To dump a chunk of trunk

The Mammal has deemed that Hox genes and good old-fashioned feel-good evo-devo are a good way to blink back to life*. Also, tardigrades. Tardigrades are awesome. Here is one viewed from above, from the Goldstein lab via Encyclopedia of Life:

hypsibius_dujardini_eol

Tardigrades or water bears are also a bit unusual. Their closest living relatives are velvet worms (Onychophora) and arthropods. Exactly who’s closest to whom in that trio of phyla collectively known as the Panarthropoda is not clear, and I don’t have the energy to wade into the debate – besides, it’s not really important for the purposes of this post. What Smith et al. (2016) concluded about these adorably indestructible little creatures holds irrespective of their precise phylogenetic position.

Anyway. I said tardigrades were unusual, and I don’t mean their uncanny ability to survive the apocalypse¬†and pick up random genes in the process (Boothby et al., 2015). (ETA: so apparently there may not be nearly as much foreign gene hoarding as the genome paper suggests – see Sujai Kumar’s comment below! Doesn’t change the fact that tardigrades are tough little buggers, though ūüôā ) The oddity we’re interested in today¬†lies in the fact that all known species are built to the exact same compact body plan.¬†Onychophorans and many arthropods are elongated animals with lots of segments, lots of legs, and often lots of variation in the number and type of such body parts. Tardigrades? A wee head, four chubby pairs of legs, and that’s it.

How does a tardigrade body relate to that of a velvet worm, or a centipede, or a spider? Based solely on anatomy, that’s a hell of a question to answer; even the homology¬†of body parts between different kinds of arthropods can be difficult to determine. I have so far remained stubbornly uneducated on the minutiae of (pan)arthropod segment homologies, although I do see papers purporting to match brain parts, appendages¬†and suchlike between different kinds of creepy-crawlies¬†on a fairly regular basis. Shame on me for not being able to care about the details, I guess – but¬†the frequency with which the subject comes up suggests that the debate is far from over.

Now, when I was first drawn¬†to the evo-devo field, one of the biggest attractions was the notion that the expression of genes as a body part forms¬†can tell us what that body part really is even when anatomical clues are less than clear. That, of course, is too good to be simply true, but sometimes the lure of genes and neat¬†homology stories is just too hard to resist. Smith et al.‘s investigation of¬†tardigrade Hox genes is definitely that kind of story.

Hox genes are generally a good place to look if you’re trying to decipher¬†body regions, since their more or less neat, orderly expression patterns are remarkably conserved between very distantly related animals (they are¬†probably as old as the Bilateria, to be precise). A polychaete worm, a vertebrate and an arthropod show the same general pattern – there is no active Hox gene at the very front of the embryo, then Hoxes 1, 2, 3 and so on appear in roughly that order,¬†all the way to the rear end. There are variations in the pattern – e.g. the expression of a gene¬†can have sharp boundaries or fade in and out gradually; different genes can overlap to different extents, the order isn’t always perfect, etc. – but staggered Hox gene expression domains, with the same genes starting up in the same general area along the main body axis, can be found all across the Bilateria.

Tardigrades are no exception, in a sense – but they are also quite exceptional. First, their complement of Hox genes is a bit of a mess. At long last, we have a tardigrade genome to hand, in which Smith et al. (2016) found good honest¬†Hox genes. What they didn’t find was a Hox cluster, an orderly series of Hox genes sitting like beads on a DNA string. Instead, the Hox genes in Hypsibius dujardini, the sequenced species,¬†are all over the genome, associating with all kinds of dubious fellows¬†who aren’t Hoxes.

What Smith et al.¬†also didn’t find was half of the Hox genes¬†they expected. A typical arthropod has ten or so Hox genes, a pretty standard ballpark for an animal that isn’t a vertebrate. H. dujardini has only seven, three of which are triplicates of Abdominal-B, a gene that normally exists in a single copy in arthropods. So basically, only five kinds of Hox gene – number two and most of the “middle” ones are missing. What’s more, two more tardigrades that aren’t closely related to H. dujardini also appear to have the same five Hox gene types (though¬†only one Abd-B each), so this massive loss is probably a common feature of Tardigrada. (No word on whether the scattering of the Hox ¬†cluster¬†is also shared by the¬†other two species.)

We know that the genes are scattered and decimated, but are their expression patterns similarly disrupted? You don’t actually need an intact Hox cluster for orderly Hox expression, and indeed, tardigrade Hox genes are activated in a perfectly neat and perfectly usual pattern that resembles what you see in their panarthropod cousins. Except for the bit where half the pattern is missing!

Here’s¬†part of Figure 4 from the paper, a schematic comparison of tardigrade Hox expression to that of other panarthropods – a generic arachnid, a millipede and a velvet worm. (otd is a “head” gene that¬†lives in the Hox-free anterior region;¬†lab is the arthropod equivalent of¬†Hox1, Dfd is Hox4, and I’m not sure which of Hox6-8 ftz is currently supposed to be.) The interesting thing about this is that according to Hox genes, the entire body of the tardigrade corresponds to just the front end of arthropods and velvet worms.

Smith_etal2016-hox_tardigrade_fig4A

In addition, one thing that is not shown on this diagram is that Abdominal-B, which normally marks the butt¬†end of the animal, is still active in the tardigrade, predictably in the last segment (L4, that is). So if you take the Hox data at face value, a tardigrade is the arse end of an arthropod tacked straight onto its head. Weird. It’s like evolution took a perfectly ordinary velvet worm-like creature and chopped out most of its trunk.

The tardigrade data suggest¬†that the original panarthropod was probably more like arthropods and velvet worms than tardigrades – an elongated animal with many segments.¬†The strange tardigrade situation can’t be the ancestral one, since the Hox genes that tardigrades lack long predate the panarthropod ancestor. Now, it¬†might be¬†possible to lose half your Hox genes while keeping your¬†ancestral body plan, but an unusual body plan and an unusual set of Hox genes is a bit of a big coincidence, innit?

Smith et al. point out that the loss of the Hox genes was unlikely to be the cause of the loss of the trunk region¬†– Hox genes only specify what grows on a segment, they don’t have much say in how many segments develop in the first place. Instead, the authors reason, the loss of the trunk in the tardigrade ancestor probably made the relevant¬†Hox genes dispensable.

Damn, this story makes me want to see the Hox genes of all those oddball lobopodians from the Cambrian. Some of them are bound to be tardigrade relatives, right?

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References:

Boothby TC et al. (2015) Evidence for extensive horizontal gene transfer from the draft genome of a tardigrade. PNAS 112:15976-15981

Smith FW et al. (2016) The compact body plan of tardigrades evolved by the loss of a large body region. Current Biology 26:224-229

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*The Mammal has been pretty depressed lately. As in mired up to her head in weird energy-sucking flu. Unfortunately, writing is one of those things that the damn brain monster has eaten most of the fun out of. Also, I have a shitty normal person job at the moment, and shitty job taking up time + barely enough motivation to crawl out of bed and pretend to be human¬†means I have, at best, one afternoon per week that I actually spend on catching up with science. That is just enough to scroll through my feeds and file away the interesting stuff, but woefully insufficient for the writing of posts, not to mention that my ability to concentrate is, to be terribly technical, absolutely fucked. It’s not an ideal state of affairs by any stretch, and I’m pretty sure that if I made more of an effort to read and write about cool things, it would pay off in the mental health department, but‚Ķ well. That sort of reasonable advice is hard to hear with the oozing fog-grey suckers of that thing clamped onto my brain.