Some funky bugs and the novelty of novelty

These must be some of the craziest-looking animals I’ve ever seen.

An assortment of treehoppers (family Membracidae), from Prud'homme et al. (2011)

(Yes, they are actually bugs, as in they belong to order Hemiptera)

Apparently, those extravagant shapes are all due to one special body part called the helmet – an outgrowth of the first thoracic segment of these insects. (Here‘s a little reminder of insect anatomy.) It only occurs in treehoppers, according to Prud’homme et al. (2011). I confess, I know very little about insects in general, and nothing about treehoppers in particular, but talk of evolutionary novelties always gives me a little kick.

[NOTE: I won’t define “novelty” exactly. You can probably figure out what it means, and it’s one of those funny concepts that defies an easy definition. Which is kind of the point of this post, though I didn’t originally intend it to come out that way.]

Evolutionary novelty, at least in complex, multicellular organisms like animals, is usually thought to come from tinkering more than “true” innovation. This is thought to hold on all levels; new genes are often modified versions of old genes, new cell types originate from old cell types, and new body parts are built on old body parts. If you think about it, this makes perfect sense: the old parts are already there, doing jobs that can be used as a starting point, whereas sticking a mutation in a piece of DNA that doesn’t encode anything and stumbling on a useful new gene is not exactly the likeliest event in evolution.

[ASIDE: Whole new body parts practically have to come from old parts on some level – the probability of evolution assembling a complex organ entirely from scratch has many times more zeroes after the decimal point than the probability of accidentally making a new gene. The question is how much of the new part is new. Is it built almost completely from an old structure, such as a whole arm – individual bones, muscles and everything – being modified into a wing, or does it only borrow basic building blocks and put them together in a completely new way?]

The outlandish helmets of treehoppers (sort of) uphold the prevailing view. Prud’homme et al. (2011) tell us that this has been a matter of some controversy – most held that they were “true” novelties that were not homologous to any other body part, but there were clues that there’s more to the story than that. And, indeed.

The first hints were anatomical. Helmets don’t simply grow out of the animal’s back – they are attached by a joint. Above that, they share a few other details, including their tissue structure and their veins, with the appendages almost all insects bear on their other thoracic segments: wings. What’s more, although the mature helmet is a single structure, it develops from two precursors that eventually fuse together. Two wings, two helmet primordia, you get the picture.

Prud’homme et al.‘s investigation involved more than dismantling the thoraxes of baby treehoppers. Homologous structures often share a common genetic underpinning, so they checked the expression of some “wingy” genes (or, to be precise, their protein products) to see just how deep the similarity between helmets and wings extended. The first of these, Nubbin, is wing-specific in better-studied insects. As expected if helmets are homologous to wings, the developing helmet was chock full of Nubbin. The two other genes they analysed, Distal-less (Dll) and homothorax (hth), are more generally expressed in insect appendages (wings, legs and antennae), defining their different regions from base (hth) to tip (Dll). They showed the same expression pattern in the helmet – which doesn’t necessarily mean that helmets are modified wings, but it does suggest they are based on some kind of appendage. And, given what appendages the other thoracic segments bear in the same position…

[NOTE: Well, I don’t know much about hth, but Dll is a bit problematic in this respect. It’s not just an “appendage gene” in insects, but also in a wide variety of other animals. Were it not for Dll expression, no one would suggest homology between, say, the tube feet of a starfish and the legs of a fly (Panganiban et al., 1997) – it’s pretty likely that Dll was originally more of an “anything that sticks out of the body” gene than an “appendage”, never mind a “wing”, gene proper. Dll/Dlx genes also do other stuff, like making neurons migrate in vertebrate brains (Anderson et al., 1997). So Dll expression alone doesn’t mean something is an appendage, let alone a specific type of appendage. Luckily, it’s not alone here. Incidentally, this is lesson number one of comparative/evolutionary developmental genetics. When the question is homology of a structure or process, always look at combinations of genes.]

This is not too surprising given the evolutionary history of wings, or what the fossil record was kind enough to preserve for posterity. The first known winged insects (link leads to drawing of Stenodictya lobata in Grimaldi and Engel, 2005) actually had winglets on the first thoracic segment as well, but those were lost before the last common ancestor of living insects. (How that happened in genetic terms, and how it may have been reversed in treehoppers, is also discussed in the paper, but it isn’t directly relevant to the novelty issue) In a way, treehoppers’ “invention” is a giant laugh in the face of Dollo’s Law, which proposes that complex features don’t re-evolve once they are lost (I kind of touched on this “law” here).

Nevertheless, helmets look nothing like wings and function nothing like wings. (To be fair, they look nothing like one another, either.) They are so dissimilar to their proposed evolutionary sisters that apparently their relationship eluded most researchers. How “novel” are they, then? It’s something of a philosophical question. Since, at this level of complexity, literally nothing comes from scratch, at what point do we stop calling something “tinkering” and start calling it “true novelty”?

As with most philosophical questions, I don’t think this one has a correct answer. That doesn’t mean these questions are not worth pondering. The way we word things influences the way we think about them. Exactly where (or even if) we draw a line between two fuzzy concepts isn’t important in my opinion. But to be aware that there is a dilemma about that line, and that other people may draw it in different places, is. Effective communication is one of my Big Issues, and being critical of your own thinking is an issue that ought to be Big for anyone doing science. (Or for anyone, full stop.) Thinking about unanswerable questions like this is a great way of exercising those (self-)critical muscles.

(Originally, I just wanted to gush about the excitement of figuring out the origin of novelties, but I managed to turn it into a philosophical treatise. Whoda thunk that? <.< )

References:

Anderson SA et al.(1997) Interneuron migration from basal forebrain to neocortex: dependence on Dlx genes. Science 278:474-476

Grimaldi D and Engel MS (2005) Evolution of the Insects. Cambridge University Press.

Panganiban G et al. (1997) The origin and evolution of animal appendages. PNAS 94:5162-5166

Prud’homme B et al. (2011) Body plan innovation in treehoppers through the evolution of an extra wing-like appendage. Nature 473:83-86

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Bacteria invented multicellularity – then thought better of it

I get content alerts from a whole host of journals, some specialist publications focusing on my field, some more general. The majority of even the former is stuff I couldn’t care less about, and the ratio of interesting to irrelevant from generalist journals like PNAS or Nature is lower still. Nevertheless, sometimes you stumble on a title that isn’t directly related to your main interests, but still makes the whole rummaging through the Pile of Irrelevance worth it.

This was the case with a paper (Schirrmeister et al., 2011) just published in the online, open-access journal BMC Evolutionary Biology. It’s so fresh that they haven’t even formatted it – the full text is only available as a “provisional” pdf where all the figures are dumped at the back of the file, separated from their captions (why they can’t wait with publication until the damned thing is in readable format escapes me).

The study by Schirrmeister and others deals with an unusual group of bacteria. Cyanobacteria are probably still better known as blue-green algae, even though they have nothing to do with anything else we call an alga (well, in truth they have everything to do with algae, but in a rather more interesting way, as we’ll see below). If I had to pick one group of organisms that had the greatest impact on the history of our planet, cyanobacteria would be it. For more than two billion years, they have contributed huge amounts of biomass to the global carbon cycle. They are solely responsible for the oxygen-rich atmosphere of the earth – and, by extension, for most eukaryotic life and all animals. They are among the distinguished group of bacteria that can fix nitrogen – a vital ingredient of DNA and proteins – straight from the air, making it available for other organisms. Without them, the world would be a vastly different place, and we wouldn’t be possible. As Andrew Knoll puts it in his wonderful book Life on a Young Planet (consider this a recommendation ;)): “animals may be evolution’s icing, but bacteria are the cake”.

Cyanobacteria live everywhere there is light, from hot springs to the ocean to puddles to stone walls (as components of lichens). They also live inside the cells of every single eukaryote capable of photosynthesis: plants, red and green algae, brown algae, diatoms, dinoflagellates, euglenids (and any others I forgot to mention). The chloroplast is a pared down cyanobacterium – a symbiont that has lost most of its genes, but the ones that remain, together with its structure, still tell of its ancestry. Plants owe all their green splendour to these tiny buggers.

Cyanobacteria are not just immensely important, they are also quite unusual among prokaryotes. As the post title implies, they invented multicellularity. Multicellular cyanobacteria display a range of complexity. Some of them are just chains of identical cells. Others, though, have up to three different cell types. Heterocysts, thick-walled cells that ensure the oxygen-free environment that these bacteria require for nitrogen fixation, sit at regular intervals among “normal” cells, and when necessary, the “normal” cells can also differentiate into hardy resting cells that can survive bad times. The most complex cyanobacteria not only have filaments with different cell types, but also introduce branching into these filaments. This is the most complex prokaryotes get.

Filaments of an unbranched, differentiated cyanobacterium. The oversized heterocysts are quite obvious in some of them. Image by Kristian Peters, from Wikimedia Commons.

The new study raises an interesting possibility: that at least the simple form of multicellularity (i.e. undifferentiated filaments) occurred very early in the history of cyanobacteria. According to Schirrmeister et al., the vast majority of modern cyanobacteria descend from multicellular ancestors, even though a great many of them are single-celled today. Even more intriguingly, they find a lineage that might have re-evolved multicellularity after losing it. I don’t pretend to fully understand the methods used to come to these conclusions, but I have to say that it’s built on an impressive dataset – the group selected 58 cyanobacterial species for more detailed study from an original phylogenetic tree built from over a thousand taxa. They then constructed trees of this smaller dataset using two separate methods, and finally, tried to reconstruct the ancestral states at various points in those trees using several different statistical methods again. The analyses all agree: multicellularity is a very ancient trait in cyanobacteria, and it was lost left and right during their three-billion-year history.

These findings go against our ingrained view of evolution as an inexorable march towards increasing complexity. We, mammals, are among the (if not the) most complex organisms the earth has ever produced. We are assemblages of some 200 distinct cell types organised into a finely regulated machinery of a multitude of specialised organs. When we look at the large-scale patterns in the fossil record, we also see that this complexity has accumulated from much simpler beginnings over the aeons. We can be forgiven for thinking, in a characteristically self-centred way, that complexity is where evolution is intrinsically headed. But every now and then, nature reminds us that “more complicated” does not necessarily equal “favoured”.

Parasites are probably best known for their tendency to become simplified – after all, if you are bathed in your host’s digestion products all the time, why waste your energy on growing your own gut? However, simplification is abundant in organisms that make their own living, too. For example, two entire phyla of distinctly unsegmented, baglike worms – spoon worms and peanut worms -, likely came from more sophisticated segmented worms (Struck et al., 2007). Now, cyanobacteria join the club, and new questions surge in their wake. Why did they go back to unicellularity? How difficult is it for them to become multicellular? Such questions, of course, can be asked about any complex trait that followed a similar evolutionary trajectory.

Most intriguingly, these tiny microbes seem to violate another “law” of evolution, known as Dollo’s law: that once lost in a lineage, a complex trait won’t reappear. If the inferences of Schirrmeister et al. are correct, then either simple multicellularity isn’t such a big deal at all for these bacteria, or Dollo’s law isn’t as much of a law as we thought.

(Actually, the latter is probably the case however the history of cyanobacteria turns out. Dollo’s law has been questioned by others, and it was recently dealt a spectacular blow by a frog that almost certainly re-evolved teeth in its lower jaw (Wiens, 2011) after at least 200 million years of not having them.)

Evolution is a fascinating story. As the example of cyanobacterial multicellularity suggests, it can also be as complex as any good novel. I for one think this makes for a much more interesting and fulfilling narrative than simplistic listings of “what’s new” through the ages.

– – –

References:

Schirrmeister BE, Antonelli A and Bagheri HC (2011) The origin of multicellularity in cyanobacteria. BMC Evol Biol 11:45

Struck TH et al. (2007) Annelid phylogeny and the status of Sipuncula and Echiura. BMC Evol Biol 7:57

Wiens JJ (2011) Re-evolution of lost mandibular teeth in frogs after more than 200 million years, and re-evaluation of Dollo’s Law. Evolution advance online publication, DOI: 10.1111/j.1558-5646.2011.01221.x