In which a “living fossil’s” genome delights me

I promised myself I wouldn’t go on for thousands and thousands of words about the Lingula genome paper (I’ve got things to do, and there is a LOT of stuff in there), but I had to indulge myself a little bit. Four or five years ago when I was a final year undergrad trying to figure out things about Hox gene evolution, I would have killed for a complete brachiopod genome. Or even a complete brachiopod Hox cluster. A year or two ago, when I was trying to sweat out something resembling a PhD thesis, I would have killed for some information about the genetics of brachiopod shells that amounted to more than tables of amino acid abundances. Too late for my poor dissertations, but a brachiopod genome is finally sequenced! The paper is right here, completely free (Luo et al., 2015). Yay for labs who can afford open-access publishing!

In case you’re not familiar with Lingula, it’s this guy (image from Wikipedia):

In a classic case of looks being deceiving, it’s not a mollusc, although it does look a bit like one except for the weird white stalk sticking out of the back of its shell. Brachiopods, the phylum to which Lingula belongs, are one of those strange groups no one really knows where to place, although nowadays we are pretty sure they are somewhere in the general vicinity of molluscs, annelid worms and their ilk. Unlike bivalve molluscs, whose shell valves are on the left and right sides of the animal, the shells of brachiopods like Lingula have top and bottom valves. Lingula‘s shell is also made of different materials: while bivalve shells contain calcium carbonate deposited into a mesh of chitin and silk-like proteins,* the subgroup of brachiopods Lingula belongs to uses calcium phosphate, the same mineral that dominates our bones, and a lot of collagen (again like bone). But we’ll come back to that in a moment…

One of the reasons the Lingula genome is particularly interesting is that Lingula is a classic “living fossil”. In the Paleobiology Database, there’s even an entry for a Cambrian fossil classified as Lingula, and there are plenty of entries from the next geological period. If the database is to be believed, the genus Lingula has existed for something like 500 million years, which must be some kind of record for an animal.** Is its genome similarly conservative? Or did the DNA hiding under a deceptively conservative shell design evolve as quickly as anyone’s?

In a heroic feat of self-control, I’m not spending all night poring over the paper, but I did give a couple of interesting sections a look. Naturally, the first thing I dug out was the Hox cluster hiding in the rather large supplement. This was the first clue that Lingula‘s genome is definitely “living” and not at all a fossil in any sense of the word. If it were, we’d expect one neat string of Hox genes, all in the order we’re used to from other animals. Instead, what we find is two missing genes, one plucked from the middle of the cluster and tacked onto its “front” end, and two genes totally detached from the rest. It’s not too bad as Hox cluster disintegration goes – six out of nine genes are still neatly ordered – but it certainly doesn’t look like something left over from the dawn of animals.

The bigger clue that caught my eye, though, was this little family tree in Figure 2:

Luo_etal2015-fig2

The red numbers on each branch indicate the number of gene families that expanded or first appeared in that lineage, and the green numbers are the families shrunk or lost. Note that our “living fossil” takes the lead in both. What I find funny is that it’s miles ahead of not only the animals generally considered “conservative” in terms of genome evolution, like the limpet Lottia and the lancelet Branchiostoma, but also the sea squirt (Ciona). Squirts are notorious for having incredibly fast-evolving genomes; then again, most of that notoriety was based on the crazily divergent sequences and often wildly scrambled order of its genes. A genome can be conservative in some ways and highly innovative in others. In fact, many of the genes involved in basic cellular functions are very slow-evolving in Lingula. (Note also: humans are pretty slow-evolving as far as gene content goes. This is not the first study to find that.)

So, Lingula, living fossil? Not so much.

The last bit I looked at was the section about shell genetics. Although it’s generally foolish to expect the shell-forming gene sets of two animals from different phyla to be similar (see my first footnote), if there are similarities, they could potentially go at least two different ways. First, brachiopods might be quite close to molluscs, which is the hypothesis Luo et al.‘s own treebuilding efforts support. Like molluscs, brachiopods also have a specialised mantle that secretes shell material, though having the same name doesn’t mean the two “mantles” actually share a common origin. So who knows, some molluscan shell proteins, or shell regulatory genes, might show up in Lingula, too.

On the other hand, the composition of Lingula’s shell is more similar to our skeletons’. So, since they have to capture the same mineral, could the brachiopods share some of our skeletal proteins? The answer to both questions seems to be “mostly no”.

Molluscan shell matrix proteins, those that are actually built into the structure of the shell, are quite variable even within Mollusca. It’s probably not surprising, then, that most of the relevant genes that are even present in Lingula are not specific to the mantle, and those that are are the kinds of genes that are generally involved in the handling of calcium or the building of the stuff around cells in all kinds of contexts. Some of the regulatory mechanisms might be shared – Luo et al. report that BMP signalling seems to be going on around the edge of the mantle in baby Lingula, and this cellular signalling system is also involved in molluscan shell formation. Then again, a handful of similar signalling systems “are involved” in bloody everything in animal development, so how much we can deduce from this similarity is anyone’s guess.

As for “bone genes” – the ones that are most characteristically tied to bone are missing (disappointingly or reassuringly, take your pick). The SCPP protein family is so far known only from vertebrates, and its various members are involved in the mineralisation of bones and teeth. SCPPs originate from an ancient protein called SPARC, which seems to be generally present wherever collagen is (IIRC, it’s thought to help collagen fibres arrange themselves correctly). Lingula has a gene for SPARC all right, but nothing remotely resembling an SCPP gene.

I mentioned that the shell of Lingula is built largely on collagen, but it turns out that it isn’t “our” kind of collagen. “Collagen” is just a protein with a particular kind of repetitive sequence. Three amino acids (glycine-proline-something else, in case you’re interested) are repeated ad nauseam in the collagen chain, and these repetitive regions let the protein twist into characteristic rope-like fibres that make collagen such a wonderfully tough basis for connective tissue. Aside from the repeats they all share, collagens are a large and diverse bunch. The ones that form most of the organic matrix in bone contain a non-repetitive and rather easily recognised domain at one end, but when Luo et al. analysed the genome and the proteins extracted from the Lingula shell, they found that none of the shell collagens possessed this domain. Instead, most of them had EGF domains, which are pretty widespread in all kinds of extracellular proteins. Based on the genome sequence, Lingula has a whole little cluster of these collagens-with-EGF-domains that probably originated from brachiopod-specific gene duplications.

So, to recap: Lingula is not as conservative as its looks would suggest (never judge a living fossil by its cover, right?) We also finally have actual sequences for lots of its shell proteins, which reveal that when it comes to building shells, Lingula does its own thing. Not much of a surprise, but still, knowing is a damn sight better than thinkin’ it’s probably so. We are scientists here, or what.

I am Very Pleased with this genome. (I just wish it was published five years ago 😛 )

***

Notes:

*This, interestingly, doesn’t seem to be the general case for all molluscs. Jackson et al. (2010) compared the genes building the pearly layer of snail (abalone, to be precise) and bivalve (pearl oyster) shells, and found that the snail showed no sign of the chitin-making enzymes and silk type proteins that were so abundant in its bivalved cousins. It appears that even within molluscs, different groups have found different ways to make often very similar shell structures. However, all molluscs shells regardless of the underlying genetics are predominantly composed of calcium carbonate.

**You often hear about sharks, or crocodiles, or coelacanths, existing “unchanged” for 100 or 200 or whatever million years, but in reality, 200-million-year-old crocodiles aren’t even classified in the same families, let alone the same genera, as any of the living species. Again, the living coelacanth is distinct enough from its relatives in the Cretaceous, when they were last seen, to warrant its own genus in the eyes of taxonomists. I’ve no time to check up on sharks, but I’m willing to bet the situation is similar. Whether Lingula‘s jaw-dropping 500-million-year tenure on earth is a result of taxonomic lumping or the shells genuinely looking that similar, I don’t know. Anyway, rant over.

***

References:

Jackson DJ et al. (2010) Parallel evolution of nacre building gene sets in molluscs. Molecular Biology and Evolution 27:591-608

Luo Y-J et al. (2015) The Lingula genome provides insights into brachiopod evolution and the origin of phosphate biomineralization. Nature Communications 6:8301

Random of the day

Because productivity is too much effort. In my defence, it was paper writing-related curiosity that led me to Wikipedia, where I found this electron microscope image of a broken piece of mother of pearl/nacre by Fabian Heinemann. (In case you wondered, I wanted to check roughly how big nacre tablets were. And no, Wikipedia is not my only source for this ;)) So: this is what mother of pearl looks like when you zoom in a few thousand times.

Nacre is made of little tablets of aragonite stacked on top of one another and separated by sheets of organic matter. The way the tablets scatter light is what gives pearls their pretty, pretty shine.

(I have a thing for electron micrographs of biominerals. Actually, I’m a big fan of close-up images of pretty much anything. It’s like looking into the secret heart of things.)

Fanworm fandom

In all my meanderings so far, I have never talked about my work in more than vague references to my connection to biominerals. Well, today won’t be the day I really start, but I would like to introduce the animals I work with. Because they are beautiful, awesome, and I love them (except when they’re sabotaging my experiments :-P). They are fan worms.

“Fan worm” is a bit of a loose term, and I’m still not entirely sure what group of worms it is/isn’t supposed to apply to. The group of fan worms I’d like to talk about today is family Serpulidae. (Call them “serps”. They won’t mind.)

Serpulidae are, if the latest phylogenetic research is to be believed, a subgroup of another “family”, the Sabellidae or feather duster worms (Kupriyanova and Rouse, 2008). All sabellids are sedentary filter-feeders. They live in tubes, putting a feathery crown of tentacles out into the water to catch their microscopic food. This is the fan in fan worm, and it’s all that most people ever see of these gorgeous creatures. It’s also today’s excuse to post some Nick Hobgood Christmas tree worms from Wikipedia, although their crazy spiralling tentacle crowns are not all that fan-like. (Bottle brush worms? :D)

These guys in the photo are mostly buried in a coral colony, with only their tentacle crowns sticking out.

Ancestrally, sabellid tubes are made of hard particles like sand and shell fragments glued together with mucus secreted by the worm. Serpulids are special in that they make their own hard material – calcium carbonate – instead of picking stuff up from the environment.

Serpulid tubes can have a highly organised structure that betrays sophisticated tube-building mechanisms (Vinn et al., 2008). Incidentally, some of them are pretty awesome if you look close enough. Below are the rather bland-looking tubes of Ditrupa arietina lying on the seafloor (from ten Hove and Kupriyanova [2009]). Then an electron microscope image of the outer tube layer showing the cool jigsaw-like cross sections of the calcareous rods it’s made of (Olev Vinn via Wiki Commons).

tHK2009-d_arietina

The general anatomy of the animal inside the tube is demonstrated quite nicely in the photograph below, from ten Hove and Kupriyanova (2009):

tHK2009-s_vermicularis

This is Serpula vermicularis, the species that gave its name to the family. The head end, obviously, is the one with the tentacles. Below it is a rather elegant thorax wearing a jacket of skin flaps (technically, “thoracic membranes”), with a wide collar folding down over the top. The collar builds the tube: when the worm wants to expand its home, it pokes its head out, wraps its collar over the rim, and deposits a new layer of material from glands under the collar.

The weird funnel-shaped thingy sticking out Serpula‘s head above is called an operculum. It’s another speciality of (most) serpulids, functioning in defence against predators. It’s used to close off the tube, but – at least in my species – it’s also a sacrifice body part that pops off at a predetermined point if you tug or prod it too hard. A bit like a lizard’s tail. (Or a sea cucumber’s guts, because gross examples are always better.) Also like the lizard’s tail, the operculum regrows easily, but unlike lizards, serps can regenerate a perfect new operculum. Some serps, including mine, have upgraded their defences further by reinforcing the operculum with calcium carbonate. A calcified body part that you can make develop on demand. What more can you dream of? 😉

Serpulids are found all over the world. Most of the 300+ species live in the sea, all the way from tidal rock pools to deep sea vents. There are a few that can handle brackish water, and there’s a single species that somehow found its way into freshwater-filled limestone caves along the Adriatic coast. According to Kupriyanova et al. (2009), this little explorer is closely related to the brackish-water species, so serps probably only figured out how to deal with lower salinity once.

They are nowhere near as famous as corals, but a few serpulid species are prolific reef builders. Ficopomatus enigmaticus (one of the brackish serps) can grow in roundish reefs made of generations of worm tubes. Although the individual tubes are only a few cm long, reefs can reach several metres across.

F. enigmaticus is an invasive species. Hitchhiking from their European homeland on boats and spawning wherever they felt happy enough, the worms have spread across the warm, shallow, brackish waters of the world. Below, their reefs are shown polka dotting the Mar Chiquita lagoon over in Argentina (photos: Alejandro Bortolus, in Schwindt et al. [2001]). Note the scale bar!

Schwindt_etal2001-ficopomatus_reefs

F. enigmaticus reefs have a pretty big ecological impact in their new territory. Their filter-feeding makes the water less murky (Bruschetti et al., 2008), which is good for the seafloor community, not so great for the phytoplankton that caused the murkiness. The reefs provide hiding places for native predators, changing the composition of the seafloor community (Schwindt et al., 2001), and they can also serve as resting stops and hunting grounds for birds (Bruschetti et al., 2009).

And finally, let’s talk a bit about serpulid babies, because baby worms are the best. I don’t know about other serps, but my species has very stylish BABY PINK EGGS. The moment you remove an adult worm from its tube, it panic-spawns all over the place. If you mix the pink eggs with the boring white sperm in some seawater, by the next day the dish will be full of tiny, zipping white balls. (At this point you’d better feed them, since unlike some other baby polychaetes, they don’t get a lot of food from mum. In nature, they’d swim off and live in the plankton, hunting tiny algae until they are ready to settle.)

In another day or two, the little balls grow quite a bit and turn into textbook examples of the type of larva known as the trochophore. If you’re good to them and give them enough food, they’ll keep growing like crazy. You can always see whether they’re hungry or not, since they are transparent and the colourful algae they like to eat show through their skin. This one, from McDougall et al. (2006) via Wiki Commons, was clearly well-fed when it fell victim to science:

They look all hairy around the broadest part – those are the cilia they use to swim. They are very good at swimming! Within a couple of weeks, they’ve transformed into a more mature form with three newfangled segments and a lovely pair of eyes, like this other one from the same paper:

They are now sniffing along the bottom, looking for a place to settle. When they find a spot they like, they lie down, secrete a tiny tube (made of just mucus at first), and metamorphose into transparent baby worms complete with an operculum and everything. This is what Pomatoceros lamarckii looks like mid-metamorphosis (again from McDougall et al.):

mcdougall_p_lamarckii_juvenile

At this point, they are a bit ugly, but don’t worry, the ugly wormling stage doesn’t last long. I’ll finish off with one of my own photos what they turn into:

DSCN0613

These are slightly over three weeks old, and they have tiny, iridescent tentacles and minute, transparent opercula. Their now-calcified baby tubes are just a few mm long.

Aren’t they lovely? 😀

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References:

Bruschetti M et al. (2008) Grazing effect of the invasive reef-forming polychaete Ficopomatus enigmaticus (Fauvel) on phytoplankton biomass in a SW Atlantic coastal lagoon. Journal of Experimental Marine Biology and Ecology 354:212-219

Bruschetti M et al. (2009) An invasive intertidal reef-forming polychaete affect habitat use and feeding behavior of migratory and locals birds in a SW Atlantic coastal lagoon. Journal of Experimental Marine Biology and Ecology 375:76-83

Kupriyanova EK & Rouse GW (2008) Yet another example of paraphyly in Annelida: molecular evidence that Sabellidae contains Serpulidae. Molecular Phylogenetics and Evolution 46:1174-1181

Kupriyanova EK et al. (2009) Evolution of the unique freshwater cave-dwelling tube worm Marifugia cavatica (Annelida: Serpulidae). Systematics and Biodiversity 7:389-401

McDougall C et al. (2006) The development of the larval nervous system, musculature and ciliary bands of Pomatoceros lamarckii (Annelida): heterochrony in polychaetes. Frontiers in Zoology 3:16

Schwindt E et al. (2001) Invasion of a reef-builder polychaete: direct and indirect impacts on the native benthic community structure. Biological Invasions 3:137-149

ten Hove HA & Kupriyanova EK (2009) Taxonomy of Serpulidae (Annelida, Polychaeta): The state of affairs. Zootaxa 2036:1-126

Vinn O et al. (2008) Ultrastructure and mineral composition of serpulid tubes (Polychaeta, Annelida). Zoological Journal of the Linnean Society 154:633-650

Ocean acidification is complicated, case in point

I once wrote about the complicated way in which ocean acidification is mostly really bad for marine creatures with calcium carbonate shells/skeletons. Well, today, while reading a book I thought had nothing to do with ocean acidification, I came across a report of one such creature for whom the change is apparently for the better. (I’d expected to find all kinds of interesting information in Embryos in Deep Time, but this was a surprise…)

Dupont et al. (2010) studied common sun stars (above; Bernard Picton, habitas.org.uk), following the larvae right up to metamorphosis under current CO2 and pH values of their home seas, and also under a near-future predicted scenario with higher CO2 concentration and lower sea pH. Surprisingly, the larvae in the “future” tanks survived just as well, grew better, and showed no obvious defects in development or calcification compared to the control group.

The authors speculate that this might be related to the reproductive strategy of these animals. While the larvae of many echinoderms have very little yolk in their eggs and have to feed the moment they look vaguely like an animal, sun star larvae are provided with a lot of yolk that can sustain them until they’re ready to metamorphose. So they don’t have to face the burdens of hunting for food; all their energy can go towards growing, which might make them more resilient to harmful environmental effects.

I’m not sure I buy such a simplistic explanation – first, other echinoderms with a similar developmental strategy suffer quite badly in similar conditions; and second, they only examined one species during the early stage of its life cycle. In fact, the authors point out these exact same caveats. (Plus the creatures not only resisted acidification, they thrived.)

Whatever the mechanism, though, Dupont et al.‘s data show that there is at least one animal for which ocean acidification may be a boon. Considering that this guy happens to be a top predator in its ecosystem, that could have major consequences for said ecosystem.

Also, they are incredibly pretty. Echinoderms rock.

***

Reference

Dupont S et al. (2010) Near future ocean acidification increases growth rate of the lecithotrophic larvae and juveniles of the sea star Crossaster papposus. Journal of Experimental Zoology 314B:382–389

Ocean Soda and the Animals

As far as scientific interests are concerned, I’m not an “environmental” person at all. Somehow, ecology and conservation managed to remain profoundly boring to me despite the fact that my heart breaks every time I think about the havoc we’re wreaking in the biosphere. The same is true for physiology except there’s not even much of an emotional response to that, aside from a sullen disgust accompanying memories of endless lectures about fish kidneys.

After telling you how much I don’t care about ecology and physiology, it probably doesn’t come as a surprise that this post is kind of about both. You see, I study an animal with calcareous hard parts. It just so happens that these days, animals like that may be in trouble. Humans are pumping insane amounts of carbon dioxide in the air at a (geologically speaking) stupid rate, the oceans are swallowing it and slowly turning into a very salty fizzy drink. Calcium carbonate and acid don’t get along.

As it happens, the subject of calcifying critters versus ocean acidification also fits one of my recurring themes, i.e. that things are usually more complicated than you think. In this case, things are certainly much more complicated than I suggested in the previous paragraph. And thus, you shall be treated to a meandering about some of the complications I’ve come across 🙂

Many, many sea creatures have hard parts – shells or skeletons – made of calcium carbonate, the mineral that also makes up limestone and marble. The long list includes stony corals, calcareous sponges, crustaceans, nearly all molluscs, starfish, sea urchins and other echinoderms, a few groups of segmented worms, and even such unlikely suspects as the “soft bodied” acorn worms (Cameron and Bishop, 2012). And then we didn’t even count the algae and assorted single-celled beasties that the food chains of these animals stand on. The bottom line is that calcium carbonate is a damn big ecological deal.

(Below: a selection of marine carbonate users from Nick Hobgood‘s Wikimedia stash. Because Nick Hobgood is amazing.)

Calcium carbonate (chemical formula CaCO3), of course, is made of calcium and carbonate ions. How easy it is for animals to put into a skeleton depends on a variety of factors. In the most trivial sense, it matters how much of the ingredients you give them. Calcium is a standard component of seawater everywhere. Carbonate is also found normally in seawater. Its abundance is in a dynamic equilibrium involving carbon dioxide, carbonate, bicarbonate, carbonic acid and water. I find the chemistry difficult to get my head around, so here’s a figure from Feely et al. (2001) for our collective education:

(The numbers are the concentrations of the various chemical species under pre-industrial atmospheric CO2 levels and doubled CO2 levels, which could easily happen in the not too distant future.)

As far as I understand this system, the problem with CO2 is twofold. First, adding more of it decreases the pH of the water, and all forms of calcium carbonate are much more soluble at lower pH. Second, it decreases the concentration of carbonate ions, which makes them harder to obtain for shell-making purposes. (The guy who wrote this Encyclopedia of Earth article probably understands the whole thing rather better than me, though.)

Because I’m a pedant, I have to note that ocean “acidification” is a bit misleadingly named, because normal seawater is (and will be for the foreseeable future) far from being actually acidic. But the rules still apply – the lower the pH, the more difficult it is to make solid CaCO3.

This seems like a straightforward equation – keep pumping CO2 into the air, and shellfish will soon be shell-less (and thoroughly screwed). However, when you look at the actual reactions of real living creatures to acidification treatments (which Kroeker et al., 2010 summarised the then-existing literature for) – or indeed what happens to said creatures in the wild (as this “historical” study of reef corals by Cooper et al., 2012 did), a slightly more nuanced picture emerges.

First of all, of course organisms aren’t passive and helpless players in this game. Just like we can sweat or shiver to keep our body temperature right, calcifying things can regulate the environment in which their skeletons are manufactured. A study that looked at the chemical environment of the specialised space in which corals build their skeletons found that the pH of the fluid there is always higher than that of the surrounding seawater – corals do their darnedest to keep it where it’s good for them (Venn et al., 2013).

Having a specialised, “insulated” space for mineral deposition is a pretty common thing in the living world. The tiny algae called coccolithophores (who are single-handedly responsible for the White Cliffs of Dover) simply make their characteristic plates (literally “limescales,” hehe) inside their cells. Echinoderm larvae merge cells to create a “spicule factory”. Molluscs deposit their shells into the protected space between a tough organic layer and the soft tissue of the mantle. Et cetera.

On top of that, all organisms have proteins specialised to transport ions through cell membranes. Creatures who build hard parts can use such proteins to actively shuttle the materials they need even when they’re working against physics.

Thus, most mineralising organisms have ways of dealing with environments not necessarily friendly to mineralisation. Some naturally have to handle a wide range of such environments, like shellfish who live in estuaries and experience changes in salinity (and calcium concentration, and pH) with every tide.

As you might expect, different organisms can react very differently to the same challenge, ocean acidification in this case (e.g. Ries et al., 2009). They could be badly affected, they could just not give a damn… or even up their game and increase their calcification rates, as a brittle star was observed to do (Wood et al., 2008). That sort of compensation appears costly in other areas, though – Wood et al’s brittle stars suffered muscle loss, for example. It’s also worth noting that even closely related species can be affected in pretty different ways. In a study of two oyster species of the same genus and similar natural habitats, the larvae of one just shrugged off a bit of acidification, whereas those of the other struggled to build their baby shells under identical conditions (Miller et al., 2009).

Overall, ocean acidification is going to be bad for most creatures who rely on calcified hard parts, but how bad and what kind of bad will vary greatly if the above examples are anything to go by.

However, carbon dioxide is not only known as an ingredient for sea soda. In fact, it’s probably better known as the baddie in the global warming story. The oceans aren’t just going to get lower on the pH scale. They are also getting warmer. And because scientists want to know everything, some of them went out and investigated what the combination of these two does to calcifying critters.

And there, in an ironic twist that allows us to feel a tiny bit of relief in the short term, they saw that a little warming (but not too much!) can actually mitigate the effects of acidification for some creatures. Make no mistake, baby sea urchins are still very screwed when you plunge them into “future” ocean water. But they are somewhat less screwed if you include warming in the package than if you just pump a load of CO2 into their tank (Byrne et al., 2010).

Calcifying animals in a real marine environment don’t exist in isolation – they prey on, are preyed on, help out and compete with members of other species. Will their different reactions to the changing chemistry of the ocean overhaul entire ecosystems? (I don’t read much ecological literature, so there are probably unseen-by-me studies of this out there…)

Lastly, there is a factor we always have to contend with when discussing environmental change, and that is adaptation. The experiments I’ve cited so far examine the reactions of individual organisms to changed circumstances, but the real change is occurring over a time scale of many generations for many of these creatures. As soon as you have such generation-spanning processes, evolution becomes a player. Will ocean calcifiers be able to adapt? Are there ways to predict which of them will?

There’s exactly one title in my reference manager that deals with that sort of thing, a breeding experiment/simulation study about a sea urchin and a mussel population by Sunday et al. (2011), but again, that paper points out how the ability to adapt will be highly dependent on the genetic variation present in a population. Genetic variation is not just species-dependent, it varies even within a species unless the entire species is one interconnected population (which does happen sometimes, see the recent news about giant squid). And there are many, many species in the ocean. Most of which we probably haven’t even seen, let alone studied.

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References:

Byrne M et al. (2011) Unshelled abalone and corrupted urchins: development of marine calcifiers in a changing ocean. Proceedings of the Royal Society B 278:2376-2383

Cameron CB & Bishop CD (2012) Biomineral ultrastructure, elemental constitution and genomic analysis of biomineralization-related proteins in hemichordates. Proceedings of the Royal Society B 279:3041-3048

Cooper TF et al. (2012) Growth of Western Australian corals in the Anthropocene. Science 335:593-596

Feely RA et al. (2001) Uptake and storage of carbon dioxide in the ocean: the global CO2 survey. Oceanography 14:18-32

Kroeker KJ et al. (2010) Meta-analysis reveals negative yet variable effects of ocean acidification on marine organisms. Ecology Letters 13:1419-1434

Miller AW et al. (2009) Shellfish face uncertain future in high CO2 world: influence of acidification on oyster larvae calcification and growth in estuaries. PLoS ONE 4:e5661

Ries JB et al. (2009) Marine calcifiers exhibit mixed responses to CO2-induced ocean acidification. Geology 37:1131-1134

Sunday JM et al. (2011) Quantifying rates of evolutionary adaptation in response to ocean acidification. PLoS ONE 6:e22881

Venn AA et al. (2013). Impact of seawater acidification on pH at the tissue–skeleton interface and calcification in reef corals. PNAS 110:1634-1639

Wood HL et al. (2008) Ocean acidification may increase calcification rates, but at a cost. Proceedings of the Royal Society B 275:1767-1773

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!

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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.

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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…

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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!

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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!

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References:

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

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.

Smith_etal2013-fig3_decorated

(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?

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*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.

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References:

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

An ode to sponges, skeletons and bacteria

Sponges are not what you’d normally think of as “exciting” animals. They are simple creatures that spend the entirety of their adult lives sitting around, patiently sifting immense amounts of water for microscopic food. The closest most of them get to “doing” anything is popping out a few babies every now and then. (Exception: deadly shrimp-killin’ predators :o) However, these (mostly) placid filter feeders have a lot to offer once we move past the usual coolness filters that make our inner ten-year-old a Velociraptor fan*.

I’ve been getting quite fond of sponges recently. It’s mostly a byproduct of the reading I do for my work, which partly concerns the mineralised hard parts of animals. All sponges have skeletons, and the majority of them make hard(ish) skeletons from one of two minerals: either amorphous silica (think glass) or calcium carbonate (think chalk, limestone, clam shell, etc.) (The rest, including bath sponges, use proteins.) Siliceous sponges in the class Hexactinellida (= glass sponges proper) can have beautiful, intricate skeletons like this one from a Venus’s flower basket (Euplectella sp. by NEON ja, Wikimedia Commons):

They are not only gorgeous, but, at least in some cases, also insanely strong and bendy – nature’s fibreglass fishing rods, if you like. See this photo from sponge guru Werner Müller’s group for a demonstration. That glass rod is the skeleton of Monorhaphis chuni, a deep-sea glass sponge that anchors itself with the largest known single structure made of silica in the living world. This “giant spicule” can be up to 3 m long, and flexible enough to bend around in a circle (Levi et al., 1989).

Some sponges have both glassy and calcareous (or “chalky”, if you like) skeletons. And such sponges are giving me all kinds of squee moments lately. Something I’ve only learned recently is that sponges often live in close association with a variety of bacteria. Now it turns out that these symbiotic bacteria contribute to their skeleton-building abilities!

Last year, Dan Jackson and his team published evidence that a sponge species stole a gene it uses to make its calcareous skeleton from a bacterium (Jackson et al., 2011). The gene in question occurs only in bacteria – and sponges. While the sponge species used in the study does harbour bacteria in the cells that produce the calcareous portion of its skeleton, multiple lines of evidence indicate that the gene in question sits in its own genome, and has done so for a long time. It is only active in the skeleton-forming cells, and its protein product is present in bits of skeleton isolated from the animal, suggesting that it does in fact function in building the skeleton. (As of that study, its exact role is still unknown.)

(Above: Astrosclera willeyana, coralline sponge and convicted gene thief. The living animal forms a crust over an ever-growing bulk of dead skeleton. From Jackson et al. [2011])

Most recently, another “spongy” research team found that members of a different sponge lineage have the actual bacteria in their cells make their skeletons for them. Uriz et al. (2012) examined three species of crater sponges, belonging to the “siliceous” sponge genus Hemimycale. In certain cells of the animals, they saw tiny round objects that molecular genetic tests revealed to be bacteria. The bacterial cells were surrounded by a coat of varying thickness that, when the researchers probed its elemental composition using X-rays, proved to be made of calcium carbonate. According to their observations, the bacteria live and divide inside membrane-enclosed vacuoles. They accumulate calcareous material as they mature, and finally the host cell spits them out to form a mineral crust around the animal. (Below: colonies of Hemimycale columella, one of the three species used in the study, from the Encyclopedia of Marine Life of Britain and Ireland via Encyclopedia of Life)

The bacteria look like they’ve had a long-standing partnership with their host sponges. They were abundant in all examined individuals of all three species. Unlike free-living bacteria, they appear to lack cell walls. They are also inherited by baby sponges. Mother Hemimycale sponges nurture their embryos in their bodies (apparently this is common among sponges). Sponges provide their embryos with so-called nurse cells, which, in the case of these species, contain some mineral-making bacteria. The young sponge eventually eats the nurse cells, thereby acquiring the bacteria. By the time it becomes independent and settles on a comfortable rock, its body is littered with tiny mineral spheres made by its inherited symbionts.

On closer examination, it seems that Hemimycale is far from the only sponge genus to harbour similar hired skeleton-builders. Uriz and colleagues tell us that they have found previously overlooked evidence of such “calcibacteria” in several other sponges – one of which is only distantly related to Hemimycale. Could calcibacteria be ancient partners of these animals, inherited by many different sponges from a distant common ancestor? Could bacteria even hold the key to the origin of calcareous animal skeletons?

(FWIW, I don’t really buy the second idea. As far as I know, all non-sponge animals that have been investigated make their skeletons with their own genes – nothing suspiciously bacterial-like the way Jackson et al.‘s spherulin is. [Caveat: there remain plenty of groups that haven’t been investigated in sufficient molecular detail.] However, the idea that sponges as a whole may have acquired their calcareous skeletons this way is fascinating. Incidentally, though the ID isn’t 100% certain yet, the calcibacteria may belong to the same bacterial class as mitochondria and these insidious bastards. Do alpha-proteobacteria have a special knack for endosymbiosis?)

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*Not to say Velociraptor isn’t cool, but being a vicious toothed, raptor-clawed killer bird is, well, not the only road to coolness 😛

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ETA: 42nd post, yay! (Also yay: random Hitchhiker’s Guide reference in completely unrelated post :D)

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References:

Jackson DJ et al. (2011) A horizontal gene transfer supported the evolution of an early metazoan biomineralization strategy. BMC Evolutionary Biology 11:238

Levi C et al. (1989) A remarkably strong natural glassy rod: the anchoring spicule of theMonorhaphis sponge. Journal of Materials Science Letters 8:337-339

Uriz MJ et al. (2012) Endosymbiotic calcifying bacteria: a new cue to the origin of calcification in Metazoa? Evolution early online view, doi: 10.1111/j.1558-5646.2012.01676.x

Much ado about nothing

I am disappointed.

I have a soft spot for Kimberella, one of the few Precambrian animals that we can identify with reasonable precision. (Not to mention its pretty name! :D) Our love affair started before I became involved with biomineralisation, which might have contributed to the fact that I totally overlooked Ivantsov (2009).

(Image: Ivantsov’s Kimberella, rendered by the masterful hands of Nobu Tamura. From Wikipedia.)

The paper shows up on Kimberella‘s lovely Wikipedia page as a citation for the following:

The deformation observed in elongated and folded specimens illustrates that the shell was highly malleable; perhaps, rather than a single integument, it consisted of an aggregation of (mineralized?) sclerites.

These days when I’m >this< close to dreaming about biominerals at night, this jumped out at me like a giant neon sign. What? A mineralising animal that old? (I think this was also before I saw Coronacollina.) So I downloaded the paper, and eventually got round to reading it, and…

Pfft.

It’s an alright piece of scientific literature, and it’s got lots of lovely pictures of Kimberella fossils (though Fedonkin et al. [2007] already had a ton of those). I would have been happy about it but for the fact that it totally flopped on the mineral thing. I thought that, you know, Ivantsov had some evidence to suggest that those bumps on the creature’s back were originally made of mineral stuff. And, indeed, his abstract quite confidently states not only that they were mineralised but also the specific mineral:

The fossil material shows that Kimberella had hard sclerites, probably of aragonite…

His reasoning? Let me quote…

The alternation of nodes and coarse folds in the central zone of the fossil may be explained by assuming that the nuclei of nodes were clumps of hard substance, which rapidly destroyed after the death of the animal. Aragonite, which obviously had no chances to be preserved in the terrigenous sediment, which, in addition, was saturated with hydrogen sulfide (Gehling, 2005), could have been such a substance.

I mean, really? They “could have been” made of aragonite because they disappeared? It’s like there is no other tough-ish material that can be destroyed after an animal dies. And he doesn’t go any deeper than that – no discussing/excluding other possibilities, nothing. He just leaves it there.

People, can you please not claim things in your abstracts that you then barely discuss, let alone demonstrate, in the paper?

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References:

Fedonkin MA et al. (2007) New data on Kimberella, the Vendian mollusc-like organism (White Sea region, Russia): palaeoecological and evolutionary implications. In: Vickers-Rich P & Komarower P (eds). The Rise and Fall of the Ediacaran Biota. Geological Society, London, Special Publications 286:157-179

Ivantsov YA (2009) New reconstruction of Kimberella, problematic Vendian metazoan. Paleontological Journal 43:601-611