Are there laws of evolution?

I’ve just come across a very interesting essay by Eugene Koonin. He asks an intriguing question: does evolution, like physics, have universal mathematical laws?

To answer it, he pulls out some fascinating patterns that keep turning up no matter what organism we look at. For example, genes that are more active tend to evolve more slowly, and the number of genes in gene families follows a power law distribution. He points out that such patterns can emerge out of simple models of the behaviour of genes and genomes. Just like physical laws. (Ha. Take that, you physicists who tell us that biology is not “really” a science!)

Koonin makes an important point using his example laws: we shouldn’t see everything about living things as an adaptation. The “adaptationist” attitude seems to be an old problem in evolutionary biology – he cites Stephen Jay Gould’s complaints about the same issue voiced back in 1979. Evolution includes not just adaptation, but also many historical leftovers and random elements. Sometimes, things just happen because that’s what follows from the physics of the system. Accordingly, Koonin’s example models produce evolution’s observed laws without incorporating any selection.

Well, some of them at least. The gene expression level/evolutionary rate relationship is actually all about selection if you pay attention to the description of the model (or check Drummond and Wilke, 2008, which proposed the model). In this model, the relationship comes about due to the cost of errors in protein synthesis – which can kill cells, so it probably qualifies as a selective pressure…* (That doesn’t make the resulting pattern any less a law, just changes the reason it’s a law.)

Of course, as Koonin reminds the reader, none of this means that selection is not important. It’s just that we should first test whether something is the result of selection before starting to concoct adaptive explanations for it.

All in all, this was a very interesting read, made even better by the fact that PLoS included a reviewer’s comment and Koonin’s response with it. It’s a cool little glimpse under the hood of peer review, and an opportunity to see a different expert viewpoint on the same subject. I think it would be great to see more of that, to be honest.

***

*Incidentally, I wonder if that means that the “law” doesn’t apply to genes that don’t encode proteins, like ribosomal RNA.

***

References

Koonin EV (2011) Are there laws of genome evolution? PLoS Computational Biology 7:e1002173

Drummond DA, Wilke CO (2008) Mistranslation-induced protein misfolding as a dominant constraint on coding-sequence evolution. Cell 134:341-352
Advertisements

300 amino acids of junk?

This is about Hox genes, but not in the way I’d normally write about them. They are the rock stars of evo-devo for a reason, but this post is not about their awesomeness. (See this Pharyngula post for a great introduction to Hox genes.) Generally, I’m more interested in how genes evolve than how they work. However, when I saw this paper in PNAS, I couldn’t help but wonder about function.

I’ll explain. The study by Papadopoulos et al. (2011) is about engineering artificial Hox genes to see how various bits of sequence affect the function of the gene product. Its main focus is the role of a small sequence motif, and the “linker” sequence that connects that motif to the main DNA-binding portion of the protein. This is a schematic of a typical Hox protein sequence, not to scale:

In a typical Hox protein, the homeodomain interacts witht DNA (Hox proteins are transcription factors – they turn genes on and off), while the YPWM motif [2] binds to other proteins [3]. Those other proteins change the preferences of the homeodomain, so they influence which specific genes are switched on or off. All Hox proteins have a homeodomain, and the majority have some variation on the YPWM theme. The yellow parts are more variable.

Now, one thing the aforementioned study did was cut pieces off a particularly well-studied Hox gene called Antennapedia. One of the truncated genes encoded a protein that consisted of just the YPWM motif and homeodomain. This gene appeared to do the same things a normal Antp gene does. It activated the same target genes. Its product interacted with the same proteins. When they switched it on in the wrong places, it turned the antennae of adult flies developing in pupae into legs, and the heads of fly embryos into thoraxes – just like normal Antp.

Just to give you an idea, this is the sequence of the protein in question (copied from Genbank):

MTMSTNNCESMTSYFTNSYMGADMHHGHYPGNGVTDLDAQQMHHYSQNANHQGNMPYPRFPPYDRMPYYN
GQGMDQQQQHQVYSRPDSPSSQVGGVMPQAQTNGQLGVPQQQQQQQQQPSQNQQQQQAQQAPQQLQQQLP
QVTQQVTHPQQQQQQPVVYASCKLQAAVGGLGMVPEGGSPPLVDQMSGHHMNAQMTLPHHMGHPQAQLGY
TDVGVPDVTEVHQNHHNMGMYQQQSGVPPVGAPPQGMMHQGQGPPQMHQGHPGQHTPPSQNPNSQSSGMP
SPLYPWMRSQFGKCQERKRGRQTYTRYQTLELEKEFHFNRYLTRRRRIEIAHALC LTERQIKIWFQNRRMKWKKENKTKGEPGSGGEGDEITPPNSPQ

If I understood them right, the highlighted portion is what the experimenters left of it.

So… if that little segment is enough to perform the duties of the whole thing, why the hell is the rest of the protein there? It seems like a total waste of genome space.

(There is an obvious answer, that is this study didn’t actually prove that the full-length and the reduced versions are totally equivalent. For that, they would have had to engineer flies without their own Antp (which would be some horribly messed up flies), and put this mini-Antp into some of them. If mini-Antp can make an otherwise screwed-up fly completely normal, chances are the original gene doesn’t do anything that mini-Antp can’t do. They didn’t do that experiment, so we can’t be sure that there aren’t differences between the two versions where they didn’t look.

It’s probably just that. It has to be that, right?)

***

Notes

[1] Well, I should say that they normally live in neat clusters. There are animals in which Hox genes have become jumbled within a cluster, torn in two or more clusters or even completely scattered throughout the genome. Nevertheless, on the whole they have a remarkable tendency to stay together and ordered.

[2] YPWM stands for the amino acids tyrosine, proline, tryptophan and methionine, in case you wondered.

[3] Actually, the homeodomain also interacts with other proteins, but DNA binding is regarded as its main function.

Reference

Papadopoulos DK et al. (2011) Functional synthetic Antennapedia genes and the dual roles of YPWM motif and linker size in transcriptional activation and repression. PNAS 108:11959-11964

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.

***

References:

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).