Putting the cart before the… snake?

Time to reexamine some assumptions (again)! And also, talk about Hox genes, because do I even need a reason?

Hox genes often come up when we look for explanations for various innovations in animal body plans – the digits of land vertebrates, the limbless abdomens of insects, the various feeding and walking and swimming appendages of crustaceans, the strongly differentiated vertebral columns of mammals, and so on.

Speaking of differentiated vertebral columns, here’s one group I’d always thought of as having pretty much the exact opposite of them: snakes. Vertebral columns are patterned, among other things, by Hox genes. Boundaries between different types of vertebrae such as cervical (neck) and thoracic (the ones bearing the ribcage) correspond to boundaries of Hox gene expression in the embryo – e.g. the thoracic region in mammals begins where HoxC6 starts being expressed.

In mammals like us, and also in archosaurs (dinosaurs/birds, crocodiles and extinct relatives thereof), these boundaries can be really obvious and sharply defined – here’s Wikipedia’s crocodile skeleton for an example:

In contrast, the spine of a snake (example from Wikipedia below) just looks like a very long ribcage with a wee tail:

Snakes, of course, are rather weird vertebrates, and weird things make us sciencey types dig for an explanation.

Since Hox genes appear to be responsible for the regionalisation of vertebral columns in mammals and archosaurs, it stands to reason that they’d also have something to do with the comparative lack of regionalisation (and the disappearance of limbs) seen in snakes and similar creatures. In a now classic paper, Cohn and Tickle (1999) observed that unlike in chicks, the Hox genes that normally define the neck and thoracic regions are kind of mashed together in embryonic pythons. Below is a simple schematic from the paper showing where three Hox genes are expressed along the body axis in these two animals. (Green is HoxB5, blue is C8, red is C6.)


As more studies examined snake embryos, others came up with different ideas about the patterning of serpentine spines. Woltering et al. (2009) had a more in-depth look at Hox gene expression in both snakes and caecilians (limbless amphibians) and saw that there are in fact regions ruled by different Hoxes in these animals, if a little fuzzier than you’d expect in a mammal or bird – but they don’t appear to translate to different anatomical regions. Here’s their summary of their findings, showing the anteriormost limit of the activity of various Hox genes in a corn snake compared to a mouse:


Such differences aside, both of the above studies operated on the assumption that the vertebral column of snakes is “deregionalised” – i.e. that it evolved by losing well-defined anatomical regions present in its ancestors. But is that actually correct? Did snakes evolve from more regionalised ancestors, and did they then lose this regionalisation?

Head and Polly (2015) argue that the assumption of deregionalisation is a bit stinky. First, that super-long ribcage of snakes does in fact divide into several regions, and these regions respect the usual boundaries of Hox expression. Second, ordinary lizard-shaped lizards (from which snakes descended back in the days of the dinosaurs) are no more regionalised than snakes.

The study is mostly a statistical analysis of the shapes of vertebrae. Using an approach called geometric morphometrics, it turned these shapes from dozens of squamate (snake and lizard) species into sets of coordinates, which could then be compared to see how much they vary along the spine and whether the variation is smooth and continuous or clustered into different regions. The authors evaluated hypotheses regarding the number of distinct regions to see which one(s) best explained the observed variation. They also compared the squamates to alligators (representing archosaurs).

The results were partly what you’d expect. First, alligators showed much more overall variation in vertebral shape than squamates. Note that that’s all squamates – leggy lizards are nearly (though not quite) as uniform as their snake-like relatives. However, in all squamates, the best-fitting model of regionalisation was still one with either three or four distinct regions in front of the hips/cloaca, and in the majority, it was four, the same number as the alligator had.

Moreover, there appeared to be no strong support for an evolutionary pattern to the number of regions – specifically, none of the scenarios in which the origin of snake-like body plans involved the loss of one or more regions were particularly favoured by the data. There was also no systematic variation in the relative lengths of various regions; the idea that snakes in general have ridiculously long thoraxes is not supported by this analysis.

In summary, snakes might show a little less variation in vertebral shape than their closest relatives, but they certainly didn’t descend from alligator-style sharply regionalised ancestors, and they do still have regionalised spines.

Hox gene expression is not known for most of the creatures for which vertebral shapes were analysed, but such data do exist for mammals (mice, here), alligators, and corn snakes. What is known about different domains of Hox gene activation in these three animals turns out to match the anatomical boundaries defined by the models pretty well. In the mouse and alligator, Hox expression boundaries are sharp, and the borders of regions fall within one vertebra of them.

In the snake, the genetic and morphological boundaries are both gradual, but the boundaries estimated by the best model are always within the fuzzy boundary region of an appropriate Hox gene expression domain. Overall, the relationship between Hox genes and regions of the spine is pretty consistent in all three species.

To finish off, the authors make the important point that once you start turning to the fossil record and examining extinct relatives of mammals, or archosaurs, or squamates, or beasties close to the common ancestor of all three groups (collectively known as amniotes), you tend to find something less obviously regionalised than living mammals or archosaurs – check out this little figure from Head and Polly (2015) to see what they’re talking about:


(Moving across the tree, Seymouria is an early relative of amniotes but not quite an amniote; Captorhinus is similarly related to archosaurs and squamates, Uromastyx is the spiny-tailed lizard, Lichanura is a boa, Thrinaxodon is a close relative of mammals from the Triassic, and Mus, of course, is everyone’s favourite rodent. Note how alligators and mice really stand out with their ribless lower backs and suchlike.)

Although they don’t show stats for extinct creatures, Head and Polly argue that mammals and archosaurs, not snakes, are the weird ones when it comes to vertebral regionalisation. For most of amniote evolution, the norm was the more subtle version seen in living squamates. It was only during the origin of mammals and archosaurs that boundaries were sharpened and differences between regions magnified. Nice bit of convergent/parallel evolution there!



Cohn MJ & Tickle C (1999) Developmental basis of limblessness and axial patterning in snakes. Nature 399:474-479

Head JJ & Polly PD (2015) Evolution of the snake body form reveals homoplasy in amniote Hox gene function. Nature 520:86-89

Woltering JM et al. (2009) Axial patterning in snakes and caecilians: evidence for an alternative interpretation of the Hox code. Developmental Biology 332:82-89

New genes, new tricks, part 2

In my previous post, I marvelled over the strange and unexpected way duplicated genes behave in fruit flies. The second study I wanted to discuss is also about new fruit fly genes gaining new functions, but unlike the other one, it’s about new genes that didn’t come from pre-existing genes.

Reinhardt et al. (2013) wasn’t the best written paper I’ve read, and I had some difficulty figuring out exactly what was going on in places, but there is some interesting stuff in there nonetheless.

The authors investigated six recently evolved new ?protein-coding genes in Drosophila. They wanted to know how they came about and managed to stick. For example, did they first originate as non-coding RNA genes? Did they gain a function through their RNA copies alone before they began to encode a protein? Or did they first awaken from the no man’s land between old genes with protein-coding potential already present?

This harkens back to one of the papers about new genes that I’d previously discussed. Xie et al. (2012) found that the genes for several human-specific proteins began life (and function?) as RNA genes expressed in particular tissues in ancestral primates. What about the six fly genes the new study investigated?

Reinhardt et al.‘s illustration of the two routes to protein-coding geneness is below. Starting with an inactive stretch of DNA (black line), you need two things: (1) an “on” switch or promoter (green box), which causes the transcription of RNA (blue) from the region, and (2) a sequence that can be translated into a decent length protein (an open reading frame or ORF, pink box). These two can theoretically appear in either order.

Before we get into the meat of the paper, let’s borrow the Drosophila family tree from the 12 genomes project page:

D. melanogaster, third from the top, is the species that has been used for every variety of biological investigation for over a hundred years, and also the focus of this study. However, the other species were also used for comparison, to see exactly where and how the genes originated.

Five of the six genes had a relatively long history, with similar sequences being found in D. yakuba and erecta or even further out in D. ananassae. Three of them were not only there in those species, but could also potentially make a nice protein. In two genes, the sequence or part of it was recognisable all the way to ananassae, but it only had long sensible ORFs in melanogaster itself.

In terms of activity… well, first of all I think they screwed up Figure 2. Supposedly, the names of the species in which transcription of these genes was detected are bolded, but actually, all the names are bolded in all the trees, which doesn’t agree with what they say (or with the green dots signifying the origin of transcription in the same figure). Anyway, assuming the bolding was a mistake and the green dots are in the right place, it sounds like four of the six genes were already active in the common ancestor of melanogaster and yakuba or earlier, while another two were only turned on in the melanogaster/sechellia/simulans lineage.

The order of events varies from gene to gene: four genes had good solid ORFs right from the start, while two were transcribed before they were suitable protein templates. The authors note that we can’t actually be sure whether or not the first four developed an ORF before they became active. To be certain of that, we would need more distantly related species with a matching ORF that isn’t transcribed, but in all four cases the species lacking expression of the gene also totally lack any trace of the sequence. So, while the remaining two genes provide positive evidence for the transcription-first scenario, the jury is still out on the ORF-first option.

In D. melanogaster, the presence of the protein product was confirmed for the four genes with the oldest ORFs. The two youngest may still be translated: the protein data came only from embryos, and in fact all six genes contain short signals that are normally associated with the transport of proteins to specific parts of the cell. You might reason that a gene that never makes a protein doesn’t need such signals, but nevertheless, the authors couldn’t positively confirm the existence of these proteins without data from other life stages.

Where these genes are active brings us back to a common theme we encountered in the previous post. In adult D. melanogaster, all six are most strongly expressed in the testicles, and the products of one of them are exclusive to those organs. Likewise, male larvae show more expression of all six genes than females do. The other species show basically the same pattern.

What do these genes do? Actually, do they do anything? Being expressed, even being translated to protein, doesn’t necessarily equate to having a function. Luckily, “function” is not terribly difficult to test for in fruit flies. There are lots of clever tricks that allow you to manipulate their genes and look at the consequences. In this case, Reinhardt et al. bred flies where these genes were turned off. If I understood them correctly, they managed to do this for five genes, four of which resulted in very dead flies. Weirdly, for all four, the affected flies died at the same life stage, just before hatching from the pupa.

With a different strategy that produced only partial knock-down of the genes, they got themselves some grown-up survivors, which allowed them to test the effect of the genes on male fertility (a sensible question given where these genes are most active). Out of three knock-downs with surviving adults of both sexes, only one showed a serious effect, and that was the one that produced generally crappy, short-lived weakling males anyway, so while these genes are active in the testicles and they might disproportionately affect males, they don’t seem to have much to do with fertility per se.

In general, the results sound like new genes that come from random bits of DNA can very quickly become essential to the organism, and it also sounds very much like an overabundance of transcripts in the testicles doesn’t mean that that’s where their function lies – it’s probably more that all kinds of things are expressed in testicles, and these genes are still expressed there because that’s how they started their lives.

Something big missing from the study is actually testing when these genes became functional – we’re told when they became expressed and when they started making a protein, but without manipulating them in relevant non-melanogaster species, it’s impossible to tell whether either of those means function. *disappointed pout*

And what’s up with those four genes that were necessary for the flies’ survival? The knock-downs all did their killing at the same stage. I don’t know what to think about that, and the authors don’t really offer an explanation beyond describing control experiments to make sure the deaths weren’t an unfortunate side-effect of the manipulation itself. Is there something about the development of adults that attracts new genes? Is the process of metamorphosis especially sensitive to even minor mess-ups? (More sensitive than early embryonic development?) Intuitively, I’d find the first possibility more likely, but gods know intuition is a poor guide to reality…



Reinhardt JA et al. (2013) De novo ORFs in Drosophila are important to organismal fitness and evolved rapidly from previously non-coding sequences. PLoS Genetics 9:e1003860

Xie C et al. (2012) Hominoid-specific de novo protein-coding genes originating from long non-coding RNAs. PLoS Genetics 8:e1002942

New genes, new tricks

I’ve previously written about the birth of new genes. Since new genes are cool, and I just found two recent papers on them, you’re getting more of them.

Part 1: how to survive duplication

Technically, the first paper isn’t about new new genes: Assis and Bachtrog (2013) examined recently duplicated genes in fruit flies. But screw technicalities, what they’re saying makes my eyes pop.

When a gene is accidentally copied, a variety of possible fates can await it. Most of the time, the extra copy just dies. Some mechanisms of gene duplication just take the gene without the regulatory elements it needs to function properly. Even if the new copy works, it’s still redundant, so there’s nothing stopping mutations from destroying it over time. However, sometimes redundancy is removed before the new gene breaks irrevocably, and both copies are kept. This can, in theory, happen in a number of ways. Because I’m feeling lazy, let me just quote them from the paper (square brackets are mine, because I hate repeatedly typing out long ugly words :)):

Four processes can result in the evolutionary preservation of duplicate genes: conservation, neofunctionalization, subfunctionalization, and specialization. Under conservation, ancestral functions are maintained in both copies, likely because increased gene dosage is beneficial (1). Under neofunctionalization [NF], one copy retains its ancestral functions, and the other acquires a novel function (1). Under subfunctionalization [SF], mutations damage different functions of each copy, such that both copies are required to preserve all ancestral gene functions (9, 10). Finally, under specialization, subfunctionalization and neofunctionalization act in concert, producing two copies that are functionally distinct from each other and from the ancestral gene (11).

We might add a variation on NF, too: Proulx and Phillips (2006) theorised that differences in function that arise in different alleles (variants) of a single gene can turn duplication into an advantage, turning the conventional duplication-first, new function-next scenario on its head.

Either way, genomes contain lots of duplicated genes, there’s no question about that. What isn’t nearly as well understood is the relative importance of various mechanisms in producing all these duplicates. It’s much easier to theorise about mechanisms than to test the theories. Since evolution doesn’t stop once a new gene has earned its place in the genome, it can be hard to disentangle the mechanism(s) responsible for its preservation from the stuff that happened to it later. Also, to really assess the relative role of different mechanisms, you’ve got to look at whole genomes.

(Assis and Bachtrog say that this hasn’t been done before, and then go right on to cite He and Zhang [2005], which is a genome-wide study of SF and NF. I guess it doesn’t look at all the mechanisms…)

Assis and Bachtrog used the amazing resource that is the 12 Drosophila genomes project, focusing on D. melanogaster and D. pseudoobscura to find slightly under 300 pairs of genes that duplicated after the divergence of those two species. Since Drosophila genomes are very well-studied, they were able to identify the “parent” and “child” in each pair based on where they sit on their chromosomes. They then also extracted thousands of unduplicated genes from the melanogaster and pseudoobscura genomes, to use as a measure of background divergence between the two species.

To measure changes in gene function, they compared the expression of parent and child genes to each other and to the “ancestral” copy (i.e. the unduplicated gene in the other species) in different parts of the body (if a gene is suddenly turned on somewhere it wasn’t before, it’s probably doing something new!).

Long story short, it turned out that in the majority of cases (167/281) cases the child copy behaved much more differently from the “ancestor” than expected, while the parent copy stayed pretty close. These child copies also showed faster sequence evolution than their parents. This means that NF – and specifically that of the new copy – is the most common fate of newly duplicated genes in these animals. There’s also a fair number of gene pairs where both copies gained new functions or both stuck with the old ones, but only three where both copies lost functions. Pure SF, which very influential studies like Force et al. (1999) championed as the dominant mode of duplicate gene survival, appears to be an incredibly rare occurrence in fruit flies!

A few paragraphs ago I mentioned the caveat that duplicated genes don’t stop evolving just because they’ve managed to survive. Well, the advantage of having all these Drosophila genomes is that you can further break down “young” duplicates into narrower age groups, using the species that fall between melanogaster and pseudoobscura on the tree. However, looking at this breakdown doesn’t change the general pattern – NF of the child copy is the most common and SF is rare or nonexistent in even the youngest age groups, along both the melanogaster and the pseudoobscura lineages.

So what exactly is going on here?

Part of the difference in expression patterns between parent/ancestral and child copies is because these new genes are turned on in the testicles, which might give us a big clue. Testicles, you see, are a bit anarchical. Things that are normally kept silent in the genome, like various kinds of parasitic DNA, wake up and run wild during the making of sperm. If you remember my throwaway reference to duplication mechanisms that cut the gene off from its old regulatory elements – well, the balls are a place where even such lost and lonely genes get a second chance.

The genomic anarchy of testes is also one of the reasons these duplications happen in the first place; the aforementioned mechanism involves those bits of parasitic DNA that copy and paste themselves via an RNA intermediate. The enzymes they use to reverse transcribe this RNA into DNA and insert it back into the genome aren’t particularly discerning, and they’ll happily do their thing on a piece of RNA that isn’t the parasite. Indeed, slightly more NFed child genes than you’d expect originated via RNA, although it’s worth noting that more than half of them still didn’t. So while the testes look like a good place for new gene copies to find a use, they aren’t totally responsible for their origins.

Why is there so little SF among these genes?

This is the Obvious Question; my jaw nearly landed on my desk when I saw the numbers. The authors have two hypotheses, both of which may be true at the same time.

First, SF assumes that the two copies have the same functions to begin with. This is not necessarily true when just a small segment of DNA is duplicated – even when it’s not just a bare gene you’re copying, the new copy might lose part of its old regulatory elements and/or land next to new ones, not to mention Proulx and Phillips’s idea of new functions appearing before duplication. So maybe SF is more common after wholesale duplications of entire genomes, and Drosophila species didn’t have any of those recently.

Secondly, SF happens by genetic drift, which is a random process that works much better in small populations. Fruit flies aren’t known for their small populations, and therefore the dominant evolutionary force acting on their genomes will be selection.

This makes sense to me, but the degree to which NF dominates the picture is still pretty amazing. I wonder what you’d get if you applied the same methods to different species. Would species with smaller populations, or those that recently duplicated their whole genomes, show more evidence for SF as you’d expect if the above reasoning is correct? Or would the data slaughter all those seemingly reasonable explanations? What would you see in parthenogenetic species that have no males (and testicles)?

Part two, with really new genes, hopefully coming soon…



Assis R & Bachtrog D (2013) Neofunctionalization of young genes in Drosophila. PNAS 110:17409-17414

He X & Zhang J (2005) Rapid subfunctionalization accompanied by prolonged and substantial neofunctionalization in duplicate gene evolution. Genetics 169:1157-1164

Force A et al. (1999) Preservation of duplicate genes by complementary, degenerative mutations. Genetics 151:1531-1545

Proulx SR & Phillips PC (2006) Allelic divergence precedes and promotes gene duplication. Evolution 60:881-892

A difficult landscape for the RNA world?

I’m back, and right now I can’t really decide if I should be squeeful or sad about Jiménez et al. (2013).

On the side of squeeing, I have some pretty compelling arguments.

  1. It’s an RNA world paper. I’m an unabashedly biased fan of the RNA world. (Not that my opinion matters, seeing as that’s the only origin-of-life hypothesis I actually know anything about. It’s like voting for the only party whose campaign ads you’ve seen.)
  2. I find the actual experiment ridiculously cool. It’s a bit like that mutation study about heat shock protein 90 that I wrote about aaaaages ago, except these guys evaluated the relative fitness of pretty much every single possible RNA molecule of 24 nucleotides. Yes, that is 4^24 different RNA molecules, each in many copies. And they did it twice, just to make sure they weren’t mistaking statistical flukes for results [1].
  3. It explores the landscape of evolution and digs into Big Questions like, how inevitable/reproducible is evolution? Or, as Stephen Jay Gould would put it, what would happen if we replayed the tape of life?

On the other hand, the findings are a bit… bleak. So the experimental setup was to select from this huge pool of RNA sequences for ones that could bind GTP, which is basically a building block of RNA with an energy package attached. In each round of selection, RNAs that could attach the most strongly to GTP did best. (The relative abundances of different sequences were measured with next-generation sequencing.) The main question was the shape of the fitness landscape of these RNAs: how common are functional GTP-binding sequences, how similar do they have to be to perform this function, how easily one functional sequence might mutate into another, that sort of thing.

And, well.

  1. There were only 15 fitness peaks that consistently showed up in both experiments. (A fitness peak consists of a group of similar sequences that are better at the selected function than the “masses”.) That sounds like GTP-binding RNAs of this size are pretty rare.
  2. The peaks were generally isolated by deep valleys – that is, if you were an RNA molecule sitting on one peak and you wanted to cross to another, you’d have to endure lots of deleterious mutations to get there. In practical terms, that means you might never get there, since evolution can’t plan ahead [2].

On the other other hand…

  1. This study considered only one function and only one environment. We have no idea how the look of the landscape would change if an experiment took into account that a primordial RNA molecule might have to do many jobs to “survive”, and it might “live” in an environment full of other molecules, ions, changing temperatures, whatever. (That would be a hell of an experiment. I think I might spontaneously explode into fireworks if someone did it.)
  2. It’s not like this is really a problem from a plausibility perspective. The early earth did have a fair amount of time and potentially, quite a lot of RNA on its hands. I don’t think it originally would have had much longer RNA molecules than the ones in this experiment, not until RNA figured out how to make more of itself, but I’m pretty sure it had more than enough to explore sequence space.

4^24 molecules is about 2.8 x 10^14, or about half a nanomole (one mole is 6 x 10^23 molecules). One mole of 24-nt single-stranded RNA is roughly 8.5 kilos – I’d think you can fit quite a bit more than a billionth of that onto an entire planet with lots of places conducive to RNA synthesis. So I see no need to panic about the plausibility of random prebiotic RNA molecules performing useful (in origin-of-life terms) functions. (My first thought when I read this paper was “oh my god, creationism fodder,” but on closer inspection, you’d have to be pretty mathematically challenged to see it as such.)

So, in the end… I think I’ll settle for *SQUEEE!* After all, this is a truly fascinating experiment that doesn’t end up killing my beloved RNA world. On the question of replaying the tape, I’m not committed either way, but I am intrigued by anything that offers an insight. And this paper does – within its limited scope, it comes down on the side of evolution being very dependent on accidents of history.

Yeah. What’s not to like?



[1] I’ve worked a bit with RNA, and I have nothing but admiration for folks who do it all the time. The damned molecule is a total, fickle, unstable pain in the arse. And literally everything is full of almost unkillable enzymes that eat it just to mock your efforts. Or maybe I just really suck at molecular biology.

[2] I must point out that deleterious mutations aren’t always obstacles for evolution. They can contribute quite significantly to adaptation or even brand new functions. I’m racking my brain for studies of real living things related to this issue, but all I can find at the moment is the amazing Richard Lenski and co’s experiments with digital organisms, so Lenski et al. (2003)  and Covert et al. (2013) will have to do for citations.



Covert AW et al. (2013) Experiments on the role of deleterious mutations as stepping stones in adaptive evolution. PNAS 110:E3171-3178

Jiménez JI et al. (2013) Comprehensive experimental fitness landscape and evolutionary network for small RNA. PNAS advance online publication, 26/08/2013, doi: 10.1073/pnas.1307604110

Lenski RE et al. (2003) The evolutionary origin of complex features. Nature 423:139-144

Oxygen and predators and Cambrian awesomeness (with worms!)

I didn’t plan to write anything today, but damn, Cambrian explosion. And polychaetes. I can’t not. Plus I’m going on holiday soon, so I might as well get something in before I potentially disappear off the internet. (Below: a Cambrian polychaete, Canadia spinosa, via the Smithsonian’s Burgess Shale pages.)

First, a confession.

I’m a bit of a coward about the Cambrian explosion.

Make no mistake, I love it. It’s fascinated me ever since I came across the heavily Stephen Jay Gould-flavoured account in The Book of Life. It’s an event that made the world into what it is today, with its complex ecosystems full of animals eating, cooperating or competing with each other. And it’s one of the great mysteries of palaeontology. What actually happened? What caused it? Why did it happen when it did? Why didn’t it happen again when animal life was nearly wiped out at the end of the Permian?

The problem is, I love it so much that I’m afraid to have an opinion about it. You have no idea how many times I wanted to discuss the big questions, only to shy away for fear of getting it wrong. Which is really kinda stupid, because no one has the one and only correct answer. Whether I’m qualified to comment on it is a different issue, but it wouldn’t be the first subject I comment on that I don’t fully understand.

So, here I take a deep breath and plunge into Sperling et al. (2013).

The abstract started by scaring me. It begins, “The Proterozoic-Cambrian transition records the appearance of essentially all animal body plans (phyla), yet to date no single hypothesis adequately explains both the timing of the event…” To which my immediate reaction was “why the fuck would you want a single hypothesis to explain it?” But luckily, they don’t. They actually argue for a combination of two hypotheses, which they think are more connected than we thought.

But let’s just briefly establish what the Cambrian explosion is.

I want to make this absolutely clear: it’s not the sudden appearance of modern animals out ot nowhere. It could be more accurately described as the appearance of basic body plans we traditionally classify as phyla, such as echinoderms, molluscs, or arthropods, in a relatively short geological period.

Doug Erwin (2011) trawled databases and literature to draw up a timeline of first appearances for animal phyla, and he found that they increase in number gradually over a period of 80 million years (see Erwin’s plot below).


Appearance of “phyla” also doesn’t equal appearance of modern animals, as Graham Budd has been known to emphasise (e.g. Budd and Jensen, 2000). For example, I already mentioned how none of the mid-Cambrian echinoderms recently described by Smith et al. (2013) would look familiar today. In fact, the modern classes of echinoderms, which include sea urchins, starfish and sea lilies, didn’t appear until after the Cambrian. Likewise, while there were chordates (our own phylum), and probably even vertebrates, in the Cambrian, such important vertebrate features as jaws or paired appendages were yet to be invented. (If memory serves, both of those inventions date to the Silurian.)

There is also a discussion to be had about the meaning and validity of concepts like a phylum or a body plan, but let’s not complicate things here. I have a paper to get to! 🙂

With that out of the way…

There is no doubt that something significant happened shortly before and during the Cambrian. Before the very latest Precambrian, fossils show little evidence of movement, of predation, or of the diverse hard parts that animals use to protect themselves or eat others today. All of these become commonplace during the Cambrian, establishing essentially modern ecosystems (Dunne et al., 2008).

There are many explanations proposed to account for the revolution. I’ve not the space (or the courage) to discuss them in any detail. If you’re interested, IIRC Marshall (2006) is a very nice and balanced review. (Link leads to a free copy.) However, we can discuss what Sperling et al. have to say about two of them.

The first hypothesis is oxygen, which likely became more abundant in the ocean towards the end of the Precambrian. That  could explain the timing, but maybe not the nature of the explosion. Oxygen levels impose a limit on the maximum size of animals, but what compels larger animals to “invent” more disparate body plans? (Also, on a side note, many Ediacaran organisms weren’t exactly tiny, so I’m not sure how much of a size limit there is in the first place.)

The second one is animal-on-animal predation (Sperling et al. prefer the term “carnivory”), which can lead to predator-prey arms races and therefore encourage the evolution of innovations like shells or burrowing or jaws that give one party an edge. This is a decent enough basis for body plan innovation, but it applies for any time and place with animals. So if carnivory is the explanation, why did the explosion happen when it did?

Because, Sperling et al. argue, carnivory and oxygen are linked.

I’m intrigued by their approach. They’re not looking at fossils in this study at all. (I always like it when palaeontology and the biology of the living join forces!) They are looking at oxygen-poor habitats in modern oceans. Specifically, they asked how low oxygen levels affect polychaete worm communities.

Why polychaetes? The authors give a list of reasons. One, polychaetes are really, really abundant on the seafloor, and particularly so in low-oxygen settings. Two, different species feed in almost every conceivable way from filtering plankton through chewing through sediment to flat out devouring other animals, and their feeding mode can usually be guessed even if you haven’t seen that particular species eat. Three, they are actually quite good at handling oxygen limitation. This is important because back in the Precambrian, all animals would have been well adapted to a low-oxygen environment, so a group that can tolerate the same may be the best comparison. (They do note that  a previous study of a single low-oxygen site that took other animals into account came up with similar results to theirs.)

They worked partly with pre-existing datasets that met a set of criteria designed to get a complete and unbiased view of local polychaete diversity. In total, they analysed data from 68 sites together featuring nearly a thousand species of worms. They also had some of their own data.

They categorised their study sites into four levels of oxygen deprivation, and counted numbers of carnivorous individuals and species at each site. They came to the conclusion that lack of oxygen basically makes carnivores disappear. The lowest-oxygen samples contained fewer carnivores on both the individual and species levels, and they were more likely to be devoid of predators altogether (# species plot from the paper below):


There are a couple of different ways in which lack of oxygen could limit predators. For example, the aforementioned size limit is one, because it’s good for a predator to be larger and stronger than its prey. But the biggest factor according to the authors is the energy required for an active predatory lifestyle. While a suspension feeder can sit in one place all day and only move to stuff a food-laden tentacle into its mouth, a predator has to find, subdue and eat its prey, which are all pretty expensive activities. Then it also has to digest a sudden, large meal, whereas the suspension feeder’s digestion works at a low and steady rate. Animals can get energy from a variety of metabolic processes, but by far the most efficient route requires oxygen. And that really sucks when you are a hunter who might need large amounts of energy at short notice.


Although I’m quite intrigued by the study, there are a couple of issues that bother me. For example, as far as I could tell, all of the study sites included in the analyses were low on oxygen. I would have liked to see them compared to “normal” sites, in particular because the trend in predator abundance wasn’t a neat straight upwards line. In fact, the least oxygen-deprived habitats appeared less predator-infested than slightly more oxygen-poor ones. What’s going on there?

In terms of interpretation in relation to the Cambrian, I also would have liked to see a comparison of the oxygen levels at their study sites to what’s estimated for the geological periods in question. I take it they just didn’t have precise enough estimates, because one of the things they discuss in the closing paragraph is the need to measure just how much oxygen went into the oceans during this late Precambrian oxygen increase.

And my semi-silly question is, how does this apply to “predators” who don’t run around chasing after and wrestling with prey? For example, sea anemones might be perfectly happy to eat large creatures. But they don’t really do much. They just sit and wait, and if a poor fish stumbles onto their sticky venomous tentacles, tough luck for it. Or there’s the unknown predator that drilled holes in late Precambrian Cloudina specimens (Bengtson and Zhao, 1992). Cloudina was sessile, the creature didn’t have to chase it… Predators such as these still have to cope with the energy demands of digesting sudden large meals, I suppose, so maybe the energetics idea still applies. And of course, if there’s no oxygen, large prey is less likely to be swimming around bumping into your tentacles.

Is this “the” explanation of the Cambrian explosion? Probably not, says the cynic in me. I highly doubt we’re done with that question. Is it a good explanation? Well, it is certainly evidence-based, and I like it that it tries to take different factors together and in context. What I don’t think it does is explain the uniqueness of the Cambrian. A thousand words or so ago, I mentioned the Permian extinction. That cataclysm very nearly left the earth devoid of animals. Afterwards, there was certainly enough oxygen for predators to thrive in the sea, and indeed they did, from sea urchins to ichthyosaurs. So why didn’t the first 40 million years of the Mesozoic era beget many new phyla the way the first 40 million years of the Palaeozoic did? Is that just an artefact of our classifications or was something really fundamentally different going on?

I ain’t Jon Snow, but when it comes to the Cambrian, I still feel like I know nothing…



Bengtson S & Zhao Y (1992) Predatorial borings in Late Precambrian mineralized exoskeletons. Science 257:367-369

Budd GE & Jensen S (2000) A critical reappraisal of the fossil record of the bilaterian phyla. Biological Reviews 75:253-295

Dunne JA et al. (2008) Compilation and network analyses of cambrian food webs. PLoS Biology 6:e102

Erwin DH (2011) Evolutionary uniformitarianism. Developmental Biology 357:27-34

Marshall CR (2006) Explaining the Cambrian “explosion” of animals. Annual Review of Earth and Planetary Sciences 34:355-384

Smith AB et al. (2013) The oldest echinoderm faunas from Gondwana show that echinoderm body plan diversification was rapid. Nature Communications 4:1385

Sperling EA et al. (2013) Oxygen, ecology, and the Cambrian radiation of animals. PNAS 110:13446-13451

Lotsa news

Hah, I open my Google Reader (damn you, Google, why do you have to kill it??? >_<), expecting to find maybe a handful of new articles since my last login, and instead getting both Nature and Science in one big heap of awesome. The latest from the Big Two are quite a treat!


By now, of course, the internet is abuzz with the news of all those four-winged birdies from China (Zheng et al., 2013). I’m a sucker for anything with feathers anywhere, plus these guys are telling us in no uncertain terms that four-wingedness is not just some weird dromaeosaur/troodontid quirk but an important stage in bird evolution. Super-cool.


Then there is that Cambrian acorn worm from the good old Burgess Shale (Caron et al., 2013). It’s described to be like modern acorn worms in most respects, except it apparently lived in a tube. Living in tubes is something that pterobranchs, a poorly known group related to acorn worms do today. The Burgess Shale fossils (along with previous molecular data) suggest that pterobranchs, which are tiny, tentacled creatures living in colonies, are descendants rather than cousins of the larger, tentacle-less and solitary acorn worms. This has all kinds of implications for all kinds of common ancestors…


Third, a group used a protein from silica-based sponge skeletons to create unusually bendy calcareous rods (Natalio et al., 2013). Calcite, the mineral that makes up limestone, is not normally known for its flexibility, but the sponge protein helps tiny crystals of it assemble into a structure that bends rather than breaks. Biominerals would just be ordinary rocks without the organic stuff in them, and this is a beautiful demonstration of what those organic molecules are capable of!


And finally, Japanese biologists think they know where the extra wings of ancient insects went (Ohde et al., 2013). Today, most winged insects have two pairs of wings, one pair on the second thoracic segment and another on the third. But closer to their origin, they had wing-like outgrowths all the way down the thorax and abdomen. Ohde et al. propose that these wing homologues didn’t just disappear – they were instead modified into other structures. Their screwing with Hox gene activity in mealworm beetles transformed some of the parts on normally wingless segments into somewhat messed up wings. What’s more, the normal development of the same bits resembles that of wings and relies on some of the same master genes. It’s a lot like bithorax mutant flies with four wings (normal flies only have two, the hindwings being replaced by balancing organs), except no modern insect has wings where these victims of genetic wizardry grew them. The team encourage people to start looking for remnants of lost wings in other insects…

Lots of insteresting stuff today! And we got more Hox genes, yayyyy!



Caron J-B et al. (2013) Tubicolous enteropneusts from the Cambrian period. Nature advance online publication 13/03/2013, doi: 10.1038/nature12017

Natalio F et al. (2013) Flexible minerals: self-assembled calcite spicules with extreme bending strength. Science 339:1298-1302

Ohde T et al. (2013) Insect morphological diversification through the modification of wing serial homologs. Science Express, published online 14/03/2013, doi: 10.1126/science.1234219

Zheng X et al. (2013) Hind wings in basal birds and the evolution of leg feathers. Science 339:1309-1312

“Same” function, but the devil is in the details.

Aaaaaand todaaaaay, ladies and, um, other kinds of people…. Hox genes!

Considering that I did my Honours project on them and I think they are made of awesome, I’m kind of shocked by the general lack of them here*. Hmmmmmm. Well, having just found Sambrani et al. (2013), I think today is a good time to do something about that.

Hox genes in general are “what goes where” type regulators of development. In bilaterian animals, they tend to work along the head to tail axis of the embryo. (Cnidarians like sea anemones also have them, but the situation re: main body axis and Hox genes in cnidarians is a leeeetle less clear. And heaven knows what sort of weird things happened with the rest of the animals.)

Hox genes are responsible for one of the peculiarities of the insect body plan. Unlike many other arthropods, insects have leg-free abdomens. On the left below is a poor little lobster with legs or related appendages all the way down (plus a bonus clutch of eggs). (Arnstein Rønning, Wikimedia Commons). To her right is a bland, boring insect abdomen (Hans Hillewaert, Wikimedia Commons).

As I said, Hox genes are responsible for the difference. Three of them are expressed in various segments of the abdomen of a developing insect: Ultrabithorax (Ubx), Abdominal-A and Abdominal-B. I’m going to whip out that amazing fluorescent image of Hox gene expression in a fruit fly embryo from Lemons and McGinnis (2006) because aside from being cool as hell, it also happens to be a good illustration:

(The embryo is folded back on itself, so the Abd-B-expressing tail end is right next to the Hox gene-free head)

In insects, all three can turn off the expression of the leg “master” gene distal-less (dll). However, they turn out to do so through two different mechanisms. Ubx and Abd-A proteins have long been known to team up with the distantly related Extradenticle (Exd) and Homothorax (Hth). With their partners, the Hoxes can sit on a regulatory region belonging to the dll gene and prevent its activation.

Sambrani et al. were curious whether Abd-B works in the same way. Sure enough, Abd-B also represses dll wherever it shows up. However, when it comes to interacting with Exd and Hth, differences start to emerge. For starters, those two aren’t even present in the rear end of the abdomen, where Abd-B does its business. When the researchers took the regulatory region of dll and threw various combinations of proteins at it, they found that (1) Abd-B is perfectly capable of binding the DNA on its own, (2) Exd, Hth or engrailed (another Hox cofactor) didn’t improve this ability at all, (3) Hth alone or in combination with the others actually inhibited the binding of Abd-B to the dll regulatory sequence.

Interestingly, dll repression in the anterior and posterior abdominal segments requires the exact same bits of regulatory DNA even though different proteins are involved. It looks like in the posterior segments, Abd-B actually takes over an “Exd” binding site – maybe that’s how it can do the job without getting Exd itself involved.

Furthermore, while the DNA-binding ability of Abd-B is crucial to its ability to kill dll expression, the same is not the case for Ubx. The authors speculate that cooperation with Exd and Hth kind of exempts Ubx from having to bind the regulatory sequences itself, while Abd-B, being on its own, can’t afford to slack off like that. The paper illustrates the idea with such a deliciously ugly pair of drawings that I feel compelled to post it:

(I know they’re going for colour-matching with the fluorescent images, but unfortunately glowy greens and reds that look good on a black background kind of just hurt my eyes on white.)

I don’t really have a point to make here. (There doesn’t always have to be a point, right?) There’s absolutely nothing surprising about the fact that different Hox genes evolved the same overall function in different ways –  after all, they existed as separate entities long before insects lost their buttward legs. I just think Hox genes are cool, and this was an interesting look into the nuts and bolts of how they work. And that’s that.



*Well, aside from this one I’ve written three posts about them and a couple more where they are mentioned. That’s maybe not that bad considering how many different things I’m interested in.



Lemons D and McGinnis W (2006) Genomic evolution of Hox gene clusters. Science 313:1918-1922

Sambrani N et al. (2013) Distinct molecular strategies for Hox-mediated limb suppression in Drosophila: From cooperativity to dispensability/antagonism in TALE partnership. PLoS Genetics 9:e1003307.

Echinoderm bonanza

Smith et al. (2013) has been sitting on my desktop waiting to be read for the last month or so. Man, am I glad that I finally opened the thing. I’m quite fond of echinoderms, and this paper is full of them. Of course. It’s about echinoderms. Specifically, it’s about the diverse menagerie of them that existed, it seems, a little bit earlier than thought.

The brief little paper introduces new echinoderm finds from two Mid-Cambrian formations in Morocco, which at the time was part of the great continent of Gondwana. As far as I’m concerned, it was worth reading just for this lineup of Cambrian echinoderms. I mean, echinoderms are so amazingly weird in such a variety of ways. They’re a delight.


(The drawings themselves are from Fig. 3. of the paper; I rearranged them to fit into my post width, and the boxes are my additions. Dark box = new groups/species from Morocco, light grey box = known groups/species whose first appearance was pushed back in time by the Moroccan finds.)

Although none of the creatures above belong to the living classes of echinoderms, they display a wide range of body plans. You could say their body plans are more diverse* than those of living echinoderms. (And if you said that, the ghost of Stephen Jay Gould would nod approvingly.) For example, modern echinoderms tend to have either (usually five-part) radial symmetry (any old starfish) or bilateral symmetry that clearly comes from radial symmetry (heart urchins).

In these Early- to Mid-Cambrian varieties, you can see some five-rayed creatures, some that are more or less bilateral without any obvious connection to the prototypical five-point star, animals that are just kind of asymmetric, and those strange spindle-shaped helicoplacoids that look like someone took an animal with radial symmetry and wrung it out. And then there are all the various arrangements of arms and stalks and armour plates that I tend to gloss over when reading about the beasts. (Yeah. I have no attention span.)

The Morroccan finds have some very interesting highlights. The second creature in the lineup above is one of them. Its top half looks like a helicoplacoid such as Helicoplacus itself (first drawing). It’s got that characteristic spiral arrangement of plates and a mouth at the top end. However, unlike previously known helicoplacoids, it sits on a stalk that resembles the radially-symmetric eocrinoids (like the creature on its right). It’s a transitional form all right, though we’ll have to wait for future publications and perhaps future discoveries to see which way evolution actually went. It’ll already help palaeontologists make sense of helicoplacoids themselves, though, which I gather is a big thing in itself. The authors promise to publish a proper description of the creature, which is really exciting.

The other exciting thing about the Moroccan echinoderms is their age. As I already hinted at with my grey boxes, the new fossils push back the known time range of many echinoderm body plans by millions of years. This means that the wide variety of body plans we saw above was already present as little as 10-15 million years after the first appearance of scattered bits of echinoderm skeleton in the fossil record.

Smith et al. argue that this is a fairly solid conclusion based on the mineralogy of echinoderm skeletons. Organisms with calcium carbonate hard parts have a tendency to adopt the “easiest” mineralogy at the time they first evolve skeletons. Seawater composition changes over geological time; most importantly, the ratio of calcium to magnesium fluctuates. Calcium carbonate can adopt several different crystal forms, and the Ca/Mg ratio influences which of them are easier to make. So when there’s a lot of Mg in the sea, aragonite is the “natural” choice, whereas low Mg levels favour calcite.

The first appearance of echinoderms around 525 million years ago coincides with a shift in ocean chemistry from “aragonite seas” to “calcite seas”. Echinoderms and a bunch of other groups that first show up around that time have skeletons that are calcite in their structure but incorporate a lot of Mg. Since the ocean before was favourable to aragonite, it’s unlikely that echinoderm skeletons appeared much earlier than this date. In other words, echinoderm evolution during this geologically short period was truly worthy of the name “Cambrian explosion”.

That is, of course, if the appearance of echinoderm skeletons precedes the appearance of echinoderm body plans. The oldest of our Cambrian treasure troves of soft-bodied fossils, such as the rocks that yielded the Chengjiang biota of China, are roughly the same age as the first echinoderm skeletons. However, they don’t contain undisputed echinoderms as far as I can tell (Clausen et al., 2010). Proposed “echinoderms” from before the Cambrian are even less accepted. Of course, the unique structure of echinoderm skeletons is easy to recognise, but how do you identify an echinoderm ancestor without such a skeleton? (Is all that bodyplan diversity even possible without hard skeletal support?)

Caveats aside, this Moroccan stuff is awesome. And also, if my caveat proves overly cautious, echinoderms did some serious evolving in their first few million years on earth. A supersonic ride with Macroevolution Airlines?


*OK, if I want to be absolutely pedantic, and I do, then body plans are disparate rather than diverse. “Disparity” in palaeontological/evo-devo parlance refers to how different two or more creatures are. Diversity means how many different creatures there are. Maybe I should do a post on that, actually.



Clausen S et al. (2010) The absence of echinoderms from the Lower Cambrian Chengjiang fauna of China: Palaeoecological and palaeogeographical implications. Palaeogeography, Palaeoclimatology, Palaeoecology 294:133-141

Smith AB et al. (2013) The oldest echinoderm faunas from Gondwana show that echinoderm body plan diversification was rapid. Nature Communications 4:1385

Macroevolution Airlines

(This post has been mostly written for a long time but I never got round to publishing it. It’s kind of my darling baby, and I never felt quite ready to let it out into the world. Well, every parent has to let go at some point…)

In the creation vs. evolution section of Christian Forums, “macroevolution” is a common topic of name-calling discussion. At some point in what seems like every other thread, a creationist demands “proof” of macroevolution. The common reaction from the evolution side is that the creationist doesn’t understand evolution, and macroevolution is just lots of microevolution, and here is a list of observed speciation events anyway. While the first point is true more often than not, I have been increasingly uncomfortable with the second lately. To my mind, and I think to anyone interested in palaeontology and/or evo-devo, it’s not at all obvious that macroevolution must be fundamentally similar to the everyday adaptations and driftings we commonly observe real-time.

(Image from the UCMP Understanding Evolution site)

What exactly is macroevolution?

Before I continue my musings, I must first clarify what I mean by micro- and macroevolution. I see two interpretations in use in the scientific community, and I don’t think they are entirely equivalent. The “rigorous” interpretation defines microevolution as anything that happens this side of speciation. Populations adapting to short-term environmental change, individuals and their genes migrating back and forth between neighbouring populations, ordinary everyday genetic drift, etc. are microevolutionary phenomena. Macroevolution starts with the formation of new species. The “wishy-washy” interpretation defines macroevolution as “evolution on the large scale”, or “big change”. This is the one I think many palaeontologists would prefer, and many students of evo-devo as well. This is also the one most creationists seem to have in mind. Most – if not all – of the examples in the well-worn speciation lists I’m guilty of pulling out myself are only macroevolution in the first sense. This is something people often seem unaware of: speciation and big change do not go hand in hand.

The definition I prefer (and I changed my mind on this fairly recently) is the second, because despite its vagueness, it gives us a word for something vitally important, all the things that are (usually) bigger than the evolutionary processes we can readily observe on human timescales. How did something resembling a sausage on legs give rise to the mind-boggling diversity of arthropods? How did our own ancestors end up with legs instead of fins? Why did dinosaurs grow into giants and rule the land while the ancestors of mammals retreated to the shadows? This is what macroevolution means to me. As far as I’m concerned, the population geneticists’ kind of macroevolution already has a perfectly good word for it, and that word is speciation.

The question: what is the question?

With that in mind, is macroevolution something different? This is actually at least two questions. One can ask whether the external forces that set out the path of evolution act in the same way on all scales. Did the environment always exert the same kinds of pressures on living things? The answer to this is probably no – from the appearance of oxygen in the atmosphere to the arrival of predators in animal communities, both non-living and living factors have changed the rules of ecosystems many times in earth history. Do the same sorts of pressures that determine the fate of single populations also affect whole lineages? Does selection operate on more than one level? Do the same traits that natural selection favours in ordinary times also help you in extraordinary times? (Another “no”, if David Jablonski can be believed.)

Alternatively, one can also ask whether small and large changes in the properties of organisms are governed by different intrinsic rules. Do, say, new body parts originate through the same kinds of mutations as new hair colours? Are major changes and small adjustments associated with different developmental stages (Arthur, 2008)? Did the nature of variation itself change over evolutionary time (Gould, 1989; Erwin, 2011)? That last one especially intrigues me, and it may yet return in future meanderings. (It’ll return in force if I ever muster the fortitude to discuss the Cambrian explosion ;))

The way to America

In the aforementioned creation vs. evolution debates, physical distance is a commonly used analogy for evolutionary distance. If you believe in centimetres, the argument goes, how can you not believe in kilometres? If you can walk to the kitchen, why can’t you walk a mile?

I think this analogy is worth examining a little further, because it turns out to be great parallel to the micro vs. macro issue. It is true that anyone who can walk can walk a mile. It may take long and it may tire you out, depending on your physique, but it is possible. However, it isn’t very hard to think of destinations that are simply impossible to reach by walking. I live in Europe. Barring ice ages and Bering land bridges, no amount of steps would take me to America. It is still possible for me to go there, but I have to take a flight or perhaps hop on a ship. Is macroevolution like a mile, or is it more like the distance between Europe and the New World? Does a velvet worm-like creature evolve into an arthropod by lots of tiny steps of its chubby legs, or does it take a ride with Macroevolution Airlines?



Arthur W (2008) Conflicting hypotheses on the nature of mega-evolution. In: Minelli A & Fusco G (eds.) Evolving Pathways: Key Themes in Evolutionary Developmental Biology. Cambridge University Press, pp. 50-61

Erwin DH (2011) Evolutionary uniformitarianism. Developmental Biology 357:27-34

Gould SJ (1989) Wonderful Life: The Burgess Shale and the Nature of History. W. W. Norton & Co.

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.)


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…


[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