Wheeee!

… sorry, guys. I did say something about squee and headdesk moments on my about page. ^_^;

It’s nothing big, really. I just got my hands on a book I’ve had on my wishlist for years, read a couple of chapters, and so far all I keep thinking is “neeeeeat!”

Dear editors and contributors, you all are officially making me happy. So happy that only the yay turtle can properly express my feelings!

(Seriously, who came up with this picture? It’s just perfect.)

We’ll read the rest of the book, and then we’ll see if Embryos in Deep Time is also as awesome as it sounds…

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Sponges never yield

Ah, those pesky sponges again. Although their lives are rather low on action, these strange animals have found lots of other ways to fascinate me. Borrowed skeletons, mysterious lost Hox genes, wonderful alien shapes and perhaps the oldest fossils that might be animals – sponges have no trouble supplying us with stories.

Sponges are also something of a headscratcher for evolutionary biologists. These days it’s generally agreed that they can be divided into four major groups, the glass sponges (hexactinellids), the demosponges, the calcareous sponges and the homoscleromorphs. My impression is that the close relationship of the first two is also well-established. However, to this day biologists haven’t quite managed to agree whether the three are one lineage to the exclusion of other animals, or two or three separate lineages with some of them being closer to non-sponge animals. The trees below illustrate two possibilities:

spongeBothSmall

This is kind of important if you want to know what kind of organism gave rise to the diversity of animals. If sponges are paraphyletic (some sponges closer to non-sponges, as in the right-hand tree), then the mother of all animals was likely sponge-like, sitting on the seafloor and driving water through its porous body to capture food. In such scenarios, two or three of the deepest branchings of the animal tree run into sponges on one side. The simplest explanation for that is that the ancestors at these branching points were themselves sponge-like.

If, however, sponges are monophyletic (their last common ancestor only gave rise to sponges, as in the left-hand tree), then the last common ancestor of animals immediately branched into sponges and non-sponges, whose living descendants are very different from sponges. Suddenly, guessing what Mummy Metazoa might have been like becomes much harder.

The deepest phylogeny of animals is difficult. We are talking about lineages that diverged over 600 million years ago even by conservative estimates (Peterson et al., 2004), and it’s also likely that their early divergences followed each other in rapid succession. That combination is depressingly good at eroding the useful information in gene and protein sequences (Rokas and Carroll, 2006). So what can a phylogeneticist do?

Picking your genes carefully is one solution – use as many as you can to maximise the information you can glean from them, but don’t use genes that evolve so fast their “information” is basically all noise. Another option is to use so-called rare genomic changes. These are things like gaining and losing bits of genes or insertions of parasitic DNA.

Their advantage is that they are unlikely to occur twice in the same way. If two animals have the same viral sequence between genes A and B, it’s far more likely to indicate relatedness as opposed to chance similarity than having the same letter at position 138 in the sequence of gene A. The principle of parsimony (choose the simplest explanation) is a shitty way of interpreting sequence similarity because there’s a high chance of any given change occurring more than once. It works much better for such unlikely events as gaining a virus in the same spot.

microRNAs look like a pretty good source of rare genomic changes. They are small RNAs encoded in the genome, and they play crucial roles in gene regulation in most animals. Their sequences evolve extraordinarily slowly, so it’s relatively easy to identify them across species despite their tiny size. There’s loads and loads of them – miRbase, the microRNA database, lists 1600 different miRNA genes for humans, yielding over 2000 mature miRNAs after processing. The miRNAs in our genome include everything from ancient types with origins in the mists of the Precambrian to young sequences confined to our close relatives. On top of all that, they are thought to be very difficult to lose. All in all, perfect phylogenetic markers.

Perfect for some cases, that is. Their presences and absences may paint a coherent evolutionary picture for most animals, but don’t ask them about sponges. Robinson et al. (2013) tried…

In their introduction stands this depressing summary of current animal miRNA lore, based on many non-sponge genomes plus that of the demosponge Amphimedon queenslandica:

“None of the thousands of miRNAs thus far discovered in eumetazoans are present in the genome [of] A. queenslandica and none of the eight silicisponge‐specific miRNAs have been described in any eumetazoan (or any other eukaryotic group for that matter).”

(Eumetazoans = all animals except sponges and the Blob; silicisponges = glass sponges + demosponges)

However, that’s only two of the four sponge groups. What about the other two? Are they any more helpful? Might they have silicisponge-like repertoires, supporting sponge monophyly? Or might they be hiding some “eumetazoan” miRNAs, arguing for one history or another involving sponge paraphyly? This is what the authors wanted to find out.

They looked for miRNAs by collecting and sequencing small RNAs from calcareous and homoscleromorph sponges. Two species of the former and one of the latter also have genome projects going, which allowed the researchers to verify the RNAs they found as bona fide miRNAs (miRNA genes have a particular structure that doesn’t all show in the mature RNA product) as well as look for the protein components of the editing machinery miRNAs need to reach maturity.

(Below: the three sponges with newly sequenced genomes. Sycon ciliatum from the Adamska group, Leucosolenia complicata from habitas.org.uk, Oscarella carmela & Oscarella sp. from the Nichols lab.)

Well, the calcarean genomes certainly contained genes for miRNA-processing enzymes, which is a good sign that they also have miRNAs somewhere. So what do those look like?

Overall, the results of Robinson et al.‘s search are a bit disappointing. They used strict criteria to identify miRNAs, since there are plenty of other kinds of small RNA molecules floating around doing stuff in animal cells. According to these criteria, only one miRNA was confidently identified in the calcareous sponges. This was present in both Sycon and Leucosolenia, but the niggardly bastards didn’t share it with either silicisponges or other animals. Leucosolenia may have a second one. A bunch of eumetazoan-like sequences also showed up, but these were probably contamination from actual eumetazoans, since the Sycon genome, which was obtained from squeaky clean lab-grown sponges, had none of them.

Oscarella only yielded two possible miRNAs, neither of which was known from anything else (including the other homoscleromorphs in this study!) Worse, they couldn’t even find the two processing enzymes in the Oscarella genome – they only recovered a small fragment of one. Maybe the genome sequence is just incomplete, which wouldn’t be very surprising. Then again, maybe Oscarella genuinely doesn’t have a functioning miRNA system, and that could be quite interesting.

Either way, now we know something about microRNAs in all the great sponge lineages. It doesn’t look like they’re going to help us sort out deep animal phylogeny, but maybe the very absence of similarities is telling us something. The reason many microRNAs are so conserved in other animals is that they play important roles in fundamental developmental processes, such as specifying cell types. If sponges aren’t really fussed about keeping them, then maybe their development just doesn’t depend heavily on miRNAs. So what do they do with theirs? Why the difference? Questions, questions…

(Incidentally, here’s yet another reason not to just look at one species and make sweeping claims about “sponges”. Here is also a reason to thank the gods for next generation sequencing. Without the ability to quickly and cheaply [for certain values of “cheap”] sequence tons of DNA and RNA from any creature you fancy, half of the story of animal evolution would be hidden in undeciphered strings of DNA in animals too few people care about for a sequencing project. Yay for technology, yay for diversity!)

[P.S.: there’s so much I’ve wanted to write about and didn’t recently. Since I came back from my Christmas break, I’ve spent most of my time buried in work-related literature. Reading more literature was the last thing I wanted to do with my free time. I’m almost done with that, though. No promises, but I’m almost done ;)]

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References:

Peterson KJ et al. (2004) Estimating metazoan divergence times with a molecular clock. PNAS 101:6536-65451

Robinson JM et al. (2013) The identification of microRNAs in calcisponges: independent evolution of microRNAs in basal metazoans. Journal of Experimental Zoology B, advance online publication available 24/01/2013, doi: 10.1002/jez.b.22485

Rokas A, Carroll SB (2006) Bushes in the tree of life. PLoS Biology 4:e352

Is Ediacara really stranded?

Heh, when I wrote a confused post about a paper by Greg Retallack that argues that classic Ediacaran fossils like Dickinsonia come from a terrestrial rather than an underwater environment, I said there’s sure to be responses. And I completely managed to miss the responses in the very same issue of Nature, apparently published online on the same day. *shameface* (I don’t think I got the commentary piece by RSS???)

One of them was actually quite nice to Retallack. L. Paul Knauth’s name doesn’t ring a bell, I suspect he’s the “geologist” out of the “palaeontologist and a geologist” the intro mentions. Of Retallack’s analysis itself, all he has to say is that Precambrian sediments can be very difficult to interpret, and one will need genuine expertise in fossilised soils ‘n’ stuff to evaluate Retallack’s claims. However, Knauth rejoices over the mere fact that there are unorthodox opinions like Retallack’s out in the open. In which he is certainly right – science wouldn’t go anywhere without disagreements.

The other commenter, Shuhai Xiao, is not so kind. (Him I’ve actually heard of; he’s published some seriously interesting stuff about Ediacaran fossils.) His commentary is kind of a polite way of saying “what a load of nonsense”. Like Knauth, he considers the evidence for the terrestrial origin of these rocks ambiguous, but he also emphasises features of the rocks that fairly unambiguously point to a marine environment. Funnily enough, he brings up geology that isn’t totally impenetrable to me as evidence, like a neat photo of Dickinsonia specimens on a slab of rock covered in nice symmetrical-looking ripples (the kind that forms under quiet waves). There’s also the fact that I forgot about when I wrote the other post: Dickinsonia itself is sometimes associated with crawling traces. Whatever that thing was and wherever it lived, it ain’t no lichen.

That’s reassuring in terms of not standing my worldview on its head, but I really wish Xiao had been less vague about some of his points. For instance, “the isotope signatures of carbonate nodules in the Ediacara Member can be accounted for by post-depositional alterations that do not involve pedogenic processes,” he says, with no further explanation and no citations. I’m thus far on Xiao’s side, but that doesn’t turn the above into a good argument…

Oh well. Let the debate rage on 🙂

(As of yet, no citations of Retallack’s paper on Google Scholar. We’ll definitely check back later. If I remember…)

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!

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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

Distinguished company

It hasn’t been long since my friend published her awesome ghost Hox paper, and it has already earned her a great honour. It seems a creationist found it and tried to wrestle it into supporting creationism. (Judging by the comments at Marmotism, he failed big time, in most of the usual creationist ways.)

And with that, young Olivia enters the distinguished company of evolutionary biologists whose works got misrepresented by creationists. Dunno about everyone else, but I’d be pretty proud to belong with the likes of Stephen Jay Gould, Jerry Coyne and Doug Erwin even in such a crooked way…(Sorry, I’ll get off gloating and back to science any time now.)

Archosaur calendar yay!

I’m a total sucker for good, accurate palaeoart, so I’m super excited for the art calendar that the fine people of Hell Creek put together for this year. Discoveries of dinosaurs, pterosaurs and other related beasts from 2012 featured in lovely pieces of art by artists who know their anatomy and shit. I strongly encourage you to take a look 😉

Here’s one of my favourite pieces from the calendar. This particular painting depicts the small Triassic dinosaur relative Diodorus scytobrachion (Kammerer et al., 2012) (art by Adrian Wimmer/yoult@deviantART):

Wheeeeee! ^.^

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Reference:

Kammerer CF et al. (2012) The first silesaurid dinosauriform from the Late Triassic of Morocco. Acta Palaeontologica Polonica 57:277-284