No one would argue that tardigrades got stiffed in the weirdness department. These teensy animals, also called water bears, look roly-poly under a microscope. Less than a millimeter long, they can survive extremes of heat, cold, pressure, and radiation that are deadly to most other lifeforms. Under duress, a tardigrade may curl itself into a dried-up ball called a tun, then stay in a state of suspended animation for years before returning to life. Now, researchers poring over the animal's genes have found another oddity. The tardigrade, they say, is essentially one giant head. Frank Smith, who's a postdoc in Bob Goldstein's lab at the University of North Carolina, Chapel Hill, and their colleagues studied the evolution of tardigrades by looking at their genes. Specifically, they looked at bits of DNA called "Hox genes." These are master controllers that organize an animal's body. During development, Hox genes make sure all the parts end up where they're supposed to be. Mutations in Hox genes can cause unsettling problems like, say, legs growing out of the head. The researchers looked for Hox genes in the genome of a tardigrade called Hypsibius dujardini. (Yes, there's more than one tardigrade. There are actually more than 1,100 species, living in wet places all over the planet.) They compared H. dujardini's Hox genes to those of arthropods, the large group of animals that includes bugs of all sorts, plus crustaceans. Arthropods are cousins to tardigrades. The researchers also looked at the genomes of two tardigrades distantly related to H. dujardini. What emerged was a kind of whodunnit. The researchers saw that as tardigrades evolved from the ancestors they shared with arthropods, four or five of their Hox genes had simply disappeared. Next, Smith and his colleagues asked what exactly the surviving Hox genes were doing in the tardigrade. Looking at where those genes switch on during the tardigrade's development, they saw a pattern "nearly identical" to how those genes are turned on in an arthropod's head, Smith says. In other words, most of a tardigrade's body is equivalent to just the head of an arthropod. "Our findings were pretty surprising," Smith says. Previously, scientists had thought that tardigrades evolved their stumpy bodies by fusing body segments together. Finding several totally absent Hox genes was an unexpected twist. Smith says tardigrade ancestors, like many tardigrades alive today, probably lived in sediment on the ocean floor. His coauthor Lorena Rebecchi has speculated that a compact body would have been useful to an ancient tardigrade burrowing through ocean muck. So if a mutation lopped off part of its body, so much the better. Here's what the researchers think happened: The ancestors of tardigrades were longer, with lots of body segments. But mutations cropped up in the genes that made these segments, causing whole sections to disappear from the tardigrade ancestor's middle. Once most of the tiny animal's body was gone, the Hox genes that used to build those segments became unnecessary. Eventually, other mutations erased those genes from the tardigrade's genome. If a tardigrade is a giant head, why does it have so many legs—eight of them? "In fact, arthropod heads most likely also have many legs, evolutionarily speaking," Smith says. There's an idea that all the appendages sticking off an arthropod's head—chewing mouthparts, antennae, and so on—evolved from legs. This fits with what Smith found. "In our model, the many legs of a tardigrade correspond to the many head appendages of an arthropod," he says. Speaking of unsettling.
Image: by Schokraie E, Warnken U, Hotz-Wagenblatt A, Grohme MA, Hengherr S, et al. (2012). Comparative proteome analysis of Milnesium tardigradum in early embryonic state versus adults in active and anhydrobiotic state. PLoS ONE 7(9): e45682. doi:10.1371/journal.pone.0045682
Smith, F., Boothby, T., Giovannini, I., Rebecchi, L., Jockusch, E., & 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