The use of a larva?

Hi! Long time no see!

(I think we’ve reached the point where it’s weird to say happy new year. I could swear xkcd had a pertinent chart of funny, but I couldn’t find it.)

Once upon a time, I briefly mentioned the problematic relationships of hemichordates. Since a short paper bearing on the subject came out relatively recently (i.e. in December, yes, I’m far behind the times ;)), I thought I’d revisit it.

To begin, let’s orient ourselves on my trusty old animal phylogeny.

animalPhylogeny

Hemichordates are a phylum of deuterostomes, and their closest relatives appear to be echinoderms like starfish. The inside of Deuterostomia looks something like this:

deuterostomes

Hemichordates come in two flavours: the butt-ugly (but nevertheless intriguing) acorn worm, which even the artistic eye of 19th century zoologists couldn’t make appealing (a selection of them from Johann Wilhelm Spengel’s work below):

… and the slightly nicer-looking pterobranch. Well. They’re kind of fluffy. That counts as “nicer,” right? (A couple of Cephalodiscus from the Halanych lab below):

Acorn worms and pterobranchs have different bodies adapted to very different lifestyles. Pterobranchs are stalked, tentacled filter-feeders that often clone themselves into colonies that live together in a branching tube system. Acorn worms are solitary burrowers without tentacles, tubes or shells. Hemichordates possess features in common with vertebrates, such as gill slits, and they seem a lot less freakish than their sister phylum Echinodermata. So hemichordates are kind of the natural go-to group to look for properties of the deuterostome common ancestor.

The only problem is, to do that, you need a solid understanding of hemichordate phylogeny itself. Because there are two very different kinds of hemichordates, you have to first figure out which of those best represents their common ancestor: the sit-at-home plankton sifter or the roaming mud-eating worm. (Maybe neither. Wouldn’t that be funny.) And, as it happens, there’s some disagreement about that.

One view, espoused by the mighty zoological tome of Brusca and Brusca (2002) among others, puts acorn worms and pterobranchs as separate sister groups, and considers pterobranchs the more conservative of the two. The Bruscas write, on page 869, that “the enteropneusts [= acorn worms] have lost [their tentacles], no doubt in connection with their development of an infaunal lifestyle.” In this view, the deuterostome ancestor was a sessile filter feeder, and the long worm-like body and general moving-aboutiness of other deuterostomes is a new feature.

The other hypothesis, backed by DNA sequence data (Cannon et al., 2009)* and more recently the discovery of a tube-dwelling acorn worm from the Cambrian (Caron et al., 2013), is that pterobranchs are a weird subgroup of acorn worms and therefore unlikely to say much about our own distant ancestors.

One thing that AFAIK both camps agree on is that the ancestral acorn worm had a larva that looked nothing like an acorn worm. That’s something pretty common for marine invertebrates. Creatures as different as sea urchins and ragworms explore the seas by way of tiny, planktonic larvae that later metamorphose into a completely different animal**. (Tornaria larva of an unidentified hemichordate below by Alvaro E Migotto from the Cifonauta image database.)

However, the specific family of acorn worms that pterobranchs supposedly come from does not have such a larval stage. They develop more or less directly from fertilised eggs into mini-acorn worms.

Pterobranchs are poorly studied, so not much is known about their babies. Are they like the conventional acorn worm larva, with its distinctive body plan and curly rows of cilia? Or are they more straightforward precursors of the adult, like their presumed closest cousins? Stach (2013) describes a larva of the pterobranch Cephalodiscus gracilis that looks more like the latter. He found the minuscule creature crawling around in a colony of adult Cephalodiscus, and used thin sections and transmission electron microscopy to make a 3D reconstruction of it.

(His account of finding the baby makes me wonder how the hell he knew it did belong to Cephalodiscus. If my experience with tube-dwelling marine invertebrates is anything to go by, being found in a certain animal’s home is no guarantee that you’re related to said animal. I suppose, incomplete though they may be, older descriptions of pterobranch babies were good enough to identify the little guy?)

The image that emerges is of a rather featureless little sausage. According to Stach, it has a through gut, one full-fledged and one partially formed gill opening (asymmetry like that is not unheard of in deuterostome embryos/larvae), as well as a body cavity and a bunch of muscle cells. What it doesn’t have is any trace of the bands of cilia that “typical” acorn worm larvae use to swim and feed, nor some other structures (e.g. nerve centres) that characterise such larvae.

Taken at face value, this would suggest (assuming this is a typical pterobranch larva) that the pterobranchs-are-acorn worms people are right. I have my reservations, and not just because a sample size of one makes me statistically nervous. Using this description as evidence for evolutionary relationships assumes that traditional larvae with ciliary bands are hard to lose. But that’s quite possibly not the case.

Echinoderm larvae, for example, have changed a lot even in the last few million years. The changes occurred many times independently, and often involved a return from a full-fledged larval stage to more direct development (Raff and Byrne, 2006). I don’t know whether acorn worms display a similar sort of flexibility. How many have even been studied in terms of development?

So: detailed internal structure of a pterobranch larva? Cool. As to the worms first hypothesis… “consistent with” would be a better description than “supports”, I think.

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Notes:

*Although microRNAs beg to differ (Peterson et al., 2013).

**The history of these larvae is a mighty can of worms, or trochophores and tornariae as the case may be. I shall say no more on the matter here. 🙂

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References:

Brusca RC & Brusca GJ (2002) Invertebrates (second edition). Sinauer Associates.

Cannon JT et al. (2009) Molecular phylogeny of hemichordata, with updated status of deep-sea enteropneusts. Molecular Phylogenetics and Evolution 52:17-24

Caron J-B et al. (2013) Tubicolous enteropneusts from the Cambrian period. Nature 495:503-506

Peterson KJ et al. (2013) MicroRNAs support the monophyly of enteropneust hemichordates. Journal of Experimental Zoology B 320:368-374

Raff RA & Byrne M (2006) The active evolutionary lives of echinoderm larvae. Heredity 97:244-252

Stach T (2013) Larval anatomy of the pterobranch Cephalodiscus gracilis supports secondarily derived sessility concordant with molecular phylogenies. Naturwissenschaften 100:1187-1191

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. Michaël 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.)

ManuelPhylo

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, Michaël 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…

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[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…

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References:

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

Animals, amoebae and assumptions

Animals aren’t the only multicellular creatures in their phylogenetic neighbourhood. Social amoebae, many fungi and quite a few of the poorly known choanoflagellates spend at least part of their lives as collections of cooperating cells. Conventional wisdom has been that these groups invented multicellularity independently, but maybe conventional wisdom needs a bit of challenging.

To tell you the truth, I never really thought about the other possibility, that being multicellular is the original state of affair for these organisms. I never really considered the evidence on which the conventional wisdom was based. You could say I didn’t really care either way. A while back I saw a paper that said something about a social amoeba having an epithelium, but I just kind of shrugged and went on with my life. I don’t know, now an article in BioEssays brought this up again, and I’m not sure I was right to ignore it back then. I think Dickinson et al. (2012) have a point, and I think some assumptions may need to be reexamined.

In case you wondered, an epithelium is a type of tissue made of a layer or layers of polarised cells. “Polarised” means that various cellular components – proteins, attachments to neighbouring cells, organelles – are distributed unevenly in the cell, clustered towards one or the other side of the cell layer. Epithelia line pretty much everything in a typical animal’s body, from, well, the entire body, to things like guts and glands. They secrete important stuff like hormones, and their closely packed cells form a barrier to keep molecules and pathogens where they belong. An epithelium was thought to be a uniquely animal thing to have, but looking more closely at that weird little amoeba suggested it may not be.

The paper that I ignored was Dickinson et al. (2011) – yes, by the exact same people who wrote the BioEssays piece. OK, I didn’t completely ignore it. I read enough of it to scribble a quick note in my citation manager saying “screams convergent evolution to me”. The paper examined the multicellular stage in the life of Dictyostelium discoideum, an ordinarily single-celled amoeba that reacts to food shortages by crowding together with friends and family to form a fruiting body that helps disperse some of its cells in search of new habitats. The fruiting body is pretty complex for a “unicellular” creature, and it turns out that this complexity includes a region of tissue that looks quite a lot like a simple epithelium. It doesn’t just look like one; it sorts out its insides and outsides with the help of proteins called catenins, which are also involved in cell polarity in the epithelia of animals. (Below: D. discoideum being multicellular, from Wikipedia)

That isn’t much evidence to base an inference of homology on, especially since other key players in animal cell polarity are entirely absent from D. discoideum. But equally, the fact that tons of unikonts (the group including amoebae, slime moulds, fungi, choanoflagellates and animals) are single-celled doesn’t mean that the multicellular groups all came up with the idea independently. Evolution doesn’t always increase complexity – sometimes complexity becomes superfluous.

I remember when we discussed the choanoflagellate genome paper (King et al., 2008) in class. The genome in question belongs to a purportedly single-celled creature, but it contains tons of genes you’d think only multicellular organisms would need, such as genes for cell-to-cell adhesion proteins. So one explanation is that these proteins originally did something else, like anchoring a single cell to its favourite spot. Another explanation is that they did have something to do with multicellularity – it just wasn’t the multicellularity of animals at first.

This suggestion isn’t terribly controversial when you’re talking about choanoflagellates, since some of them do obviously form colonies (one such colony of Salpingoeca/Proterospongia rosetta is shown below, from Mark Dayel of the King lab via ChoanoWiki). It’s not hard to imagine that either the “single-celled” species whose genome was sequenced also has a colonial stage the scientists just never saw, or that its recent ancestors did.

Whether or not the same applies to the whole of unikonts is a more difficult question. I’m not at all familiar with the details of unikont relationships, but based on the tree shown in the BioEssays article, multicellularity is all over the group. In most cases, it’s facultative multicellularity; animals are rather the exception in being doomed to it for their entire lives. However, if you just looked at that tree, you’d wonder why the hell anyone thought the common ancestor of these things wasn’t some kind of multicellular.

Yet the details of animal-like multicellularity aren’t so widespread. True cadherins (the cell adhesion proteins I mentioned) have only been found in animals proper. Choanoflagellates and some even more obscure relatives of animals have bits and pieces of them, and other unikonts have none at all as far as anyone knows. Epithelium-like tissues have only been described in that one species of amoeba – but, as Dickinson and colleagues note, no one really looked in the others.

Personally, I wouldn’t be at all surprised if the conventional wisdom ended up shifting. I still don’t think that the evidence from Dictyostelium is enough to draw a conclusion. We obviously need to know a lot more about unikont genomes, tissues and life cycles to piece together the history of multicellularity in the group, but I’m not sure that right now a unicellular ancestor has a lot more going in its favour than a multicellular one. Guess we’ll have to wait and look with an open mind 🙂

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References

Dickinson DJ et al. (2011) A polarized epithelium organized by β- and α-catenin predates cadherin and metazoan origins. Science 331:1336-1339

Dickinson DJ et al. (2012) An epithelial tissue in Dictyostelium challenges the traditional origin of metazoan multicellularity. BioEssays advance online publication, 29/08/2012, doi:10.1002/bies.201100187

King N et al. (2008) The genome of the choanoflagellate Monosiga brevicollis and the origin of metazoans. Nature 451:783-788

 

What might have been possible

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

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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” 😉

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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 ;))

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References

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

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