozoan novelties

“…Hox genes are prone to gains (15-17) and losses (18)(19)(20)(21), and their arrangement in a cluster can be interrupted, or even completely disintegrated (22)(23)(24)(25). Furthermore, the collinear character of the Hox gene expression can fade temporally (24,26,27) and/or spatially (28).…”

Non-model model organisms

“…Water bears’ compact bodies appear to have arisen by loss of a large part of an ancestral body plan, corresponding to the entire thorax and nearly the entire abdomen of Drosophila . This work revealed that animal body plans can arise by loss of a large body part, and a far larger part than we had anticipated [251]. How the finer, essential details of water bear anatomy first evolved and later diversified is not yet known.…”

“…Postdoc Frank Smith, who had developed in situ hybridization methods for water bears, has sought to understand how the compact body plan of water bears arose long ago, back when the major groups of animals had diverged. Frank found that the Hox genes that define the head segments of arthropods are expressed in the same anterior-to-posterior register in water bears—but throughout almost their entire body—leading the animals to be called at times “walking heads” [251, 252]. Water bears’ compact bodies appear to have arisen by loss of a large part of an ancestral body plan, corresponding to the entire thorax and nearly the entire abdomen of Drosophila .…”