A bit of Hox gene nostalgia

I had the most random epiphany over my morning tea today. I don’t even know what got me thinking about the Cambrian explosion (as if I needed a reason…). Might have been remembering something from the Euro Evo Devo conference I recently went to. (I kind of wanted to post about that, because I saw some awesome things, but too much effort. My brain isn’t very cooperative these days.)


I was thinking about explanations of the Cambrian explosion and remembering how the relevant chapter in The Book of Life (otherwise known as the book that made me an evolutionary biologist)  tried to make it all about Hox genes. It’s an incredibly simplistic idea, and almost certainly wrong given what we now know about the history of Hox genes (and animals)*. At the time, and for a long time afterwards, I really wanted it to be true because it appeals to my particular biases. But I digress.

Then it dawned on me just how new and shiny Hox genes were when this book was written. I thought, holy shit, TBoL is old. And how far evo-devo as a field has come since!

The Book of Life was first published in 1993. That is less than a decade after the discovery of the homeobox in fruit fly genes that controlled the identity of segments (McGinnis et al., 1984; Scott and Weiner, 1984), and the finding that homeoboxes were shared by very distantly related animals (Carrasco et al., 1984). It was only four years after the recognition that fly and vertebrate Hox genes are activated in the same order along the body axis (Graham et al., 1989; Duboule and Dollé, 1989).

This was a HUGE discovery. Nowadays, we’re used to the idea that many if not most of the genes and gene networks animals use to direct embryonic development are very ancient, but before the discovery of Hox genes and their clusters and their neatly ordered expression patterns, this was not at all obvious. What were the implications of these amazing, deep connections for the evolution of animal form? It’s not surprising that Hox genes would be co-opted to explain animal evolution’s greatest mysteries.

It also occurred to me that 1993 is the year of the zootype paper (Slack et al., 1993). Slack et al. reads like a first peek into a brave new world with limitless possibilities. They first note the similarity of Hox gene expression throughout much of the animal kingdom, then propose that this expression pattern (their “zootype”) should be the definition of an animal. After that, they speculate that just as the pattern of Hox genes could define animals, the patterns of genes controlled by Hoxes could define subgroups within animals. Imagine, they say, if we could solve all those tough questions in animal phylogeny by looking at gene expression.

As always, things turned out More Complicated, what with broken and lost Hox clusters and all the other weird shit developmental “master” genes get up to… but it was nice to look back at the bright and simple childhood of my field.

(And my bright and simple childhood. I read The Book of Life in 1998 or 1999, not entirely sure, and in between Backstreet Boys fandom, exchanging several bookfuls of letters with my BFF and making heart-shaped eyes at long-haired guitar-playing teenage boys, I somehow found true, eternal, nerdy love. *nostalgic sigh*)


*Caveat: it’s been years since I last re-read the book, and my copy is currently about 2500 km from me, so the discussion of the Cambrian explosion might be more nuanced than I remember. Also, my copy is the second edition, so I’m only assuming that the Hox gene thing is there in the original.



Carrasco AE et al. (1984) Cloning of an X. laevis gene expressed during early embryogenesis coding for a peptide region homologous to Drosophila homeotic genes. Cell 37:409-414

Duboule D & Dollé P (1989) The structural and functional organization of the murine HOX gene family resembles that of Drosophila homeotic genes. The EMBO Journal 8:1497-1505

Graham A et al. (1989) The murine and Drosophila homeobox gene complexes have common features of organization and expression. Cell 57:367-378

McGinnis W et al. (1984) A conserved DNA sequence in homoeotic genes of the Drosophila Antennapedia and bithorax complexes. Nature 308:428-433

Scott MP & Weiner AJ (1984) Structural relationships among genes that control development: sequence homology between the Antennapedia, Ultrabithorax, and fushi tarazu loci of Drosophila. PNAS 81:4115-4119

Slack JMW et al. (1993) The zootype and the phylotypic stage. Nature 361:490-492

A bunch of cool things

From the weeks during which I failed to check my RSS reader…

1. The coolest ribozyme ever. (In more than one sense.)

I’ve made no secret of my fandom of the RNA world hypothesis, according to which early life forms used RNA both as genetic material and as enzymes, before DNA took over the former role and proteins (mostly) took over the latter. RNA is truly an amazing molecule, capable of doing all kinds of stuff that we traditionally imagined as the job of proteins. However, coaxing it into carrying out the most important function of a primordial RNA genome – copying itself – has proven pretty difficult.

To my knowledge, the previous record holder in the field of RNA copying ribozymes (Wochner et al., 2011) ran out of steam after making RNA strands only half of its own length. (Which is still really impressive compared to its predecessors!) In a recent study, the same team turned to an alternative RNA world hypothesis for inspiration. According to the “icy RNA world” scenario, pockets of cold liquid in ice could have helped stabilise the otherwise pretty easily degraded RNA as well as concentrate and isolate it in a weird inorganic precursor to cells.

Using experimental evolution in an icy setting, they found a variation related to the aforementioned ribozyme that was much quicker and generally much better at copying RNA than its ancestors. Engineering a few previously known performance-enhancing mutations into this molecule finally gave a ribozyme that could copy an RNA molecule longer than itself! It still wouldn’t be able to self-replicate, since this particular guy can only copy sequences with certain properties it doesn’t have itself, but we’ve got the necessary endurance now. Only two words can properly describe how amazing that is. Holy. Shit. :-O


Attwater J et al. (2013) In-ice evolution of RNA polymerase ribozyme activity. Nature Chemistry, published online 20/10/2013, doi: 10.1038/nchem.1781

Wochner A et al. (2011) Ribozyme-catalyzed transcription of an active ribozyme. Science 332:209-212


2. Cambrian explosion: evolution on steroids.

This one’s for those people who say there is nothing special about evolution during the Cambrian – and also for those who say it was too special. (Creationists, I’m looking at you.) It is also very much for me, because Cambrian! (How did I not spot this paper before? Theoretically, it came out before I stopped checking RSS…)

Lee et al. (2013) used phylogenetic trees of living arthropods to estimate how fast they evolved at different points in their history. They looked at both morphology and genomes, because the two can behave very differently. It’s basically a molecular clock study, and I’m still not sure I trust molecular clocks, but let’s just see what it says and leave lengthy ruminations about its validity to my dark and lonely hours 🙂

They used living arthropods because, obviously, you can’t look at genome evolution in fossils, but the timing of branching events in the tree was calibrated with fossils. With several different methods, they inferred evolutionary trees telling them how much change probably happened during different periods in arthropod history. They tweaked things like the estimated time of origin of arthropods, or details of the phylogeny, but always got similar results.

On average, arthropod genomes, development and anatomy evolved several times faster during the Cambrian than at any later point in time. Including the aftermath of the biggest mass extinctions. Mind you, not faster than modern animals can evolve under strong selection – they just kept up those rates for longer, and everyone did it.

(I’m jumping up and down a little, and at the same time I feel like there must be something wrong with this study, the damned thing is too good to be true. And I’d still prefer to see evolutionary rates measured on actual fossils, but there’s no way on earth the fossil record of any animal group is going to be good enough for that sort of thing. Conflicted much?)


Lee MSY et al. (2013) Rates of phenotypic and genomic evolution during the Cambrian explosion. Current Biology 23:1889-1895


3. Chitons to sausages

Aplacophorans are probably not what you think of when someone mentions molluscs. They are worm-like and shell-less, although they do have tiny mineralised scales or spines. Although they look like one might imagine an ancestral mollusc before the invention of shells, transitional fossils and molecular phylogenies have linked them to chitons, which have a more conventional “sluggy” body plan with a wide foot suitable for crawling and an armoured back with seven shell plates.

Scherholz et al. (2013) compared the musculature of a living aplacophoran to that of a chiton and found it to support the idea that aplacophorans are simplified from a chiton-like ancestor rather than simple from the start. As adults, aplacophorans and chitons are very different – chitons have a much more complex set of muscles that includes muscles associated with their shell plates. However, the missing muscles appear to be present in baby aplacophorans, who only lose them when they metamorphose. (As a caveat, this study only focused on one group of aplacophorans, and it’s not entirely certain whether the two main groups of these creatures should even be together.)


Scherholz M et al. (2013) Aplacophoran molluscs evolved from ancestors with polyplacophoran-like features. Current Biology in press, available online 17/10/2013, doi: 10.1016/j.cub.2013.08.056


4. Does adaptation constrain mammalian spines?

Mammals are pretty rigid when it comes to the differentiation of the vertebral column. We nearly all have seven neck vertebrae, for example. This kind of conservatism is surprising when you look at other vertebrates – which include not only fairly moderate groups like birds with their variable necks, but also extremists like snakes with their lack of legs and practically body-long ribcages. Mammalian necks are evolutionarily constrained, and have been that way for a long time.

Emily Buchholz proposes an interesting explanation with links to previous hypotheses. Mammals not only differ from other vertebrates in the less variable numbers of vertebrae in various body regions; these regions are also more differentiated. For example, mammals are the only vertebrates that lack ribs in the lower back. In Buchholz’s view, this kind of increased differentiation contributes to adaptation but costs flexibility.

Her favourite example is the muscular diaphragm unique to mammals. This helps mammals breathe while they move, and also makes breathing more powerful, which is nice for active, warm-blooded creatures that use a lot of oxygen. However, it also puts constraints on further changes. Importantly, Buccholz argues that these constraints don’t all have to work in the same way.

For example, the constraint on the neck may arise because muscle cells in the diaphragm come from the same place as muscle cells associated with specific neck vertebrae. Moving the forelimbs relative to the spine, i.e. changing the number of neck vertebrae, would mess up their migration to the right place, and we’d end up with equally messed up diaphragms.

A second possible constraint has less to do with developmental mishaps and more to do with plain old functionality. If you moved the pelvis forward, you may not screw with the development of other bits, but you’d squeeze the space behind the diaphragm, which you kind of need for your guts, especially when you’re breathing in using your lovely diaphragm.


Buccholz E (2013) Crossing the frontier: a hypothesis for the origins of meristic constraint in mammalian axial patterning. Zoology in press, available online 28/10/2013, doi: 10.1016/j.zool.2013.09.001


And… I think that approximately covers today’s squee moments 🙂

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

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

Ediacaran Underground

As you may have guessed from my blog title, I’m fascinated by the early history of animals. Part of the problem with this early history is that its fossil record is extremely sketchy, extremely difficult to interpret, or both. One of the things that marks the diversification of animals late in the Ediacaran (the last period of the Precambrian) and even more during the Cambrian explosion, is the appearance of burrows and other trace fossils. Marks on the seafloor don’t have to be made by what we usually think of as “complex” animals, though. Burrowing sea anemones are well known, and even single-celled creatures can plough a track in the sediment. That makes things rather complicated when you are looking for the first signs of complex bilaterian animals in the rocks.

Pecoits et al. (2012) are convinced that the trace fossils they found in Uruguay are such a sign, perhaps indeed the oldest. The gently meandering little burrows they report in Science are shaped much like the burrows made by some modern molluscs and annelid worms, possessing features that are hard to explain with a rolling protist or a simple animal. Among other things, they have minute indentations in their walls that may indicate the places where leg-like body parts pushed against the sediment as the animal pulled itself along.

The mysterious burrowers’ path was relatively simple, meandering in broad sine waves that may preserve the unknown creature’s search for food. Burrows often cross, suggesting that their makers made no effort to avoid each other. However, they sometimes disappear and reappear a few millimetres later, as if the animal made a detour upwards or downwards. The few abrupt turns, combined with the width of the burrows, indicate that the creature who left these traces was small, less than a centimetre long.

These burrows – if they are indeed that – are somewhere between 585-600 million years old, at least 30 million years older than the oldest uncontested bilaterians. My question, though, is are they? Bilaterian burrows, I mean. It’s a good thing I double-checked about trace-making protists, since it turns out that the protists in question leave tracks that have supposedly bilaterian characteristics, like consisting of two ruts on either side of a central ridge (Matz et al., 2008). This is one of the similarities the new paper draws between modern bilaterian burrows and their Precambrian precursors! (The weirdest thing is they cite Matz et al. but kind of dismiss the eerily bilaterian character of protist traces…)

Pecoits et al. (2012) do take some time to argue against a protist or non-bilaterian origin of the burrows. There are the little indentations that may have come from something like a worm’s parapodia but are perhaps more difficult to reconcile with a simple rolling ball of cytoplasm. There are also the disappearances and reappearances that indicate the creature moving up and down levels. The authors also argue that the burrows are definitely burrows – i.e. actually under the sediment surface -, though I’m not sure this follows from their evidence.

Then again, they’re the experts here, I’m just a geologically challenged biologist looking at pictures of grooves in rocks… The disappearance-reappearance thing does seem to imply that whatever left these fossils could burrow. (Unless it suddenly hopped off the bottom and landed nearby? And why can’t protists burrow anyway? We didn’t even know they made fake animal traces until a few years ago… I think I’m beginning to sound silly…)

As far as arguments for a bilaterian trace-maker go, a lot is made of the infillings in the burrows, and of the parts that look like the roof collapsed after the animal moved on, but honestly I can’t see what they are talking about in the photos, so I’ll stay on the safe side and reserve judgement there 🙂

And here I meander off track (terrible pun fully intended)

Aaaaanyway, let’s assume they are right, and there’s a reasonably complex worm behind these burrows.

That would be awesome.

However, it poses some questions. In fact, it poses the same questions my friend Kimberella does. I’ve been ruminating about this since I wound up explaining what we know of the bilaterian ancestor to some random guy on the internetz. Let me pour out the contents of my brain here, and let’s hope they make sense >_>

Kimberella. This creature is at the very least a bilaterian, but probably not too far off from molluscs. Its amazing fossil record includes incontrovertible evidence that it could move around and graze on whatever it ate (microbes, probably) by scraping it off the seafloor. It was covered in a knobby armour – fairly flexible and probably not made of a single peace, but definitely a shell of sorts. That’s one of the things that suggest ties to molluscs. Either way, something that we can identify as a member of a subgroup of bilaterians must postdate the bilaterian common ancestor by a fair bit – all those lineages needed time to split and evolve their recognisable body plans.

Palaeontologists and developmental biologists (Budd and Jensen, 2000; Erwin and Davidson, 2002) made a good case in arguing that the last common ancestor of bilaterians must have been small and simple. We know this creature must have predated Kimberella by some time – and this is where we run into problems. One of the strongest arguments for a small and simple bilaterian ancestor is the paucity of Precambrian trace fossils. Large and complex bilaterians make a big mess of seafloor sediment. They dig into it, they walk over it, they churn it up and eat it and spit it out. Nonetheless, the Precambrian is full of virtually undisturbed microbial mats, an unexploited bonanza for any bilaterian with the means to graze. So the conclusion is that large, complex bilaterians must have been rare or non-existent. But, Kimberella? Burrows of a large-and-complex bilaterian* that predate Kimberella by 30 million years?

Something odd is going on here.

I suppose the question could be put as: if these creatures were around in the late Precambrian, why weren’t there more of them? (And where are the bodies?) Why didn’t they swarm out and eat all the microbial mats that made the preservation of many Ediacaran fossils possible (Narbonne, 2005)? Kimberella was doing its best to graze them off the face of the earth, yet this same type of preservation is common even in the formations everyone’s favourite proto-mollusc comes from.

Too little oxygen? But Kimberella is large, relatively compact and partly covered in armour. It’s the sort of creature that we’d expect to have a specialised respiratory system even in an oxygen-rich modern sea, so at least one animal clearly solved this problem…

I suppose it all comes back to what caused the Cambrian explosion, which is a tough question. (Marshall [2006] is a pretty nice review if memory serves.) If we figure out why molluscs and worms and other bilaterians didn’t take over the oceans long before the Cambrian, we’ll have figured out why they did so in the Cambrian.

I’m not sure that did make sense in the end, but I’m glad I could get it off my chest 😀


*A centimetre may not sound very large, but a pretty big percentage of the animal kingdom comes nowhere near it in size.



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

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

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

Matz MV et al. (2008) Giant deep-sea protist produces bilaterian-like traces. Current Biology 18:1849-1854

Narbonne GM (2005) The Ediacara biota: Neoproterozoic origin of animals and their ecosystems. Annual Review of  Earth and Planetary Sciences  33:421-442

Pecoits E et al. (2012) Bilaterian burrows and grazing behavior at >585 million years ago. Science 336:1693-1696

News bites

Just quickly before I completely forget about these…

(1) Common ancestry of segmentation: back-and-forth-and-back-and-forth

Seaver EC et al.(2012) Expression of the pair-rule gene homologs runt, Pax3/7, even-skipped-1 and even-skipped-2 during larval and juvenile development of the polychaete annelid Capitella teleta does not support a role in segmentation. EvoDevo 3:8

I’ve made throwaway mentions of segmentation before. The conundrum about segmentation is whether (or rather, to what extent) it is homologous in the three “eusegmented” phyla, arthropods, annelids and chordates. It arises because all three phyla are separated from the others by many lineages that aren’t usually considered segmented – yet the three share some tantalising similarities. People have been trying to solve the question by comparing the genetic mechanisms generating the segments in each group, with mixed results. One of the papers in my previous news bite post was about the similarity of segmentation in arthropods and vertebrates. Now, here’s one for the differences between arthropods and the wormies. (You can’t say I’m not fair :-P) The genes listed in the study’s title were originally described in the fruit fly Drosophila melanogaster, one of the best studied animals in developmental biology (and, like, every other area of biology). There, they have an interesting role in that each of them helps define every other body segment. IIRC, Pax3/7 (known in flies as paired) and even-skipped are for even-numbered segments, runt is for the odd ones. Now, segmentation in Drosophila is (to put it mildly) fucking weird, but if memory serves, several of these pair-rule genes have been confirmed to play similar roles in less eccentric arthropods. Elaine Seaver and colleagues looked at their expression in their favourite worm (this guy. Seaver’s group obviously didn’t pick it for its beauty :-P), and they found that they were active in… nothing resembling a two-segment pattern. Or anything segment-related. The more genetic studies come out, the more complicated the whole segmentation issue is looking…

(2) Someone found the cause of the Cambrian explosion. (Again.)

Peters SE & Gaines RR (2012) Formation of the ‘Great Unconformity’ as a trigger for the Cambrian explosion. Nature 484:363-366

The Cambrian explosion is probably not what you think it is (no, all animal phyla didn’t just suddenly pop into existence fully formed ;)). Nevertheless, the (relatively) quick rise of animals – particularly animals with hard parts – beginning in the Early Cambrian is still odd enough to fascinate generations of palaeontologists, evolutionary biologists and geologists. The list of proposed causes is pretty long by this point (and believe me, I really really would like to go into them once… but, uh. Huge, dauntingly huge topic). Explanations range from denying the need for an explanation through pinning it on oxygen levels, ice ages, developmental genetics, predation, biomineralisation, even the evolution of eyes, and, working from memory, I probably left some more out of that list. Peters and Gaines’ preferred explanation seems to be geological and ecological: they suggest that a combination of lots of erosion/weathering on land, and a subsequent rise in sea levels, led to large new shallow seas that were chock full of dissolved minerals. New habitats to conquer + widely available minerals = an explosion of new animals with mineralised hard parts. This study is a nice two-in-one: it purports to explain not only the Cambrian explosion, but also the conspicuous gap in the geological record that separates Cambrian from Precambrian rocks in many places.

Jean-Bernard Caron likes molluscs!

A while back, I discussed the interpretation of the enigmatic Cambrian creature Nectocaris on this space. I just discovered that the same guy (or, well, one of the guys) who described the new Nectocaris fossils as the remains of a primitive cephalopod had also been part of a publication “molluscifying” another enigmatic Cambrian creature. In this somewhat earlier case, Caron et al. (2006) interpret Odontogriphus as a soft-bodied primitive mollusc. Something of a grand-uncle to everything molluscan that lives today. (Unlike Nectocaris, Odontogriphus did, apparently, have a radula.)

Needless to say, this interpretation was immediately contested by another Cambrian expert, Nick Butterfield (Butterfield, 2006). The radula of Odontogriphus (and of the more popular “spiny slug” Wiwaxia) aren’t necessarily true radulae, the serial gills of Odontogriphus need not be the specific kind of gills that molluscs have, etc. (This then triggered a response from Team Mollusc [Caron et al., 2007], but I digress :))

I’m beginning to see a pattern here, something much broader than J-B Caron vs. everyone else. It basically reminds me of the contrast the whole of Wonderful Life (Gould, 1991) was built on. To those who haven’t read the book, one of the central themes of Wonderful Life is the (re-)interpretation of Burgess Shale fossils. Initially, the fossils were all shoehorned into already known groups. Decades later, palaeontologists began to examine them more closely, and found that few of them truly fit into those groups. Out of these surprises grew Stephen Jay Gould’s brave new Cambrian world, the festival of freaks that later dwindled to the pathetic little remnant of its full diversity that populates today’s seas. (We’ll leave the discussion of how right or wrong either view is for another time ;))

Another parallel that comes to mind is the extreme range of interpretations of the earlier Ediacaran organisms, which researchers have flagged as everything from early members of living animal groups to a totally new form of life.

Also, somewhat, the lumper/splitter division that seems to exists in vertebrate palaeontology. There are the “lumpers” who want to group everything vaguely similar into the same taxon, and there are those that want to split everything vaguely unique into its own group. (It should go without saying, but there are also opinions in between. I don’t want you to come away thinking that palaeontology and taxonomy are just armed camps of lumpers and splitters shouting obscenities at each other across a barricade ;))

I get the impression that hardcore lumpers tend to consistently be lumpers and hardcore splitters tend to remain splitters.

Are there just some people who want to connect every new observation to something we’ve already seen? Are there just people with a natural tendency to emphasise the uniqueness of new observations? Or prefer to take the middle ground, as the case may be? Why? And more generally, what makes scientists pick one side – or refuse to pick sides – in controversial issues?



Butterfield NJ (2006) Hooking some stem-group “worms”: fossil lophotrochozoans in the Burgess Shale. BioEssays 28:1161-1166

Caron J et al. (2006) A soft-bodied mollusc with radula from the Middle Cambrian Burgess Shale. Nature 442:159-163

Caron J et al. (2007) Reply to Butterfield on stem-group “worms”: fossil lophotrochozoans in the Burgess Shale. BioEssays 29:200-202

Gould SJ (1991) Wonderful Life. Penguin.

Mazurek D and Zatoń M (2011) Is Nectocaris pteryx a cephalopod? Lethaia 44:2-4

Unravelling the Kraken

Nectocaris could be seen as an embodiment of the Weirdness of Cambrian life. It is (or originally was) pretty much a symbol of the Cambrian explosion as Stephen Jay Gould saw it – a festival of brand new, strange body plans that didn’t really belong with anything alive today. Gould’s is a fairly radical interpretation of the Cambrian, and I don’t think most experts share it, but that’s a discussion probably worth a whole book. This post is about Nectocaris alone.

Why did I say that Nectocaris was the embodiment of Cambrian Weirdness? It’s a really obscure creature, and other, more well-known Cambrian animals like Anomalocaris are strange enough for our icon-seeking purposes. Well, yes, but outlandish as it is, Anomalocaris makes sense. For a long time, Nectocaris didn’t.

One more Cambrian puzzle

Until very recently, only a single specimen of Nectocaris was known, and virtually no literature existed on it. What little information seeped out into public perception painted a truly baffling picture. If you believe Gould, this creature was a mongrel of creation that seemed to have the head of an armoured crustacean on the long, finned body of a chordate.

The old Nectocaris by Ghedoghedo, Wikimedia Commons

I have to say something about the family tree of animals here to explain why an animal like that is pretty much impossible unless everything we know about evolution is wrong. Animals are generally classified in 30+ different phyla, e.g. molluscs, arthropods and chordates (Chordata is our own phylum, which we share with other vertebrates, as well as sea squirts and lancelets). Phyla fall into even higher-level groups, whose more or less accepted relationships are summarised on the diagram below:

An outline of animal phylogeny, with examples of each lineage. Groups written in italic are phyla, the rest include more than one phylum. The diagram is my own, but the pictures were all taken from Wikimedia Commons. If you actually care what all the examples are, I have a list at the end of this post.

(Sometimes, biologists seem to go out of their way to make their terminology as arcane as possible. With monsters like “Lophotrochozoa”, it’s no wonder taxonomy isn’t sexy!)

Crustaceans (which are arthropods, which are ecdysozoans) and chordates (which are deuterostomes) are on completely different branches of the tree. Their last common ancestor would have shared some general features with both – but it wouldn’t have had any specific characteristics of arthropods or chordates. If an animal had both arthropod and chordate characteristics, it would violate evolution worse than a Precambrian bunny. Or, alternatively, the resemblance to arthropods, chordates or both would have to be the result of convergent evolution.

As it happens, it was neither.

The original specimen of Nectocaris isn’t that well-preserved. It’s obviously very hard to tell from it what the animal resembled in life. Simon Conway Morris, who described the fossil (Conway Morris, 1976), couldn’t really place it, though he apparently toyed with an arthropod identity*. Simonetta (1988) argued it was a chordate, interpreting what others saw as a “carapace” as the wall of the gill cavity of a primitive chordate. Then, with the discovery of good fossils of a seemingly related animal (Chen et al., 2005), another possibility arose that involved neither arthropods nor chordates – nor impossible crosses between distant lineages. Maybe Nectocaris was a secret lophotrochozoan all along?

A few years later, Smith and Caron (2010) argued that a humongous number of new Nectocaris specimens confirm the last idea. According to them, the animal (along with Chen and colleagues’ Vetustovermis) was not only a lophotrochozoan, but a relative of cephalopods – a bona fide mollusc. From the new fossils, it was obvious that the original specimen was twisted and distorted. What seemed like the vertical tail of a chordate was actually flattened horizontally, with fins on its sides, like the body of a squid. The “vertical” stripes that Simonetta (1988) interpreted as the characteristic muscle blocks of a chordate might have been gill structures, the “fin rays” fibres of connective tissue. The head sported no carapace, but there were two long, flexible tentacles. The big, stalked eyes were not faceted like those of many arthropods, but appeared to be camera eyes like those of cephalopods (and ourselves). Smith and Caron also saw a large floppy structure attached to the underside of the head, which they thought resembled the funnel of cephalopods.

The new Nectocaris by Citron, Wikimedia Commons

But despite more than ninety beautiful specimens, Nectocaris hasn’t given up its stubborn refusal to fall into place. The things that struck me as suspicious in Smith and Caron’s description are some of the same things Polish palaeontologists Dawid Mazurek and Michał Zatoń (2011) found wanting. Most importantly, Nectocaris shows no trace of either the vicious beaks of cephalopods proper (formidable-looking example halfway down this page), or the trademark feeding organ of molluscs, the radula.

You could say that these organs were just not preserved. After all, fossils are never quite complete; scavengers, decay and the vagaries of geological history see to that. That would sound reasonable, except that radulae and beaks are quite durable. One of the first things anyone learns about fossilisation is that hard parts are preserved much more easily than soft parts; beaks, bones and shells don’t rot rapidly like skin and flesh do. But soft tissue is all that remains of Nectocaris, in all ninety-two known specimens. Chances are it never had a radula. The “funnel” is also suspect, Mazurek and Zatoń point out, since its shape is completely wrong for what cephalopod funnels do (squirt water for jet propulsion). Without a funnel, all that’s really left of Nectocaris’s “molluscness” is a superficial resemblance to a flattened squid. Fins and tentacles are hardly defining characteristics of any one group of animals. (Here’s another lophotrochozoan with some lovely tentacles. Don’t click if freakish-looking worms give you bad dreams ;))

So, what on earth IS Nectocaris?

Mazurek and Zatoń (2011) very tentatively go back to the arthropod hypothesis, comparing the creature to anomalocaridids, which are close relatives of true arthropods (Budd and Telford, 2009). But to me, the resemblance to Anomalocaris is as superficial – if not more – as the similarity to cephalopods. Just as fins on the side don’t make Nectocaris a cephalopod, they don’t make it an anomalocaridid either. The slim, supple tentacles are nothing like the sturdy, jointed, clawed, hardened head appendages of Anomalocaris and its kin. While Nectocaris has no molluscan radula, it also lacks the unique pineapple-slice mouth of an anomalocaridid.

Much as it pains me, I still don’t think we know what Nectocaris is. I think the mollusc people and Chen et al. (2005) were on to something. By its general appearance, the creature seems more lophotrochozoan than anything else. Maybe it was a stem mollusc, not quite a mollusc but related, just like Anomalocaris was not quite an arthropod. Or maybe it was related to another lophotrochozoan phylum, say, flatworms, or not particularly close to any living phylum at all.

Until there are even better fossils, we can’t know – and I think that’s the take-home message of this post (insofar as it has one). The problem with fossils is that you can have literally thousands of them, and be no closer to the truth (Shu et al., 2003 and the responses to it are a case in point). To move beyond reasonable speculation, you need clear details of diagnostic traits – those that actually tell you where a creature belongs. In soft-bodied creatures, such details not only decay, but they may decay in a downright misleading way (Sansom et al., 2010). Vertebrate palaeontologists have it easy with their bones and teeth.

*Alas, I don’t have access to that paper, so I’ll have to take Simonetta’s and others’ word on it.



Budd GE and Telford MJ (2009) The origin and evolution of arthropods. Nature 457:812-817

Chen J-Y et al. (2005) An Early Cambrian problematic fossil: Vetustovermis and its possible affinities. Proceedings of the Royal Society B 272:2003-2007

Conway Morris S (1976) Nectocaris pteryx, a new organism from the Middle Cambrian Burgess Shale of British Columbia. Neues Jahrbuch für Geologie und Paläontologie 12:705-713

Gould SJ (1991) Wonderful Life. Penguin.

Mazurek D and Zatoń M (2011) Is Nectocaris pteryx a cephalopod? Lethaia 44:2-4

Sansom RS et al. (2010) Non-random decay of chordate characters causes bias in fossil interpretation. Nature 463:797-800

Shu D-G et al. (2003) A new species of yunnanozoan with implications for deuterostome evolution. Science 299:1380-1384

Simonetta AM (1988) Is Nectocaris pteryx a chordate? Italian Journal of Zoology 55:63-68

Smith MR and Caron J-B (2010) Primitive soft-bodied cephalopods from the Cambrian. Nature 465:469-472

List of animals pictured with the phylogeny:

Sponges: ??? Ctenophores: sea walnut (Mnemiopsis). Placozoans: Trichoplax (I didn’t have much choice there – that insignificant blob is the only known placozoan). Cnidarians: sea nettle jellyfish (Chrysaora) and beadlet sea anemone (Actinia). Deuterostomes: acorn worm (Balanoglossus), a hemichordate; common starfish (Asterias), an echinoderm; and poison dart frog (Phyllobates), a chordate. Lophotrochozoans: garden snail (Helix), a mollusc; serpulid tube worm (Protula), a segmented worm; and freshwater planarian (Dugesia), a flatworm. Lophotrochozoa is actually the largest of the three bilaterian “superphyla”, but I didn’t have space to do its diversity justice. Ecdysozoans: Trichinella, a nematode; Heliconius butterfly, an arthropod; and a penis worm (Priapulus).