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:


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 🙂 ) 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.


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?



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


*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
 well. That sort of reasonable advice is hard to hear with the oozing fog-grey suckers of that thing clamped onto my brain.

Thumbs down, what?

Bird fingers confuse me, but the explanations confuse me more, it seems.

I didn’t mean to post today, but I’ve just read a new review/hypothesis paper about the identities of the stunted little things that pass for fingers in the wings of modern birds. The review part is fine, but I’m not sure I get the difference between the hypothesis Čapek et al. (2013) are proposing and the hypothesis they are trying to replace/improve.

To recap: the basic problem with bird fingers is that fossil, genetic and developmental evidence seem to say different things about them.

1. Fossils: birds pretty clearly come from dinosaurs, and the early dinosaurs we have fossils of have five fingers on their hands with the last two being reduced. Somewhat closer to birds, you get four fingers with #4 vestigial. And the most bird-like theropods have only three fingers, which look most like digits 1, 2 and 3 of your ordinary archosaur. (Although Limusaurus messes with this scheme a bit.)

2. Embryology: in developing limb buds, digits start out as little condensations of tissue, which develop into bits of cartilage and then finger bones. Wing buds develop a short-lived condensation in front of the first digit that actually forms, and another one behind the last “surviving” digit. Taking this at face value, then, the fingers are equivalent to digits 2, 3 and 4.

3. Genetics: In five-fingered limbs, each digit has a characteristic identity in terms of the genes expressed during its formation. The first finger of birds is most like an ordinary thumb, both when you focus on individual genes like members of the HoxD cluster and when you take the entire transcriptome. However, the other two digits have ambiguous transcriptomic identities. That is, bird wings have digit 1 and two weirdos.

Add to this the fact that in other cases of digit loss, number one is normally the first to go and number four stubbornly sticks around to the end, and you can see the headache birds have caused.

So those are the basic facts. The “old” hypothesis that causes the first part of my confusion is called the frame shift hypothesis, which suggests that the ancestors of birds did indeed lose digit 1, as in the digit that came from condensation 1 – but the next three digits adopted the identities of 1-2-3 rather than 2-3-4. (This idea, IMO, can easily leave room for mixed identities – just make it a partial frame shift.)

Čapek et al.’s new one, which they call the thumbs down hypothesis, is supposedly different from this. This is how the paper states the difference:

The FSH postulates an evolutionary event in which a dissociation occurs between the developmental formation of repeated elements (digits) and their subsequent individualization.


According to the TDH no change of identity of a homeotic nature occurs, but only the phenotypic realization of the developmental process is altered due to redirected growth induced by altered tissue topology. Digit identity stays the same. Also the TDH assumes that the patterning of the limb bud, by which the digit primordia are laid down, and their developmental realization, are different developmental modules in the first place.

(Before this, they spent quite a lot of words explaining how the loss of the original thumb could trigger developmental changes that make digit 2 more thumb-like.)

I…. struggle to see the difference. If you’ve (1) moved a structure to a different position, (2) subjected it to the influence of different genes, (3) and turned its morphology into that of another structure, how exactly is that not a change in identity?

Maybe you could say that “an evolutionary event” dissociating digit formation and identity is different from formation and identity being kind of independent from the start, but I checked Wagner and Gauthier’s (1999) original frame shift paper, and I think what they propose is closer to the second idea than the first:

Building on Tabin’s (43) insight, we suggest causal independence between the morphogenetic processes that create successive condensations in the limb bud and the ensuing developmental individualization of those repeated elements as they become the functional fingers in the mature hand, thus permitting an opportunity for some degree of independent evolutionary change.

Am I missing something? I feel a little bit stupid now.



Čapek D et al. (2013) Thumbs down: a molecular-morphogenetic approach to avian digit homology. Journal of Experimental Zoology B, published online 29/10/2013, doi: 10.1002/jez.b.22545

Wagner GP and Gauthier JA (1999) 1,2,3 = 2,3,4: A solution to the problem of the homology of the digits in the avian hand. PNAS 96:5111-5116

Another man after my own heart

It’s not terribly hard to turn me into a squealing fangirl. One of the ways is to agree with me eloquently and/or share my pet peeves. Another is to give me lightbulb moments. A third is to disagree with me in a well-reasoned, intelligent way. And finally, if I see you thoughtfully examining your own thinking, you are awesome by definition. MichaĂ«l Manuel’s monster review of body symmetry and polarity in animals (Manuel, 2009) did all of the above.

(In case you wondered, that means a long, squeeful meandering >.>)

Manuel writes about the evolution of two fundamental properties of animal body plans [1]: symmetry and polarity. You probably have a good intuitive understanding of symmetry, but here’s a definition anyway. An object is symmetrical if you can perform some transformation (rotation, reflection, shifting etc.) on it and get the same shape. Polarity is a different but equally simple concept – it basically means that one end of an object is different from the other, like the head and tail of a cat or the inner and outer arcs of a rainbow.

I can’t say that I’d thought an awful lot about either before I came across this review, so it’s not really surprising that I had lightbulbs going off in my head left and right while I was reading it. Because I didn’t think deeply about symmetry and polarity and complexity, I basically held the mainstream view I – and, I suspect, most of the mainstream – mostly picked up by osmosis.

That meant I fell victim to my own biggest pet peeve big time – I believed, without good reason and without even realising, that the body plan symmetries of major lineages of living animals represented successive increases in complexity. Sponges are kind of asymmetrical, cnidarians and ctenophores are radially symmetrical, and bilaterians such as ourselves have (more or less) mirror image symmetry, and these kinds of symmetry increase in complexity in this order. Only… they aren’t, and they don’t.

It turns out that this guy not only shares my pet peeve but uses it to demolish my long-held hidden assumptions. Double fangirl points!

Let there be light(bulbs)!

Problem number one with the traditional view – aside from ignoring that evolution ain’t a ladder – is that the distribution of symmetry types among animals is a little more complicated. Most importantly, most kinds of sponges are not asymmetrical. Most species may be, but that’s not the same thing. You see, most sponge species are demosponges, which make up only one of the four great divisions among sponges. Demosponges do have a tendency towards looking a bit amorphous, but the other three – calcareous sponges, glass sponges and homoscleromorphs – usually are some kind of symmetrical. All in all, the evidence points away from an asymmetrical animal ancestor. (Below: calcareous sponges being blatantly symmetrical, from Haeckel’s Kunstformen der Natur.)

The second problem is that my old view ignores at least one important kind of symmetry. Some “radially” symmetrical animals are actually closer to cylindrical symmetry. To understand the difference, imagine rotating a brick and a straight piece of pipe around their respective long axes. You can rotate the pipe as much or as little as you like, it’ll look exactly the same. In contrast, the only rotation that brings the brick back onto itself is turning it by 180° or multiples thereof. A pipe, with its infinitely many rotational symmetries, is cylindrically symmetrical, while the brick has a finite number of rotational symmetries [2], making it radially symmetrical.

Problem number three is that bilateral symmetry is actually no more complex than radial symmetry! What does “complexity” mean in this context? Manuel defines it as the number of coordinates required to specify any point in the animal’s body. In an animal with cylindrical symmetry, you only need a maximum of two: where along the main body axis and how far from the main body axis you are. Everything else is irrelevant, since these are the only axes along which the animal may be polarised. (Add any other polarity axis, and you’ve lost the cylindrical symmetry.)

Take a radially symmetrical creature, like a jellyfish. These also have a main rotational axis and an inside-outside axis of polarity. However, now the animal’s circumference is also divided up into regions, like slices in a cake. How does a skin cell around a baby jelly’s mouth know whether it’s to grow out into a tentacle or contribute to the space between tentacles? That is an extra instruction, an extra layer of complexity. We’re up to three. (Incidentally, here’s some jellyfish symmetry from Haeckel’s Kunstformen. [Here‘s photos of the real animal] A big cheat he may have been, but ol’ Ernst Haeckel certainly had an eye for beauty!)

And with that, jellies and their kin essentially catch up to the basic bilaterian plan. Because what do you need to specify a worm? You need a head-to-tail coordinate, you need a top-to-bottom one, and you need to say how far from the plane of symmetry you are. Still only three! Many bilaterians, including us, added a fourth coordinate by having different left and right sides, but that’s almost certainly not how we started when we split from the cnidarian lineage. (Below: radial symmetry doesn’t hold a monopoly on beauty! Three-striped flatworm [Pseudoceros tristriatus] by wildsingapore.)

Not only that, but Manuel argues that there’s very little evidence bilateral symmetry evolved from radial symmetry. By his reckoning, the most likely symmetry of the cnidarian-bilaterian common ancestor was cylindrical and not radial (more on this later, though). Thus the (mostly) radial cnidarians and the (mostly) bilateral bilaterians represent separate elaborations of a cylinder rather than stages in the same process.

There were a bunch more smaller lightbulb moments, but I’m already running long, so let’s get on to other things.

Respectful disagreement

I think my disagreements with Manuel’s review are more of degree than of kind. Our fundamental difference of opinion comes back to the symmetries of various ancestors and the evidence for them. He argues that key ancestors in animal phylogeny – that of cnidarians + bilaterians, that of cnidarians + bilaterians + ctenophores, and that of all animals – were cylindrical. (Below is the reference tree Manuel uses for his discussion, with symmetry types indicated by the little icons.)


I think he may well be correct in his conclusions, but I’m not entirely comfortable with his reasons. For example, he infers that the last common ancestor of cnidarians and ctenophores was cylindrical. One of his main arguments is that the repeated structures that “break up the cylinder” to confer radial symmetry are not the same in these two phyla. I think this is an intelligent point a smart guy who knows his zoology would make, so disagreement with it becomes debate as opposed to steamrolling [3].

Why I still disagree? As I said, it comes down to degrees and not kinds. Manuel considers the above evidence against a radially symmetrical common ancestor. I consider it lack of evidence for same. The situation reminds me of Erwin and Davidson (2002), which is also one of my favourite papers ever. They raise perhaps the most important point one could make about comparative developmental genetics: homologous pathways could have been present in common ancestors without the complex structures now generated by those pathways being there. Likewise, I think, radial symmetry could have been there in the common ancestor of cnidarians and ctenophores while none of the complex radially symmetrical structures (tentacles, stomach pouches, comb rows etc.) in the living animals were. Perhaps there were simpler divisions of cell types or whatnot that gave rise to the more overt radial symmetry of jellyfish, sea anemones and comb jellies.

In a related argument, Manuel discusses the homology (or lack thereof) of the dorsoventral axis in bilaterians and the so-called directive axis in sea anemones. Sea anemones actually show hints of bilateral symmetry, which prompted some authors (e.g. Baguñà et al., 2008) to argue that this bilateral symmetry and ours was inherited from a common ancestor (i.e. the cnidarian-bilaterian ancestor was bilateral).

I agree with Manuel that the developmental genetic evidence for this is equivocal at best. I even agree with him that developmental genetics isn’t decisive evidence for homology even if it matches better than it actually does in this case. But again, once the genetic evidence is dismissed as inconclusive, he relies on the non-homology of bilaterally symmetrical structures to conclude non-homology of bilateral symmetry. Again, I think this is a plausible but premature inference. Since I’m not sure whether homology or independent origin of bilateral symmetry is the better default hypothesis in this case, and I don’t think the evidence for/against either is convincing, I actually wouldn’t come down on either side as of yet.

But I can see his point, and that’s really cool.

Why else you’re awesome, MichaĂ«l Manuel…

Because you have a whole rant about “basal lineages”. I grinned like a maniac throughout your penultimate paragraph. Incidentally, you might have given me another favourite paper – anything with “basal baloney” in its title sounds like it’s worth a few squees of its own!

Because you apply critical thinking to your own thinking. See where we disagreed, non-homology of structures vs. symmetries, evidence against vs no evidence for, and all that? After you made the argument from non-homology of structures, I expected you to leave it at that. And you didn’t. You went and acknowledged its limitations, even though you stood by your original conclusions in the end.

Because you reminded me that radial symmetry is similar to metamerism/segmentation. I’d thought of that before, but it sort of went on holiday for a long time. Connections, yay!

Because you were suspicious about sponges’ lack of Hox/ParaHox genes. And how right you were!


Phew, that turned out rather longer and less coherent than I intended. And I didn’t even cover half of the stuff in my notes. I obviously really, really loved this paper…


[1] Or any body plan, really…

[2] Astute readers might have noticed that a brick has more than one axis of symmetry, plus several planes of symmetry as well. So it’s not only radially but also bilaterally symmetrical. The one thing it certainly isn’t is cylindrical 😉

[3] Not to say I don’t enjoy steamrolling obvious nonsense, but I also like growing intellectually, and steamrolling obvious nonsense rarely stretches the mind muscles…



Baguñà J et al. (2008) Back in time: a new systematic proposal for the Bilateria. Philosophical Transactions of the Royal Society B 363:1481-1491

Erwin DH & Davidson EH (2002) The last common bilaterian ancestor. Development 129:3021-3032

Manuel M (2009) Early evolution of symmetry and polarity in metazoan body plans. Comptes Rendus Biologies 332:184-209

Treehoppers redux

Or how I learned (again) that there are no truly simple stories in biology.

In the name of fairness and plain old intellectual integrity, I should mention some interesting new developments in the treehopper-helmet-novelty issue. Back in the first treehopper post I acknowledged that I’m a far cry from an entomologist, and a new study argues that Benjamin Prud’homme and the entire crew on Prud’homme et al. (2011) may share that attribute with me.

A paper published recently in the open-access online journal PLoS ONE (MikĂł et al., 2012) questions basically every interpretation the previous study made about those funky thoracic appendages. After dissecting, CT-ing and microscoping several treehoppers and related insects, they conclude that:

  • The helmet is not an appendage that articulates with the first thoracic segment – it’s actually most of the first thoracic segment itself.
  • The joint at the base of the helmet is the articulation between the first two thoracic segments.
  • The paired “helmet buds” Prud’homme et al. reported are more likely to be artefacts of the way they sectioned their specimens, since MikĂł et al. couldn’t find any in treehoppers of a similar developmental stage.

If all of this is correct, that would suggest that the helmet has nothing to do with wings, it’s just like other less extreme outgrowths of the thorax that you find in a large variety of insects.

What about the genes?

If you take a gander at the first treehopper post or Prud’homme et al. (2011) itself, you’ll see that they supported their microscopic observations with gene expression data including two appendage-specific genes and one that they considered specific to wings. However, even I had a note of caution about using Dll/Dlx genes – which seem to be there whenever anything starts sticking out of an animal’s body – as evidence of homology to anything. MikĂł et al. (2012) point out that nubbin, the supposed “wing gene” actually has quite variable roles in wing and other appendage development when you look at more insect species besides fruit flies. The Hth-Dll combo, it appears, is also involved in the development of more obviously non-wing thoracic outgrowths, like beetle horns.

Where does that leave us?

Seeing as I’m still no entomologist, I can’t really take sides in the anatomical arguments. The genetics? What immediately springs to my mind is Keys et al. (1999), and how some butterflies grow their eyespots by the wholesale co-option of a genetic regulatory circuit from wing development. Did the same sort of thing happen to beetles and treehoppers, then?

This, in fact, only reinforces my general opinion about novelties and the nature of genetic evidence. Evolution rarely, if ever, works from scratch, and the boundary between “novelty” and “tinkering” is as blurry as it gets. Thus, “homology” is rarely a clear-cut and straightforward issue. All of that still stands [1], even if treehoppers might have shifted on some sliding scales. (Which direction is an interesting question. Is a re-activated wing homologue more or less “novel” than a generic thoracic outgrowth patterned by some wing circuitry? Does the distinction even make sense?)

All in all, this is getting quite interesting. It feels decidedly like the beginning of a heated debate [2]. I’ll certainly keep an eye out for future episodes of the treehopper saga.


[1] Though I have to say, I have a couple of papers on my reading list that may mess with my opinions… Don’t want to jinx it, so I won’t say more, but I’m hoping to make a post out of them one day.

[2] Or a beautiful friendship. *ducks*



Keys DN et al. (1999) Recruitment of a hedgehog regulatory circuit in butterfly eyespot evolution. Science 283:532-534

MikĂł I et al. (2012) On dorsal prothoracic appendages in treehoppers (Hemiptera: Membracidae) and the nature of morphological evidence. PLoS ONE 7:e30137

Prud’homme B et al. (2011) Body plan innovation in treehoppers through the evolution of an extra wing-like appendage. Nature 473:83-86

What might have been possible

(Of fins, genes, fossils and the nature of evidence)


Behold the lengthy going-on about limbs, developmental genetics and semi-philosophical stuff that I promised! I mentioned that this was long in the making. Ironically, that means I’m not sure I managed to make it coherent… Then again, my blog subtitle does warn you about certain “meanderings” 😉


I previously mentioned that limbs kind of brought me to evo-devo. I haven’t closely followed the subject since, but a recent paper (Schneider et al., 2011) brought it back to my attention. Aside from the nostalgia, the evolution of limbs is also a perfect excuse for me to ruminate on some of the issues I consider important in evo-devo – such as the meaning of evidence, the role of “model organisms” and the nature of homology and novelty. (Some of this I touched on in my treehopper post)

I love developmental genetics. Davis et al. (2007), which through the blurred glasses of hindsight I’ll call the paper that made me an evo-devo nerd, is a genetic study. Genes are really exciting for us evolutionists because they obey different rules from the traits they control. Especially for regulatory genes – those that affect the activity of other genes –, gene sequence doesn’t correspond to the appearance of the organism in any straightforward way. The same circuitry of regulatory genes can also control the development of quite different structures, because most of the actual work is done by their target genes. Therefore, genes can often preserve connections we can no longer see in higher-level traits. (My favourite combination of evidence is genes plus fossils, but bear with me a little…)

The gist of Davis et al. (2007) is as follows. Hands and feet (collectively known as the autopod) are unique to tetrapods, or vertebrates with legs. There’s a special pattern of Hox gene activity that controls autopod formation. This pattern was missing from the fish that had been examined at the time. However, those fish are quite different from the distant ancestors they shared with tetrapods. There are living fish whose fin skeletons include bits that might correspond to digits, and there are many fossil examples. These include, as it later turned out, not just the iconic fishapod Tiktaalik, but also its slightly less tetrapod-like relative Panderichthys (Boisvert et al., 2008). Hence the question: did common lab animals like zebrafish lose the bones and the genetic circuitry, and did the bones of the autopod evolve from particular bones of the ancestral fin, or did tetrapods invent something new?

The answer is almost certainly the former, Davis et al. (2007) tell us after they find the tetrapod kind of Hox gene expression in the fins of a comparatively “primitive” ray-finned fish (Ray-fins are one of the two main groups of bony fishes. The zebrafish is a ray-fin, as are other familiar fish like cod and tuna. The other group – lobe-fins – include lungfish, coelacanths and tetrapods themselves). Around the same time, other teams found similar patterns in lungfish (Johanson et al., 2007), which are probably the closest living relatives of tetrapods, and sharks (Freitas et al., 2007), which are only distantly related to any of the creatures mentioned above.

Schneider et al. (2011), which caused this post, found that some DNA elements that regulate the Hox genes in the autopod are shared by tetrapods, ray-fins and sharks (ergo, probably all living vertebrates with fins or limbs). Together with the evidence from fossil and modern skeletons, this suggests that the digits of tetrapods evolved from pre-existing fin bones by tweaking an ancient genetic program. Fins and limbs really are variations on a single ancient theme. (Illustration of “fishapod” fins and early tetrapod limbs below is by Dennis C Murphy, from Devonian Times)

It is at this conclusion that we come to the stuff Hox gene expression can’t tell us. Knowing that radial bones (or cartilages, as the case may be) in fins and digits in limbs are “really the same thing” in some way is one thing. But radials and digits are not that similar, and neither is a shark’s fin and a newt’s leg. Maybe you’re interested in how one became the other, how fins suited to balancing and manoeuvring in water became limbs suited to plodding along on land. The autopod-like Hox pattern doesn’t say, since it’s basically the same in appendages that look very different, a perfect example of what I said about regulatory genes a few paragraphs back. Clearly, Hox genes define a distinct part of the fin or limb, but they don’t give detailed instructions on how to flesh it out. The details depend on the genes under Hox control.

Unseen ancestors

Now, fins and limbs are relatively easy, because we have a really quite awesome fossil record of their history (and also, some cool computer models :D). But the same lessons we can learn from their example apply equally to countless other cases where the fossil record is silent. Shared expression patterns of “master” genes and genetic pathways are often used to infer things about ancestors that aren’t known from fossils at all (De Robertis, 2008 is a nice review of such pathways). How far can we take such inferences? What does the fact that arthropods, vertebrates and segmented worms all seem to use some of the same genetic pathways to generate their bodies from repeating units (e.g. Stollewerk et al., 2003; Pueyo et al., 2008; Rivera and Weisblat, 2009)? Was their common ancestor as obviously segmented as an earthworm, did it just have a few repeated body parts like a chiton, or maybe nothing more than the basic ladder-like nervous system* of bilaterian animals? Or perhaps even less?

[*Photo of the nervous system of a planarian flatworm stained with a fluorescent dye, by the Agata group.]

The fossil record of early animal evolution (or rather, the lack of it) argues that this common ancestor was relatively small and simple (Erwin and Davidson, 2002). We know that quite different structures can be underpinned by the same “master” genes. Given this, can we really say anything meaningful about such long-extinct creatures? Well, we certainly can. They probably had the genetic circuitry their descendants share today. But what does that say about their body plans?

The answer may not be too far from “fuck all”. That’s why I chose a quote from Tabin et al. (1999) for the title of this post. I couldn’t agree more when they write, “developmental genetics only tells us what characters might have been possible”. I love finding out where we and the other creatures with whom we share this planet came from. That’s why I’m in this business. But there is only so much that any given type of evidence can tell us. And this is why I think the fossil record is so important. Like Erwin and Davidson (2002) argue, it can help us distinguish between “might have beens” in sometimes surprising ways.

Same difference

All of this puts the whole concept of homology into a slightly unsettling new perspective. Homologues (often spelled “homologs” nowadays) are supposed to be traits (genes, organs, behaviours etc.) that are derived from the same ancestral trait. The original concept of homology was defined for whole organs/body parts. Now, what do we do with organs that are made by the same genetic networks? Some of them show obvious historical continuity with the organs of other organisms. A bird’s wing is clearly homologous to my arm, on probably every level imaginable. They are connected by similar position on the body, similar basic structure, similar development and developmental genetics, and a rich fossil record. But that absolutely need not be the case.

Some butterflies use the same genetic circuitry to put eyespots on their wings that insects in general use to subdivide their wings into different regions (Keys et al., 1999). It would be quite absurd to call wings and eyespots homologous because of that – but in a very real sense, the gene network underpinning both is “the same thing”. And there is everything in between. Eyes, for example, share common “master” developmental genes including Pax6/eyeless. They were probably built around homologous cell types (i.e. photoreceptors) in most animals that have them (e.g. Arendt, 2003). Nonetheless, the highly complex eye structures of, say, a squid, a dragonfly and a falcon almost certainly evolved independently. And then there are the strange, confused identities of bird fingers that I talked about on previous occasions. Thus, when we ask the question: “are these two structures homologous?” – there is often no simple yes/no answer. At the very least, you have to ask: at what level?

An ode to diversity

The whole autopod business also highlights the dangers of extrapolation. Scientists believed that the autopod-specific Hox code was invented by tetrapods because their staple experimental fish didn’t have it. But life is a huge, diverse bush. Every twig has its own unique quirks, and we can’t take any of them to represent everything on its branch in every respect. In fact, some of the most popular lab animals – fruit flies, nematode worms, the aforementioned zebrafish – are also among the quirkier denizens of the planet. This is why I find it really really important not to limit ourselves to a few well-worn “model organisms”, not to draw sweeping conclusions from them. Although our common ancestry means that fruit flies or nematodes will in many ways help us understand ourselves, there is no guarantee. Comparative biology thrives on diversity.

(Of course, I say that as an evolutionary biologist working on a non-model organism. I may be somewhat biased ;))



Arendt D (2003) Evolution of eyes and photoreceptor cell types. The International Journal of Developmental Biology 47:563-571

Boisvert CA et al. (2008) The pectoral fin of Panderichthys and the origin of digits. Nature 456:636-638

Davis MC et al. (2007) An autopodial-like pattern of Hox expression in the fins of a basal actinopterygian fish. Nature 447:473-476

De Robertis EM (2008) Evo-devo: Variations on ancestral themes. Cell 132:185-195

Erwin DH & Davidson EH (2002) The last common bilaterian ancestor. Development 129:3021-3032

Freitas R et al. (2007) Biphasic Hoxd gene expression in shark paired fins reveals ancient origin of the distal limb domain. PLoS ONE 2:e754

Johanson Z et al. (2007) Fish fingers: digit homologues in sarcopterygian fish fins. Journal of Experimental Zoology Part B 308:757-768

Keys DN et al. (1999) Recruitment of a hedgehog regulatory circuit in butterfly eyespot evolution. Science 283:532-534

Pueyo JI et al. (2008) Ancestral Notch-mediated segmentation revealed in the cockroach Periplaneta americana. PNAS 105:16614-16619

Rivera AS & Weisblat DA (2009) And Lophotrochozoa makes three: Notch/Hes signaling in annelid segmentation. Development Genes and Evolution 219:37-43

Schneider I et al. (2011) Appendage expression driven by the Hoxd Global Control Region is an ancestral gnathostome feature. PNAS 108:12782-12786

Stollewerk A et al. (2003) Involvement of Notch and Delta genes in spider segmentation. Nature 423:863-865

Tabin CJ et al. (1999) Out on a limb: Parallels in vertebrate and invertebrate limb patterning and the origin of appendages. Integrative and Comparative Biology 39:650-663

Some funky bugs and the novelty of novelty

These must be some of the craziest-looking animals I’ve ever seen.

An assortment of treehoppers (family Membracidae), from Prud'homme et al. (2011)

(Yes, they are actually bugs, as in they belong to order Hemiptera)

Apparently, those extravagant shapes are all due to one special body part called the helmet – an outgrowth of the first thoracic segment of these insects. (Here‘s a little reminder of insect anatomy.) It only occurs in treehoppers, according to Prud’homme et al. (2011). I confess, I know very little about insects in general, and nothing about treehoppers in particular, but talk of evolutionary novelties always gives me a little kick.

[NOTE: I won’t define “novelty” exactly. You can probably figure out what it means, and it’s one of those funny concepts that defies an easy definition. Which is kind of the point of this post, though I didn’t originally intend it to come out that way.]

Evolutionary novelty, at least in complex, multicellular organisms like animals, is usually thought to come from tinkering more than “true” innovation. This is thought to hold on all levels; new genes are often modified versions of old genes, new cell types originate from old cell types, and new body parts are built on old body parts. If you think about it, this makes perfect sense: the old parts are already there, doing jobs that can be used as a starting point, whereas sticking a mutation in a piece of DNA that doesn’t encode anything and stumbling on a useful new gene is not exactly the likeliest event in evolution.

[ASIDE: Whole new body parts practically have to come from old parts on some level – the probability of evolution assembling a complex organ entirely from scratch has many times more zeroes after the decimal point than the probability of accidentally making a new gene. The question is how much of the new part is new. Is it built almost completely from an old structure, such as a whole arm – individual bones, muscles and everything – being modified into a wing, or does it only borrow basic building blocks and put them together in a completely new way?]

The outlandish helmets of treehoppers (sort of) uphold the prevailing view. Prud’homme et al. (2011) tell us that this has been a matter of some controversy – most held that they were “true” novelties that were not homologous to any other body part, but there were clues that there’s more to the story than that. And, indeed.

The first hints were anatomical. Helmets don’t simply grow out of the animal’s back – they are attached by a joint. Above that, they share a few other details, including their tissue structure and their veins, with the appendages almost all insects bear on their other thoracic segments: wings. What’s more, although the mature helmet is a single structure, it develops from two precursors that eventually fuse together. Two wings, two helmet primordia, you get the picture.

Prud’homme et al.‘s investigation involved more than dismantling the thoraxes of baby treehoppers. Homologous structures often share a common genetic underpinning, so they checked the expression of some “wingy” genes (or, to be precise, their protein products) to see just how deep the similarity between helmets and wings extended. The first of these, Nubbin, is wing-specific in better-studied insects. As expected if helmets are homologous to wings, the developing helmet was chock full of Nubbin. The two other genes they analysed, Distal-less (Dll) and homothorax (hth), are more generally expressed in insect appendages (wings, legs and antennae), defining their different regions from base (hth) to tip (Dll). They showed the same expression pattern in the helmet – which doesn’t necessarily mean that helmets are modified wings, but it does suggest they are based on some kind of appendage. And, given what appendages the other thoracic segments bear in the same position…

[NOTE: Well, I don’t know much about hth, but Dll is a bit problematic in this respect. It’s not just an “appendage gene” in insects, but also in a wide variety of other animals. Were it not for Dll expression, no one would suggest homology between, say, the tube feet of a starfish and the legs of a fly (Panganiban et al., 1997) – it’s pretty likely that Dll was originally more of an “anything that sticks out of the body” gene than an “appendage”, never mind a “wing”, gene proper. Dll/Dlx genes also do other stuff, like making neurons migrate in vertebrate brains (Anderson et al., 1997). So Dll expression alone doesn’t mean something is an appendage, let alone a specific type of appendage. Luckily, it’s not alone here. Incidentally, this is lesson number one of comparative/evolutionary developmental genetics. When the question is homology of a structure or process, always look at combinations of genes.]

This is not too surprising given the evolutionary history of wings, or what the fossil record was kind enough to preserve for posterity. The first known winged insects (link leads to drawing of Stenodictya lobata in Grimaldi and Engel, 2005) actually had winglets on the first thoracic segment as well, but those were lost before the last common ancestor of living insects. (How that happened in genetic terms, and how it may have been reversed in treehoppers, is also discussed in the paper, but it isn’t directly relevant to the novelty issue) In a way, treehoppers’ “invention” is a giant laugh in the face of Dollo’s Law, which proposes that complex features don’t re-evolve once they are lost (I kind of touched on this “law” here).

Nevertheless, helmets look nothing like wings and function nothing like wings. (To be fair, they look nothing like one another, either.) They are so dissimilar to their proposed evolutionary sisters that apparently their relationship eluded most researchers. How “novel” are they, then? It’s something of a philosophical question. Since, at this level of complexity, literally nothing comes from scratch, at what point do we stop calling something “tinkering” and start calling it “true novelty”?

As with most philosophical questions, I don’t think this one has a correct answer. That doesn’t mean these questions are not worth pondering. The way we word things influences the way we think about them. Exactly where (or even if) we draw a line between two fuzzy concepts isn’t important in my opinion. But to be aware that there is a dilemma about that line, and that other people may draw it in different places, is. Effective communication is one of my Big Issues, and being critical of your own thinking is an issue that ought to be Big for anyone doing science. (Or for anyone, full stop.) Thinking about unanswerable questions like this is a great way of exercising those (self-)critical muscles.

(Originally, I just wanted to gush about the excitement of figuring out the origin of novelties, but I managed to turn it into a philosophical treatise. Whoda thunk that? <.< )


Anderson SA et al.(1997) Interneuron migration from basal forebrain to neocortex: dependence on Dlx genes. Science 278:474-476

Grimaldi D and Engel MS (2005) Evolution of the Insects. Cambridge University Press.

Panganiban G et al. (1997) The origin and evolution of animal appendages. PNAS 94:5162-5166

Prud’homme B et al. (2011) Body plan innovation in treehoppers through the evolution of an extra wing-like appendage. Nature 473:83-86