The greatest science paper ever published in the history of humankind

Posted 12 July 2011 by PZ Myers

That's not hyperbole. I really mean it. How else could I react when I open up the latest issue of Bioessays, and see this: Cephalopod origin and evolution: A congruent picture emerging from fossils, development and molecules. Just from the title alone, I'm immediately launched into my happy place: sitting on a rocky beach on the Pacific Northwest coast, enjoying the sea breeze while the my wife serves me a big platter of bacon, and the cannula in my hypothalamus slowly drips a potent cocktail of cocain and ecstasy direct into my pleasure centers…and there's pie for dessert. It's like the authors know me and sat down to concoct a title where every word would push my buttons.

The content is pretty good, too. It's not perfect; the development part is a little thin, consisting mainly of basic comparative embryology of body plans, with nothing at all really about deployment of and interactions between significant developmental genes. But that's OK. It's in the nature of the Greatest Science Papers Ever Written that stuff will have to be revised and some will be shown wrong next month, and next year there will be more Greatest Science Papers Ever Written — it's part of the dynamic. But I'll let it be known, now that apparently the scientific community is aware of my obsessions and is pandering to them, that the next instantiation needs more developmental epistasis and some in situs.

This paper, though, is a nice summary of the emerging picture of cephalopod evolution, as determined by the disciplines of paleontology, comparative embryology, and molecular phylogenetics, and that summary is internally consistent and is generating a good rough outline of the story. And here is that story, as determined by a combination of fossils, molecular evidence, and comparative anatomy and embryology.

Cephalopods evolved from monoplacophoran-like ancestors in the Cambrian, about 530 million years ago. Monoplacophorans are simple, limpet-like molluscs; they crawl about on the bottom of the ocean under a cap-like shell, foraging snail-like on a muscular foot. The early cephalopods modified this body plan to rise up off the bottom and become more active: the flattened shell elongated to become a cone-like structure, housing chambers for bouyancy. Movement was no longer by creeping, but used muscular contractions through a siphon to propel the animal horizontally. Freed from its locomotor function, the foot expanded into manipulating tentacles.

These early cephalopods, which have shells common in the fossil record, would have spent their lives bobbing vertically in the water column, bouyed by their shells, and with their tentacles dangling downward to capture prey. They wouldn't have been particularly mobile — that form of a cone hanging vertically in the water isn't particularly well-streamlined for horizontal motion — so the next big innovation was a rotation of the body axis, swiveling the body axis 90° to turn a cone into a torpedo. There is evidence that many species did this independently.

The tilting of the body axes of extant cephalopods. This was a result of a polyphyletic and repeated trend towards enhanced manoeuverability. The morphological body axes (anterior-posterior, dorso-ventral) are tilted perpendicularly against functional axes in the transition towards extant cephalopods.

We can still see vestiges of this rotation in cephalopod embryology. If you look at early embryos of cephalopods (at the bottom of the diagram below), you see the same pattern: they are roughly disc-shaped, with a shell gland on top and a ring of tentacle buds on the bottom. They subsequently extend and elongage along the embryonic dorsal-ventral axis, which becomes the anterior-posterior axis in the adult.

In extant cephalopods the body axes of the adult stages are tilted perpendicularly versus embryonic stages. As a con- sequence, the morphological anterior-posterior body axis between mouth and anus and the dorso-ventral axis, which is marked by a dorsal shell field, is tilted 908 in the vertical direction in the adult cephalopod. Median section of A: Nautilus, B: Sepia showing the relative position of major organs (Drawings by Brian Roach). C: shared embryonic features in embryos of Nautilus (Nautiloidea) and Idiosepius (Coleoidea) (simplified from Shigeno et al. 2008 [23] Fig. 8). Orientation of the morphological body axes is marked with a compass icon (a, anterior; d, dorsal; p, posterior; v, ventral; dgl, digestive gland; gon, gonad; ngl, nidamental gland).

The next division of the cephalopods occurred in the Silurian/Devonian, about 416 million years ago, and it involved those shells. Shells are great armor, and in the cephalopods were also an organ of bouyancy, but they also greatly limit mobility. At that early Devonian boundary, we see the split into the two groups of extant cephalopods. Some retained the armored shells; those are the nautiloids. Others reduced the shell, internalizing it or even getting rid of it altogether; those are the coleoids, the most successful modern group, which includes the squids, cuttlefish, and octopuses. Presumably, one of the driving forces behind the evolution of the coleoids was competition from that other group of big metazoans, the fish.

The nautiloids…well, the nautiloids weren't so successful, evolutionarily speaking. Only one genus, Nautilus has survived to the modern day, and all the others followed the stem-group cephalopods into extinction.

The coleoids, on the other hand, have done relatively well. The number of species have fluctuated over time, but currently there are about 800 known species, which is respectable. The fish have clearly done better, with about 30,000 extant species, but that could change — there are signs that cephalopods have been thriving a little better recently in an era of global warming and acute overfishing, so we humans may have been giving mobile molluscs a bit of a tentacle up in the long evolutionary competition.

There was another major event in coleoid history. During the Permian, about 276 million years ago, there was a major radiation event, with many new species flourishing. In particular, there was another split: between the Decabrachia, the ten-armed familiar squid, and the Vampyropoda, a group that includes the eight-armed octopus, the cirroctopodes, and Vampyroteuthis infernalis. The Vampyropoda have had another locomotor shift, away from rapid jet-propelled movement to emphasizing their fins for movement, or in the case of the benthic octopus, increasing their flexibility to allow movement through complex environments like the rocky bottom.

Time for the big picture. Here's the tree of cephalopod evolution, using dates derived from a combination of the available fossil evidence and primarily molecular clocks. The drawings illustrate the shell shape, or in the case of the coleoids, the shape of the internal shell, or gladius, if they have one.

A molecularly calibrated time-tree of cephalopod evolution. Nodes marked in blue are molecular divergence estimates (see methods in Supplemental Material). The divergence of Spirula from other decabrachiates are from Warnke et al. [43], the remaining divergences are from analyses presented in this paper. Bold lineages indicate the fossil record of extant lineages, stippled lines are tentative relationships between modern coleoids, partly based on previous studies [41, 76, 82] and fossil relationships are based on current consensus and hypoth- eses presented herein. Shells of stem group cephalopods and Spirula in lateral view with functional anterior left. Shells of coleoids in ventral view with anterior down. The Mesozoic divergence of coleoids is relatively poorly resolved compared to the rapid evolution of Cambro- Ordovician stem group cephalopods. Many stem group cephalopod orders not discussed in the text are excluded from the diagram.

The story and the multiple lines of evidence hang together beautifully to make a robust picture of cephalopod evolution. The authors do mention one exception: Nectocaris. Nectocaris is a Cambrian organism that looks a bit like a two-tentacled, finned squid, which doesn't fit at all into this view of coleoids evolving relatively late. The authors looked at it carefully, and invest a substantial part of the review discussing this problematic species, and decided on the basis of the morphology of its gut and of the putative siphon that there is simply no way the little beast could be ancestral to any cephalopods: it's a distantly related lophotrochozoan with some morphological convergence. It's internal bits simply aren't oriented in the same way as would fit the cephalopod body plan.

So that's the state of cephalopod evolution today. I shall be looking forward to the Next Great Paper, and in particular, I want to see more about the molecular biology of tentacles — that's where the insights about the transition from monoplacophoran to cephalopod will come from, I suspect.

Kröger B, Vinther J, Fuchs D (2011) Cephalopod origin and evolution: A congruent picture emerging from fossils, development and molecules: Extant cephalopods are younger than previously realised and were under major selection to become agile, shell-less predators. Bioessays doi: 10.1002/bies.201100001.

38 Comments

mrg · 12 July 2011

Greatest thing since icecream? Arguable. But cool, definitely.

cronk · 13 July 2011

Upon first glance of the title of this thread I thought it would be another screed from Casey Luskin.
My first clue (of many) should have been the word 'published'.

harold · 13 July 2011

It's extremely interesting that some cephalopods have developed behavior that we describe as intelligent.

In mammalian lineages, we usually see such behavior in the context of high degree of cephalization, carnivore or omnivore status, relatively long period of young to maturity, some degree of "raising" of young, and often if not exclusively, social behavior.

In other vertebrate lineages such as birds, this may be less the case.

Cephalopods have very different neurobiology from mammals or any vertebrates, to put it mildly.

More research on the neurobiology of cephalopod learning could be quite illuminating.

John · 13 July 2011

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Robert Byers · 15 July 2011

This is a good example of some YEC complaints about evolutionary research.
First conclusions are based greatly on the geological presumptions of time.
There is evolution, they say, because the geology teaches these long ages and segegated ages to the fossil sequences.
This is not biology but geology.
Therefore the conclusions are not based on biological research alone or some cases very much.
Indeed how can one do much biology on mere casts of remains of former biology?
A flaw in the whole thing.

There is no reason or hunch that these creatureslived at different times. They simply show the great diversity at the time of collective fossilization.

Another point is how the researchers admit they make decisions on classification based on bits and pieces.
Then everyone argues about it.
In fact I don't see how convergence ideas can't always be invoked to throw in doubt how to lump creatures together.

I understand the eyes of these creatures are unlike other sea creatures entirely. i'm not sure but if so its another case of convergence with landlovers.
most unlikely. Better ideas are that there are simple and limited options in biology for complex body parts.

Don't mean to ruin anyones summer reading but just bringing up common creationist complaints never dealt with very much.

pianoguy · 15 July 2011

What I love about your headline, more than anybody has ever loved anything ever before, is the way it avoids, to a degree never before approached in any writing by anybody anywhere, even the faintest hint of hyperbole.

John · 15 July 2011

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John Harshman · 15 July 2011

I continually worry about how much of our knowledge of past life is conditioned by taphonomic bias. Do shelled cephalopods really provide an adequate guide to the evolution of all cephalopods? Certainly the preservable cnidarians don't tell us a lot about that taxon. Then again, the preserved gastropods are probably pretty good. So where do cephalopods fall on that scale? And how could we tell?

circleh · 15 July 2011

Robert Byers said: This is a good example of some YEC complaints about evolutionary research. First conclusions are based greatly on the geological presumptions of time. There is evolution, they say, because the geology teaches these long ages and segegated ages to the fossil sequences. This is not biology but geology. Therefore the conclusions are not based on biological research alone or some cases very much. Indeed how can one do much biology on mere casts of remains of former biology? A flaw in the whole thing.

Are you saying there should be no connection between biology and geology? On the contrary, there needs to be such connections because both fields of study work in the same universe. Long periods of time are indicated by the consistent application of physical and chemical laws, and there is NO evidence that those laws are not universal.

There is no reason or hunch that these creatures lived at different times. They simply show the great diversity at the time of collective fossilization.

Liar.

Another point is how the researchers admit they make decisions on classification based on bits and pieces. Then everyone argues about it. In fact I don't see how convergence ideas can't always be invoked to throw in doubt how to lump creatures together.

I hope you never become a police detective or do forenics.

I understand the eyes of these creatures are unlike other sea creatures entirely. i'm not sure but if so its another case of convergence with landlovers. most unlikely. Better ideas are that there are simple and limited options in biology for complex body parts. Don't mean to ruin anyones summer reading but just bringing up common creationist complaints never dealt with very much.

Those complaints are bullcrap, as usual.

John · 15 July 2011

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John · 15 July 2011

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John Harshman · 16 July 2011

John said: Methinks you worry too much John. The record is especially good for shelly marine invertebrates, which do comprise a substantially large segment of the modern marine biosphere. Shelled cephalopods - including nautiloids and ammonoids - are exceedingly rich, especially in Paleozoic and Mesozoic marine faunas. I strongly doubt that shell-less cephalopods were important - or had evolved - in the midst of the Great Ordovician Diversification Event which saw the rise of eurypterids and other heavily armored predators. Against predators like eurypterids, placoderms and other predatory fishes, I strongly suspect that "naked" cephalopods had much evolutionary success.

And I don't see how your suspicions can amount to more than a guess. There are many ways to evade predators other than armor. They're common in today's biota, and I see no reason to suppose that the Ordovician predators were such super-monsters that the same sort of thing wouldn't have worked then. We just have little means of knowing. Our knowledge of soft-bodied taxa is largely limited to a few lagerstaetten, and most of that is of ecdysozoans or other animals with cuticles; even there, I suspect, molluscs would be under-represented. It may well be that shell-less cephalopods are a recent development. But how can we tell?

Early Paleozoic marine faunas have many taxa that were heavily armored against top predators like eurypterids, other arthropods like Anomalocaris (which apparently did persist into the Early Ordovician based on ongoing research by Yale invertebrate paleobiologist Derek Briggs and one of his postdocs) and placoderms. For these reasons, I strongly doubt that there were any "naked" cephalopods in existence. And this merely supports my contention that the fossil record for shelly marine invertebrates is much better - and has less of a taphonomic constraint imposed upon it - than you seem willing to admit (On the other hand, notable ecologists like Arizona's Michael Rosenzweig and Stony Brook's Jeff Levinton clearly understand that the metazoan marine invertebrate fossil record is quite substantial and a strong indicator of Earth's marine biodiversity for the entire Phanerozoic Eon and would disagree with your grave concerns with regards to any strong taphonomic biases.).

First, I'm not saying that the record of shelly marine invertebrates is poor. I'm just saying the whole record is biased in their favor. Whether that results in missing a lot of taxa is not at issue, unless you think, say, rotifers and nematodes are also recent developments. The question is whether there are large, cryptic radiations of shell-less cephalopods. I don't know if there are, but I don't know if there aren't. The claim that there can't be because predators were just too mean until recently does not, in my mind, hold any credibility. There is one argument that might work. There has been a claim of a late Mesozoic increase in diversity of durophages, possibly a response to the evolution of hermit crabs. More durophages would lessen the utility of shells and make going naked more attractive. Still speculative, though. Finally, I'm sure that Rosenzweig and Levinton would agree that the record of well-skeletonized marine invertebrates is quite adequate for many purposes, but not for many others. As an index to changes in diversity of the whole biota, it might be pretty good. But it's hardly a good count of total diversity, given the dozen or so entire phyla with no or almost no record, including what's probably the second most diverse animal phylum.

Robert Byers · 18 July 2011

John said:
John Harshman said: I continually worry about how much of our knowledge of past life is conditioned by taphonomic bias. Do shelled cephalopods really provide an adequate guide to the evolution of all cephalopods? Certainly the preservable cnidarians don't tell us a lot about that taxon. Then again, the preserved gastropods are probably pretty good. So where do cephalopods fall on that scale? And how could we tell?
Methinks you worry too much John. The record is especially good for shelly marine invertebrates, which do comprise a substantially large segment of the modern marine biosphere. Shelled cephalopods - including nautiloids and ammonoids - are exceedingly rich, especially in Paleozoic and Mesozoic marine faunas. I strongly doubt that shell-less cephalopods were important - or had evolved - in the midst of the Great Ordovician Diversification Event which saw the rise of eurypterids and other heavily armored predators. Against predators like eurypterids, placoderms and other predatory fishes, I strongly suspect that "naked" cephalopods had much evolutionary success.

You say "strongly doubt" and "strongly suspect". I see this also in the this threads lead. Conclusions on such matters must be on solid quality and quantity of evidence. This is a creationist complaint. Where is the 'science'. It all seems very simple decisions on minor points about these casts! I always note in classifications that there are disagreements about how to score relationships based on having this or that part. Since evolution sees gradualism it really gets mixed up. Then I note convergence conclusions are thrown in when needed. In fact convergence of forms and functions is so applied that it makes meaningless any confidence in who is deciding whats parts are the defining trail of identity. Then I note that very people are involved at all and it seems to any curious creationist the whole thing is set for a knock down . In my interests I note the creodonta group which has creatures with same shaped bodies as other creatures in earth history but said to be unrelated was said to be from some of original rodent but now they just invoke convergent evolution acting on different creatures to explain how they got like creodonta features. Just that easy I read in wiki.

Dave Luckett · 18 July 2011

Here's Byers, again.

A man who is to science what William Topaz Mcgonagall was to (as he would put it) the bardic arts.

apokryltaros · 18 July 2011

Dave Luckett said: Here's Byers, again. A man who is to science what William Topaz Mcgonagall was to (as he would put it) the bardic arts.

Robert Byers confuses ignorance with skepticism, and wants to convince us to abandon science simply because GODDIDIT is easier to remember.

mrg · 18 July 2011

Dave Luckett said: Here's Byers, again.

"Byers"?! People are talking about this mysterious "Byers" again! Is this some sort of a prank? You can't convince me such a thing exists. Next you'll be claiming you believe in BigFoot and the Loch Ness Monster.

Shebardigan · 18 July 2011

Dave Luckett said: A man who is to science what William Topaz Mcgonagall was to (as he would put it) the bardic arts.

Hmm. Mcgonagall was at least, to some of us working in obscure corners of the entertainment industry, useful. Unintentionally amusing, unlike the antecedent above.

Mike Elzinga · 18 July 2011

If Bobby Byers has formed an alliance,

With the purveyors of pseudo-science,

Then it makes sense,

That he is so dense,

And his postings are merely acts of defiance.

Burma Shave.

John · 18 July 2011

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John · 18 July 2011

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John · 18 July 2011

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Mike Elzinga · 18 July 2011

John said:
Mike Elzinga said: If Bobby Byers has formed an alliance, With the purveyors of pseudo-science, Then it makes sense, That he is so dense, And his postings are merely acts of defiance. Burma Shave.
Booby's comments are not worthy of comment except maybe in song. Too bad I can't think of a clever Bernie Taupin lyric to describe the acute state of his mental retardation with respect to science.

In order to be come a poet laureate, One’s poems have to tell a story; yet, To get past the vetter, The stories have to be better Than all of the attempts by such people whose goals are on glory set. (Look, Ma; I’m a natural!)

John Harshman · 18 July 2011

John said: Sorry John, we've been bickering back and forth over this for months. Am surprised you didn't raise a stink with Jack Sepkoski, David Raup and David Jablonski. As for Michael Rosenzweig, he's worked off and on with taxonomic diversity data from both the Phanerozoic invertebrate and vertebrate fossil record for years, and I do know that he had spent a lot of time discussing it with Jablonski prior to Jablonski's move from Arizona to Chicago.

In what way have I disagreed with any of those folks?

It's not until the Mesozoic Era that you see a substantial fossil record in "naked" cephalopods,

Not quite. There is no appreciable fossil record for naked cephalopods. The one's you're thinking of have readily preservable internal shells. How do you know there weren't plenty of others without those internal shells?

and I think a very important reason for that is because it probably took the coleoids that long to diverge from ancestral ammonoids sometime in the latest Paleozic and develop jet propulsion to evade predators. I think the paucity of soft-bodied taxa in the early Paleozoic represents real data, not something you can just dismiss simply on the basis of the poor distribution of lagerstatten. As for the durophagy argument, that may be a possible explanation, but it would not account for the preponderance of heavily armored predators and prey during the earliest Paleozoic.

How do you even know it's a preponderance? How do you know the paucity of soft-bodied taxa is not an artifact? It's hardly a feature of the Paleozoic record. There are few soft-bodied taxa anywhere. You can think any think you like. The question is whether you have defensible reasons for your thoughts. I think we've been through that before too. (Though in fact I have only just now realized that you are Kwok. Call me unobservant.)

Mike Elzinga · 18 July 2011

John said: Booby's comments are not worthy of comment except maybe in song. Too bad I can't think of a clever Bernie Taupin lyric to describe the acute state of his mental retardation with respect to science.

I think Dave Luckett and Shebardigan have hit the nail right on the head by comparing McGonagall to Byers (and the other trolls here). To a scientist’s ears, ID/creationist doggerels about science are just as grating as MCGonagall is to the ears of the poet. Here is another example of ear-grating verse. -------------------------------------------------------------------- The creationist troll’s fight song. Because I am a man of great humility, I seek God and his great tranquility. But because God does will me, To seek out battles that do thrill me, I go to Panda’s Thumb and shame evolutionists with my powerful ability. ------------------------------------------------------------------------- It hadn’t occurred to me, until Dave and Shebardigan mentioned it, that creationists can be parodied with bad poetry. And that doesn’t require years of training in science to appreciate. I think Dave’s and Shebardigan’s observation is brilliant.

John · 18 July 2011

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John · 18 July 2011

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John · 18 July 2011

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Dave Luckett · 19 July 2011

THE EXPULSION FROM THE GARDEN, only not.

It was perhaps a wee while after the first Sabbath Day

When God from Labours did rest, and put his tools away

That our very first ancestress, on the side of the distaff,

Was out walking, and chanced to see on the path

A serpent, and instead of crushing its head

As any man with sense would do, she listened as it said,

"Oh eat of the fruit of the tree which is knowledge,

And you won't have to go out to school or to college!"

And she saith, "What are you, crazy? You schlemiel!" For I wish

To inform you that she was certainly Jewish.

"You momser! You putz!" And I wish to relate

Many other expressions that are hard to translate.

But the snake said, "Just think! It is good for you, madam.

So have some yourself, and give the rest to Adam."

But she wouldn't. So that's why we still live in Eden,

Which we now call "Dundee", where we have all that we're needing.

John · 19 July 2011

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tomh · 19 July 2011

I have only just now realized that you are Kwok

hehe, Kwok dropped his last name to avoid the automatic trip to the BW that PZ usually gives him. He is too shrewd!

John · 19 July 2011

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John · 19 July 2011

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mrg · 19 July 2011

tomh said: hehe, Kwok dropped his last name to avoid the automatic trip to the BW that PZ usually gives him. He is too shrewd!

Looks like PZ, probably distracted, didn't realize that until you mentioned it, and now it's all been flushed. I think most everybody else figured it out after a posting or two ... the style is unmistakeable, in much the same way that I can quickly recognize when I'm downwind of a cattle feedlot.

John Harshman · 19 July 2011

What? Kwok is banned? Why? Is there a rule against poor reasoning?

mrg · 19 July 2011

John Harshman said: What? Kwok is banned? Why? Is there a rule against poor reasoning?

I believe it has to do at least in part with JK's demand that PZ buy him a camera. BTW, I checked out PZ's file on "Rate My Professors". He gets high marks, the only big complaint is that he's running around so much he's hard to get hold of. Behe gets fair marks. Some students of Duesberg flatly called him a crank.

D P Robin · 19 July 2011

John Harshman said: What? Kwok is banned? Why? Is there a rule against poor reasoning?

John Kwok and PZ have a long-standing feud. He is banned on Pharyngula, http://scienceblogs.com/pharyngula/2009/03/survivor_pharyngula_day_five.php and is listed in the Dungeon as guilty of the crimes of "insipidity" and "stupidity" http://scienceblogs.com/pharyngula/plonk.php PZ usually flushes JK into (onto?) the BW. Whenever JK comments in one of his threads. dpr

mrg · 19 July 2011

I wouldn't call it a feud. JK acts pretty much as he always does, PZ flushes him on sight.

Mike Elzinga · 19 July 2011

Dave Luckett said: THE EXPULSION FROM THE GARDEN, only not. It was perhaps a wee while after the first Sabbath Day When God from Labours did rest, and put his tools away That our very first ancestress, on the side of the distaff, Was out walking, and chanced to see on the path A serpent, and instead of crushing its head As any man with sense would do, she listened as it said, "Oh eat of the fruit of the tree which is knowledge, And you won't have to go out to school or to college!" And she saith, "What are you, crazy? You schlemiel!" For I wish To inform you that she was certainly Jewish. "You momser! You putz!" And I wish to relate Many other expressions that are hard to translate. But the snake said, "Just think! It is good for you, madam. So have some yourself, and give the rest to Adam." But she wouldn't. So that's why we still live in Eden, Which we now call "Dundee", where we have all that we're needing.

I sure would be curious to see how Ken Ham would respond. :-)