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This post is solely my opinion; not reflecting any views of my coauthors, my university, etc, and was written in my free time at home. I am just putting my current thoughts in writing, with the hope of stimulating some discussion. My post is based on some ruminations I’ve had over recent years, in which I’ve seen a lot of change happening in how science’s self-correcting process works, and the levels of openness in science, which are trends that seem likely to only get more intense.

That’s what this post ponders- where are we headed and what does it mean for scientists and science? Please stay to the end. It’s a long read, but I hope it is worth it. I raise some points at the end that I feel strongly about, and many people (not just scientists) might also agree with or be stimulated to think about more.

I’ve always tried to be proactive about correcting my (“my” including coauthors where relevant) papers, whether it was a publisher error I spotted or my/our own; I’ve done at least 5 such published corrections. Some of my later papers have “corrected” (by modifying and improving the methods and data) my older ones, to the degree that the older ones are almost obsolete. A key example is my 2002 Nature paper on “Tyrannosaurus rex was not a fast runner“- a well-cited paper that I am still proud of. I’ve published (with coauthors aplenty) about 10 papers since then that explore various strongly related themes, the accuracy of assumptions and estimates involved, and new ways to approach the 2002 paper’s main question. The message of that paper remains largely the same after all those studies, but the data have changed to the extent that it would no longer be viable to use them. Not that this paper was wrong; it’s just we found better ways to do the science in the 12 years since we wrote it.

I think that is the way that most of science works; we add new increments to old ones, and sooner or later the old ones become more historical milestones for the evolution of ideas than methods and data that we rely on anymore. And I think that is just fine. I cannot imagine it being any other way.

If you paid close attention over the past five months, you may have noticed a kerfuffle (to put it mildly) raised by former Microsoft guru/patent afficionado/chef/paleontologist Nathan Myhrvold over published estimates of dinosaur growth rates since the early 2000’s. The paper coincided with some emails to authors of papers in question, and some press attention, especially in the New York Times and the Economist. I’m not going to dwell on the details of what was right or wrong about this process, especially the scientific nuances behind the argument of Myhrvold vs. papers in question. What happened happened. And similar things are likely to happen again to others, if the current climate in science is any clue. More about that later.

But one outcome of this kerfuffle was that my coauthors and I went through (very willingly; indeed, by my own instigation) some formal procedures at our universities for examining allegations of flaws in publications. And now, as a result of those procedures, we issued a correction to this paper:

Hutchinson, J.R., Bates, K.T., Molnar, J., Allen, V., Makovicky, P.J. 2011. A computational analysis of limb and body dimensions in Tyrannosaurus rex with implications for locomotion, ontogeny, and growth. PLoS One 6(10): e26037. doi: 10.1371/journal.pone.0026037  (see explanatory webpage at: http://www.rvc.ac.uk/SML/Projects/3DTrexGrowth.cfm)

The paper correction is here: http://www.plosone.org/article/info%3Adoi/10.1371/journal.pone.0097055. Our investigations found that the growth rate estimates for Tyrannosaurus were not good enough to base any firm conclusions are, so we retracted all aspects of growth rates from that paper. The majority of the paper, about estimating body mass and segment dimensions (masses, centres of mass, inertia) and muscle sizes as well as their changes through growth and implications for locomotor ontogeny, still stands; it was not in question.

For those (most of you!) who have never gone through such a formal university procedure checking a paper, my description of it is that it is a big freakin’ deal! Outside experts may be called in to check the allegations and paper, you have to share all your data with them and go through the paper in great detail, retracing your steps, and this takes weeks or months. Those experts may need to get paid for their time. It is embarassing even if you didn’t make any errors yourself and even if you come out squeaky clean. And it takes a huge amount of your time and energy! My experience started on 16 December, reached a peak right around Xmas eve (yep…), and finally we submitted our correction to PLoS and got editorial approval on 20 March. So it involved three months of part-time but gruelling dissection of the science, and long discussions of how to best correct the problems. Many cooks! I have to admit that personally I found the process very stressful and draining.

Next time you wonder why science can be so slow at self-correction, this is the reason. The formal processes and busy people involved mean it MUST be slow– by the increasingly speedy standards of  modern e-science, anyway. Much as doing science can be slow and cautious, re-checking it will be. Should be?

My message from that experience is to get out in front of problems like this, as an author. Don’t wait for someone else to point it out. If you find mistakes, correct them ASAP. Especially if they (1) involve inaccurate data in the paper (in text, figures, tables, whatever), (2) would lead others to be unable to reproduce your work in any way, even if they had all your original methods and data, or (3) alter your conclusions. It is far less excruciating to do it this way then to have someone else force you to do it, which will almost inevitably involve more formality, deeper probing, exhaustion and embarassment. And there is really no excuse that you don’t have time to do it. Especially if a formal process starts. I can’t even talk about another situation I’ve observed, which is ongoing after ~3 years and is MUCH worse, but I’ve learned more strongly than ever that you must demonstrate you are serious and proactive about correcting your work.

I’ve watched other scientists from diverse fields experience similar things– I’m far from alone. Skim Retraction Watch and you’ll get the picture. What I observe both excites me and frightens me. I have a few thoughts.

1) The drive to correct past science is a very good development and it’s what science is meant to be about. This is the most important thing!

2) The digital era, especially trends for open access and open data for papers, makes corrections much easier to discover and do. That is essentially good, and important, and it is changing everything about how we do science. Just watch… “we live in interesting times” encapsulates the many layers of feelings one should react with if you are an active researcher. I would not dare to guess what science will be like in 20 years, presumably when I’ll be near my retirement and looking back on it all!

3) The challenge comes in once humans get involved. We could all agree on the same lofty principles of science and digital data but even then, as complex human beings, we will have a wide spectrum of views on how to handle cases in general, or specific cases.

This leads to a corollary question– what are scientists? And that question is at the heart of almost everything controversial about scientific peer review, publishing and post-publication review/correction today, in my opinion. To answer this, we need to answer at least two sub-questions:

1–Are we mere cogs in something greater, meant to hunker down and work for the greater glory of the machine of science?

(Should scientists be another kind of public servant? Ascetic monks?)

2–Are we people meant to enjoy and live our own lives, making our own choices and value judgements even if they end up being not truly optimal for the greater glory of science?

(Why do we endure ~5-10 years of training, increasingly poor job prospects/security, dwindling research funds, mounting burdens of expectations [e.g., administrative work, extra teaching loads, all leading to reduced freedoms] and exponentially growing bureaucracies? How does our experience as scientists give meaning to our own lives, as recompense?)

The answer is, to some degree, yes to both of the main questions above, but how we reconcile these two answers is where the real action is. And this brew is made all the spicier by the addition of another global trend in academia: the corporatization of universities (“the business model”) and the concomitant, increasing concern of universities about public image/PR and marketing values. I will not go any further with that; I am just putting it out there; it exists.

The answer any person gives will determine how they handle a specific situation in science. You’ve reminded your colleague about possible errors in their work and they haven’t corrected it. Do you tell their university/boss or do you blog and tweet about it, to raise pressure and awareness and force their hand? Or do you continue the conversation and try to resolve it privately at any cost? Is your motive truly the greater glory of science, or are you a competitive (or worse yet, vindictive or bitter) person trying to climb up in the world by dragging others down? How should mentors counsel early career researchers to handle situations like this? Does/should any scientist truly act alone in such a regard? There may be no easy, or even mutually exclusive, answers to these questions.

We’re all in an increasingly complex new world of science. Change is coming, and what that change will be like or when, no one truly knows. But ponder this:

Open data, open science, open review and post-publication review, in regards to correcting/retracting past publications: how far down the rabbit hole do we go?

The dinosaur growth rates paper kerfuffle concerned numerous papers that date back to earlier days of science, when traditions and expectations differed from today’s. Do we judge all past work by today’s standards, and enforce corrections on past work regardless of the standards of its time? If we answer some degree of “yes” to this, we’re in trouble. We approach a reductio ad absurdum: we might logic ourselves into a corner where that great machine of science is directed to churn up great scientific works of their time. Should Darwin’s or Einstein’s errors be corrected or retracted by a formal process like those we use today? Who would do such an insane thing? No one (I hope), but my point is this: there is a risk that is carried in the vigorous winds of the rush to make science look, or act, perfect, that we dispose of the neonate in conjunction with the abstergent solution.

OK I used 1 image...

There is always another way. Science’s incremental, self-correcting process can be carried out quite effectively by publishing new papers that correct and improve on old ones, rather than dismantling the older papers themselves. I’m not arguing for getting rid of retractions and corrections. But, where simple corrections don’t suffice, and where there is no evidence of misconduct or other terrible aspects of humanity’s role in science, perhaps publishing a new paper is a better way than demolishing the old. Perhaps it should be the preferred or default approach. I hope that this is the direction that the Myhrvold kerfuffle leans more toward, because the issues at stake are so many, so academic in nature, and so complex (little black/white and right/wrong) that openly addressing them in substantial papers by many researchers seems the best way forward. That’s all I’ll say about that.

I still feel we did the right thing with our T. rex growth paper’s correction. There is plenty of scope for researchers to re-investigate the growth question in later papers.  But I can imagine situations in which we hastily tear down our or others’ hard work in order to show how serious we are about science’s great machine, brandishing lofty ideals with zeal– and leaving unfairly maligned scientists as casualties in our wake. I am reminded of outbursts over extreme implementations of security procedures at airports in the USA, which were labelled “security theatre” for their extreme cost, showiness and inconvenience, with negligible evidence of security improvements.

The last thing we want in science is an analogous monstrosity that we might call “scientific theatre.” We need corrective procedures for and by scientists, that serve both science and scientists best. Everyone needs to be a part of this, and we can all probably do better, but how we do it… that is an interesting adventure we are on. I am not wise enough to say how it should happen, beyond what I’ve written here. But…

A symptom of scientific theatre might be a tendency to rely on public shaming of scientists as punishment for their wrongs, or as encouragement for them to come clean. I know why it’s done. Maybe it’s the easy way out; point at someone, yell at them in a passionate tone backed up with those lofty ideals, and the mob mentality will back you up, and they will be duly shamed. You can probably think of good examples. If you’re on social media you probably see a lot of it. There are naughty scientists out there, much as there are naughty humans of any career, and their exploits make a good story for us to gawk at, and often after a good dose of shaming they seem to go away.

But Jon Ronson‘s ponderings of the phenomenon of public shaming got me thinking (e.g., from this WTF podcast episode; go to about 1 hr 9 min): does public shaming belong in science? As Ronson said, targets of severe public shaming have described it as “the worst pain ever”, and sometimes “there’s no recourse” for them. Is this the best way to live together in this world? Is it really worth it, for scientists to do to others or to risk having done to them? What actually are its costs? We all do it in our lives sometimes, but it deserves introspection. I think there are lessons from the dinosaur growth rates kerfuffle to be learned about public shaming, and this is emblematic of problems that science needs to work out for how it does its own policing. I think this is a very, very important issue for us all to consider, in the global-audience age of the internet as well as in context of the intense pressures on scientists today. I have no easy answers. I am as lost as anyone.

What do you think?

 

EDIT: I am reminded by comments below that 2 other blog posts helped inspire/coagulate my thoughts via the alchemy of my brain, so here they are:

http://dynamicecology.wordpress.com/2014/02/24/post-publication-review-signs-of-the-times/ Which considers the early days of the Myhrvold kerfuffle.

http://blogs.discovermagazine.com/neuroskeptic/2014/01/27/post-publication-cyber-bullying/ Which considers how professional and personal selves may get wounded in scientific exchanges.

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(John: here’s a guest post from my former PhD student, soon to be 100% legit PhD, Dr., and all that jazz, Julia Molnar!)

This is my first guest post, but I have been avidly following what’s in John’s freezer (and the blog too) for quite a while. I joined the lab in 2009 and left a month ago on the bittersweet occasion of surviving my PhD viva (oral exam/defense), so I’d like to take a moment here to thank John and the Structure & Motion Lab for a great 4 years!

Moving on to freezer-related matters; specifically, a bunch of frozen crocodile spines. It was late 2011, and the reason for the spines in John’s freezer was that John, Stephanie Pierce, and I were trying to find out more about crocodile locomotion. This was anticipated to become my first major, first-author research publication (but see my Palaeontologia Electronica paper on a related subject), and I was about to find out that these things seldom go as planned; for example, the article would not be published for more than three years (the research took a long time!). Before telling the story of how it lurched and stumbled toward eventual publication, I’ll give you some background on the project.

Stomach-Churning Rating: 3/10; x-ray of dead bits and nothing much worse.

A stumbly sort-of-bounding crocodile. They can do better.

First of all, why crocodiles? For one thing, they’re large, semi-terrestrial animals, but they use more sprawling postures than typical mammals. Along with alligators and gharials, they are the only living representatives of Crocodylomorpha, a 200+ million year-old lineage that includes wolf-like terrestrial carnivores, fish-like giants with flippers and a tail fin, even armored armadillo-like burrowers. Finally, crocodiles are interesting in their own right because they use a wide variety of gaits, including bounding and galloping, which are otherwise known only in mammals.

Nile croc

Nile crocodile skeletal anatomy

OK, so why spines? Understanding how the vertebral column works is crucial to understanding locomotion and body support on land, and inter-vertebral joint stiffness (how much the joints of the backbone resist forces that would move them in certain directions) in particular has been linked to trunk movements in other animals. For this reason, vertebral morphology is often used to infer functional information about extinct animals, including dinosaurs. However, vertebral form-function relationships have seldom been experimentally tested, and tests on non-mammals are particularly scarce. So we thought the crocodile spines might be able to tell us more about the relationship between vertebral morphology, mechanics, and locomotion in a broader sample of vertebrate animals. If crocodile spine morphology could be used to predict joint stiffness, then morphological measurements of extinct crocodile relatives would have some more empirical heft to them. Several skeletal features seem to play roles such as levers to mechanically stiffen crocodile spines (click to emcroc’en):

Croc vertebra-01

Anatomy of a crocodile vertebra

We decided to use a very simple technique that could be replicated in any lab to measure passive stiffness in crocodile cadavers. We dissected out individual joints were and loaded with known weights. From the movement of the vertebrae and the distance from the joint, we calculated how much force takes to move the joint a certain number of degrees (i.e. stiffness).

Julia w vertebra (480x640)

Me with crocodile vertebra and G-clamp

Xray

X-ray of two crocodile vertebrae loaded with a metric weight to calculate their joint’s stiffness

Afterwards, we boiled the joints to remove the soft tissues – the smell was indescribable! We took 14 measurements from each vertebra. All of these measurements had been associated with stiffness or range of motion in other studies, so we thought they might be correlated with stiffness in crocodiles also.

morphometrics

Some of the vertebral measurements that were related to stiffness

Despite my efforts to keep it simple, the process of data collection and analysis was anything but. I recall and exchange with Stephanie Pierce that went something like this:

Stephanie: “How’s it going?”

Me: “Well, the data are messy, I’m not seeing the trends I expected, and everything’s taking twice as long as it was supposed to.”

Stephanie: “Yes, that sounds like science.”

That was the biggest lesson for me: going into the project, I had been unprepared for the amount of bumbling around and re-thinking of methods when the results were coming up implausible or surprising. In this case there were a couple of cool surprises: for one thing, crocodiles turn out to have a very different pattern of inter-vertebral joint stiffness than typical mammals: while mammals have stiff thoracic joints and mobile lumbar joints, crocodiles have stiffer lumbar joints. Many mammals use large lumbar movements during bounding and galloping, so crocodiles must use different axial mechanics than mammals, even during similar gaits. While that’s not shocking (they did evolve their galloping and bounding gaits, and associated anatomy, totally independently), it is neat that this result came out so clearly. Another unexpected result was that, although several of our vertebral measurements were correlated with stiffness, some of the best predictors of stiffness in mammals from previous studies were not correlated with stiffness in crocodiles. The study tells a cautionary tale about making assumptions about extinct animals using data from only a subset of their living relatives or intuitive ideas about form and function.

Finally, the experience of doing the experiments and writing the paper got me interested in other aspects of crocodilian functional anatomy. For instance, how does joint stiffness interact with other factors, such as muscle activity and properties of the ribs, skin, and armor in living crocodiles? Previous studies by Frey and Salisbury had commented on this, but the influence of those factors is less tractable to experiment on or model than just naked backbones with passively stiff joints. In the future, I’d like to study vertebral movements during locomotion in crocodiles – especially during bounding and galloping – to find out how these patterns of stiffness relate to movement. In the meantime, our study shows that, to a degree, crocodile backbone dimensions do give some clues about joint stiffness and locomotor function.

To find out more, read the paper! It was just featured in Inside JEB.

Julia Molnar, Stephanie Pierce, John Hutchinson (2014). An experimental and morphometric test of the relationship between vertebral morphology and joint stiffness in Nile crocodiles (Crocodylus niloticus). The Journal of Experimental Biology 217, 757-768 link here and journal’s “Inside JEB” story

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Today, to help thaw you poor Americans out of that Arctic Vortex, we have a guest post bringing the heat, by my PhD student Sophie Regnault! This relates to some old posts about rhinos, which are a mainstay here at the WIJF blog- I’ve posted a lot about the rhino extinction crisisfeet, skin, big and bigger bones, and more, but this is our first rhinoceros-focused, actual published scientific paper! Take it away, Sophie! (We’re planning a few more “guest” blog posts from my team, so enjoy it, folks!)

Almost a year ago to the day, I submitted my first paper written with John Hutchinson and Renate Weller at the RVC and it has (finally!) just been published. To celebrate, I have been allowed to temporarily hijack ‘What’s in John’s Freezer?’ for my first foray into the world of blogging. I started the paper back as an undergraduate veterinary student. It was my first experience of proper research, and so enjoyable that I’m now doing a PhD, studying sesamoid bones like the patella!

We wanted to discover more about the types of bony disease rhinos get in their feet, of which there isn’t much known. Rhinos, of course, are big, potentially dangerous animals – difficult enough to examine and doubly difficult to x-ray clearly because of their thick skin. Unlike diseases which are fairly easy to spot (like abscesses or splitting of the nails and footpad), there is hardly anything out there in the scientific literature on bony diseases in rhino feet. It’s no small issue, either. When your feet each need to support over 900kg (typical for a large white rhino), even a relatively minor problem can be a major pain. Progressing unseen under their tough hide, lesions in the bone can eventually become so serious than the only solution is euthanasia, but even mild conditions can have negative consequences. For example, foot problems in other animals are known to have knock-on effects on fertility, which would be a big deal for programs trying to breed these species in captivity.

Hidden treasures abound!

Hidden treasures abound! (Photos can be clicked to embiggen)

Data gathering was a blast. I got to travel to Cambridge, Oxford, and London during one of England’s better summers, and these beautiful old museums were letting me snoop around their skeleton collections. I’d been there often as a visitor, but it was anatomy-nerd-heaven to go behind the scenes at the Natural History Museum, and to be left alone with drawers and drawers of fantastic old bones. Some of the specimens hadn’t been touched for decades – at Cambridge University Museum of Zoology, we opened an old biscuit tin filled with the smallest rhinoceros foot bones, only to realise they were wrapped in perfectly preserved 1940’s wartime Britain newspaper.

rhino-feet (2)

rhino-feet (4)

rhino-feet (3)

Osteomyelitis… (3 clickable pics above) the toe’s probably not meant to come off like that!

In addition to my museum studies, I had another fun opportunity to do hands-on research.  John (of course!) had freezers full of rhino legs (looking disconcertingly like doner kebabs, but maybe that’s just me!), which we CT scanned to see the bones. Although it is a pretty standard imaging technique, at this point I had only just started my clinical studies at the vet hospital, and being able to flick through CT scans felt super badass. Most vet students just get to see some horse feet or dog/cat scans, at best.

Another osteomyelitis fracture, visible in a CT scan.

Another osteomyelitis fracture, visible in a CT scan reconstruction.

We expected to find diseases like osteoarthritis (a degenerative joint disease) and osteomyelitis (bone infection and inflammation). Both had previously been reported in rhinoceroses, although it was interesting that we saw three cases of osteomyelitis in only 27 rhinos, perhaps making it a fairly common complication. It’s an ugly-looking disease, and in two of the cases led to the fat, fluffy bones fracturing apart.

We also had several unexpected findings, like flakes of fractured bone, mild dislocations, tons of enthesiophytes (bone depositions at tendon/ligament attachments) and lots of holes in the bones (usually small, occasionally massive). For me, writing up some of these findings was cool and freaky paranoid in equal measures. They hadn’t been much described before, and we were unsure of their significance. Was it normal, or pathological? Were we interpreting it correctly? Discussions with John and Renate (often involving cake) were reassuring, as was the realisation that in science (unlike vet school at the time, where every question seemed to have a concrete answer) you can never be 100% sure of things. Our study has a few important limitations, but has addressed a gap in the field and found some neat new things. Six months into my PhD, I’m enjoying research more than ever, and hoping that this paper will be the first of many (though I promise I won’t keep nicking John’s blog for my own shameless self-promotion if that happens!  EDIT BY JOHN: Please do!).

Nasty osteoarthritis wearing away the bone at the joint surface. Most cases occurred in the most distal joint.

Nasty osteoarthritis wearing away the bone at the joint surface. Most cases occurred in the most distal joint.

Deep holes in some of the bones: infection, injury?

Deep holes in some of the bones: infection, injury?

The paper:
Sophie Regnault, Robert Hermes, Thomas Hildebrandt, John Hutchinson, and Renate Weller (2013) OSTEOPATHOLOGY IN THE FEET OF RHINOCEROSES: LESION TYPE AND DISTRIBUTION. Journal of Zoo and Wildlife Medicine: December 2013, Vol. 44, No. 4, pp. 918-927.

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Models of a basal dinosaur and bird, showing methods and key differences in body shape.

Our 3D computer models of a basal dinosaur and bird, showing methods and key differences in body shape. The numbers at the bottom are museum specimen numbers.

At about the moment I’m posting this, our Nature paper (our more formal page here, and the actual article here) embargo is ending, drawing a 14+ year gestation to a close. The paper is about how dinosaur 3D body shape changed during their evolution, and how that relates to changes in hindlimb posture from early dinosaurs/archosaurs to birds; “morpho-functional evolution” sums up the topic. We used the 3D whole-body computational modelling that I, Allen and Bates (among others) have developed to estimate evolutionary changes in body dimensions, rather than focusing on single specimens or (as in our last study) tyrannosaur ontogeny. We’ve strongly supported the notion (dating back to Gatesy’s seminal 1990 Paleobiology paper) that the centre of mass of dinosaurs shifted forwards during their evolution, and that this shift gradually led to the more crouched (flexed) hind leg posture that characterizes living birds. Here is a movie from our paper showing how we did the modelling:

And here is a summary of our 17 computer models of archosaur bodies, shown as one walks along the tips of the phylogeny shown in the video (the models are not considered to be ancestral to one another; we used a common computer algorithm called squared-change parsimony to estimate ancestral state changes of body dimensions between the 16 numbered nodes of the tree):

But we’ve done much more than just put numbers on conventional wisdom.

We’ve shown, to our own surprise, that the shift of the centre of mass was largely driven by evolutionary enlargements of the forelimbs (and the head and neck, and hindlimbs, to a less strong degree), not the tail as everyone including ourselves has assumed for almost 25 years. And the timing of this shift occurred inside the theropod dinosaur group that is called Maniraptora (or Maniraptoriformes, a slightly larger group), so the change began in animals that were not flying, but not long before flight evolved (depending on whom you ask, what taxonomy they favour and what evidence one accepts, either the smaller clade Eumaniraptora/Paraves or the bird clade Aves/Avialae).

Now, if you don’t like the cliche “rewriting the textbooks”, do have a look through texts on dinosaur/early avian palaeobiology and you probably will find a discussion of how the tail shortened, the centre of mass moved forwards as a consequence, the caudofemoral musculature diminished, and theropod dinosaurs (including birds) became more crouched as a result. We did that to confirm for ourselves that it’s a pretty well-accepted idea. Our study supports a large proportion of that idea’s reasoning, but modifies the emphasis to be on the forelimbs more than the tail for centre of mass effects, so the story gets more complex. The inference about caudofemoral muscles still seems quite sound, however, as is the general trend of increased limb crouching, but out paper approximates the timing of those changes.

Figure 3 from our paper, showing how the centre of mass moved forwards (up the y-axis) as one moves toward living birds (node 16); the funny dip at the end is an anomaly we discuss in the paper.

Figure 3 from our paper, showing how the centre of mass moved forwards (up the y-axis) as one moves toward living birds (node 16); the funny dip at the end is an anomaly we discuss in the paper.

A final implication of our study is that, because the forelimbs’ size influenced the centre of mass position, and thus influenced the ways the hindlimbs functioned, the forelimbs and hindlimbs are more coupled (via their effects on the centre of mass) than anyone has typically considered. Thus bipedalism and flight in theropods still have some functional coupling– although this is a matter of degree and not black/white, so by no means should we do away with helpful concepts like locomotor modules.

And in addition to doing science that we feel is good, we’ve gone the extra mile and presented all our data (yes, 17 dinosaurs’ worth of 3D whole body graphics!) and the critical software tools needed to replicate our analysis, in the Dryad database (link now working!), which should have now gone live with the paper! It was my first time using that database and it was incredibly easy (about 1 hour of work once we had all the final analysis’s files properly organized)– I strongly recommend others to try it out.

That’s my usual general summary of the paper, but that’s not what this blog article is about. I’ll provide my usual set of links to media coverage of the paper below, too. But the focus here is on the story behind the paper, to put a more personal spin on what it means to me (and my coauthors too). I’ll take a historical approach to explain how the paper evolved.


This paper’s story, with bits from the story of my life:

Embarassing picture of me before I became a scientist. Hardee's fast food restaurant cashier, my first "real job."

Embarassing picture of me before I became a scientist. Hardee’s fast food restaurant cashier, my first “real job”, from ~1999- no, wait, more like 1986. The 1980s-style feathered (and non-receding) hair gives it away!

Rewind to 1995. I started my PhD at Berkeley. I planned to use biomechanical methods and evidence to reconstruct how Tyrannosaurus rex moved, and started by synthesizing evidence on the anatomy and evolution of the hindlimb musculature in the whole archosaur group, with a focus on the lineage leading to Tyrannosaurus and to living birds. As my PhD project evolved, I became more interested and experienced in using 3D computational tools in biomechanics, which was my ultimate aim for T. rex.

In 1999, Don Henderson published his mathematical slicing approach to compute 3D body dimensions in extinct animals, which was a huge leap for the field forward beyond statistical estimates or physical toy models, because it represented dinosaurs-as-dinosaurs (not extrapolated reptiles/mammals/whatever) and gave you much more information than just body mass, with a lot of potential to do sensitivity analysis.

I struggled to upgrade my computer skills over the intervening years. I was developing the idea to reconstruct not only the biomechanics of T. rex, but also the evolutionary changes of biomechanics along the whole archosaur lineage to birds– because with a series of models of different species and a working phylogeny, you could do that. To me this was far more interesting than the morphology or function of any one taxon, BUT required you to be able to assess the latter. So Tyrannosaurus became a “case study” for me in how to reconstruct form and function in extinct animals, because it was interesting in its own right (mainly because of its giant size and bipedalism). (Much later, in 2007, I finally finished a collaboration to develop our own software package to do this 3D modelling, with Victor Ng-Thow-Hing and F. Clay Anderson at Honda and Stanford)

Me and a Mystery Scientist (then an undergrad; now a successful palaeontologist), measuring up a successful Cretaceous hypercarnivore at the UCMP; from my PhD days at Berkeley, ~2000 or so.

Me and a Mystery Scientist (then an undergrad; now a very successful palaeontologist!), measuring up a successful Cretaceous hypercarnivore at the UCMP; from my PhD days at Berkeley, ~2000 or so.

In all this research, I was inspired by not only my thesis committee and others at Berkeley, but also to a HUGE degree by Steve Gatesy, a very influential mentor and role model at Brown University. I owe a lot to him, and in a sense this paper is an homage to his trailblazing research; particularly his 1990 Paleobiology paper.

In 2001, I got the NSF bioinformatics postdoc I badly wanted, to go to the Neuromuscular Biomechanics lab at Stanford and learn the very latest 3D computational methods in biomechanics from Prof. Scott Delp’s team. This was a pivotal moment in my career; I became partly-an-engineer from that experience, and published some papers that I still look back fondly upon. Those papers, and many since (focused on validating and testing the accuracy/reliability of computer models of dinosaurs), set the stage for the present paper, which is one of the ones I’ve dreamed to do since the 1990s. So you may understand my excitement here…

Stanford's Neuromuscular Biomechanics Lab, just before I left in 2003.

Stanford’s Neuromuscular Biomechanics Lab, just before I left in 2003.

But the new paper is a team effort, and was driven by a very talented and fun then-PhD-student, now postdoc, Dr Vivian Allen. Viv’s PhD (2005-2009ish) was essentially intended to do all the things in biomechanics/evolution that I had run out of time/expertise to do in my PhD and postdoc, in regards to the evolution of dinosaur (especially theropod) locomotor biomechanics. And as I’d hoped, Viv put his own unique spin on the project, proving himself far better than me at writing software code and working with 3D graphics and biomechanical models. He’s now everything that I had hoped I’d become by the end of my postdoc, but didn’t really achieve, and more than that, too. So huge credit goes to Viv for this paper; it would never have happened without him.

We also got Karl Bates, another proven biomechanics/modelling expert, to contribute diverse ideas and data. Furthermore, Zhiheng Li (now at UT-Austin doing a PhD with Dr Julia Clarke) brought some awesome fossil birds (Pengornis and Yixianornis) from the IVPP in Beijing in order to microCT scan them in Londo. Zhiheng thus earned coauthorship on the paper — and I give big thanks to the Royal Society for funding this as an International Joint Project, with Dr Zhonghe Zhou at the IVPP.

That’s the team and the background, and I’ve already given you the punchlines for the paper; these are the primitive and the derived states of the paper. The rest of this post is about what happened behind the scenes. No huge drama or anything, but hard, cautious work and perseverance.

Me shortly after I moved to the RVC; video still frame from a dinosaur exhibit I was featured in. Embarassingly goofy pic, but I like the blurb at the bottom. It's all about the evolutionary polarity, baby!

Me shortly after I moved to the RVC; video still frame from a dinosaur exhibit (c. 2004) I was featured in. Embarassingly goofy pic, but I like the blurb at the bottom. It’s all about the evolutionary polarity, baby!

The paper of course got started during Viv’s PhD thesis; it was one of his chapters. However, back then it was just a focus on how the centre of mass changed, and the results for those simple patterns weren’t very different from those we present in the paper. We did spot, as our Nature supplementary information notes,  a strange trend in early theropods (like Dilophosaurus; to a lesser degree Coelophysis too) related to some unusual traits (e.g. a long torso) and suggested that there was a forward shift of centre of mass in these animals, but that wasn’t strongly upheld as we began to write the Nature paper.

On the urging of the PhD exam committee (and later the paper reviewers, too), Viv looked at the contributions of segment (i.e. head, neck, trunk, limbs, tail) mass and centre of mass to the overall whole body centre of mass. And I’m glad he did, since that uncovered the trend we did not expect to find: that the forelimb masses were far more important for moving the centre of mass forwards than the mass (or centre of mass) of the tail was– in other words, the statistical correlation of forelimb mass and centre of mass was strong, whereas changes of tail size didn’t correlate with the centre of mass nearly as much. We scrutinized those results quite carefully, even finding a very annoying bug in the 3D graphics files that required a major re-analysis during peer review (delaying the paper by ~6 months).

The paper was submitted to Nature first, passing a presubmission inquiry to check if the editor felt it fit the journal well enough. We had 3 anonymous peer reviewers; 1 gave extensive, detailed comments in the 3 rounds of review and was very fair and constructive, 1 gave helpful comments on writing style and other aspects of presentation as well as elements of the science, and 1 wasn’t that impressed by the paper’s novelty but wanted lots more species added, to investigate changes within different lineages of maniraptorans (e.g. therizinosaurs, oviraptorosaurs). That third reviewer only reviewed the paper for the first round (AFAIK), so I guess we won them over or else the editor overruled their concerns. We argued that 17 taxa were probably good enough to get the general evolutionary trends that we were after, and that number was ~16 more species than any prior studies had really done.

Above: CT scan reconstruction of the early extinct bird Yixianornis in slab conformation, and then Below: 3D skeletal reconstruction by Julia Molnar, missing just the final head (I find this very funny; Daffy Duck-esque) which we scaled to the fossil’s dimensions from the better data in our Archaeopteryx images. Yixianornis reconstruction There is also the concern, which the reviewers didn’t focus on but I could see other colleagues worrying about, that some of the specimens we used were either composites, sculpted, or otherwise not based on 100% complete, perfectly intact specimens. The latter are hard to come by for a diversity of extinct animals, especially in the maniraptoran/early bird group. We discussed some of these problems in our 3D Tyrannosaurus paper. The early dinosauromorph Marasuchus that we used was a cast/sculpted NHMUK specimen based on original material, as was our Coelophysis, Microraptor and Archaeopteryx; and our Carnegie ??Caenagnathus?? specimen was based more on measurements from 1 specimen than from direct scans, and there were a few other issues with our other specimens, all detailed in our paper’s Supplementary Information.

But our intuition, based on a lot of time spent with these models and the analysis of their data, is that these anatomical imperfections matter far, far less than the statistical methods that we employed– because we add a lot of flesh (like real animals have!) outside of the skeleton in our method, the precise morphology of the skeleton doesn’t matter much. It’s not like you need the kind of quality of anatomical detail that you need to do systematic analyses or osteological descriptive papers. The broad dimensions can matter, but those tend to be covered by the (overly, we suspect) broad error bars that our study had (see graph above). Hence while anyone could quibble ad infinitum about the accuracy of our skeletal data, I doubt it’s that bad– and it’s still a huge leap beyond previous studies, which did not present quantitative data, did not do comparative studies of multiple species, or did not construct models based on actual 3D skeletons as opposed to artists’ 2D shrinkwrapped reconstructions (the “Greg Paul method”). We also did directly measure the bodies of two extant archosaurs in our paper: a freshwater crocodile and a junglefowl (CT scan of the latter is reconstructed below in 3D).

One thing we still need to do, in future studies, is to look more carefully inside of the bird clade (Aves/Avialae) to see what’s going on there, especially as one moves closer to the crown group (modern birds). We represented modern birds with simply 1 bird: the “wild-type chicken” Red junglefowl, which isn’t drastically different in body shape from other basal modern birds such as a tinamou. Our paper was not about how diversity of body shape and centre of mass evolved within modern birds. But inspecting trends within Palaeognathae would be super interesting, because a lot of locomotor, size and body shape changes evolved therein; ostriches are probably a very, very poor proxy for the size and shape of the most recent common ancestor of all extant birds, for example, even though they seem to be fairly basal within that whole lineage. And, naturally, our study opens up opportunities for anyone to add feathers to our models and investigate aerodynamics, or to apply our methods to other dinosaur/vertebrate/metazoan groups. If the funding gods are kind to us, later this year we will be looking more closely, in particular, at the base of Archosauria and what was happening to locomotor mechanics in Triassic archosaurs…

Clickum to embiggum:

Australian freshwater crocodile, Crocodylus johnstoni; we CT scanned it in 3 pieces.

Australian freshwater crocodile, Crocodylus johnstoni; we CT scanned it in 3 pieces while visiting the Witmer lab in Ohio.

A Red junglefowl cockerel, spotted in Lampang, Thailand during one of my elephant gait research excursions there. Svelte, muscular and fast as hell.

A Red junglefowl cockerel, spotted in Lampang, Thailand during one of my elephant gait research excursions there. Svelte, muscular and fast as hell. This photo is here to remind me to TAKE BLOODY PICTURES OF MY ACTUAL RESEARCH SPECIMENS SO I CAN SHOW THEM!

I’d bore you with the statistical intricacies of the paper, but that’s not very fun and it’s not the style of this blog, which is not called “What’s in John’s Software Code?”. Viv really worked his butt off to get the stats right, and we did many rounds of revisions and checking together, in addition to consultations with statistics experts. So I feel we did a good job. See the paper if that kind of thing floats your boat. Someone could find a flaw or alternative method, and if that changed our major conclusions that would be a bummer– but that’s science. We took the plunge and put all of our data online, as noted above, so anyone can do that, and that optimizes the reproducibility of science.

What I hope people do, in particular, is to use the 3D graphics of our paper’s 17 specimen-based archosaur bodies for other things– new and original research, video games, animations, whatever. It has been very satisfying to finally, from fairly early in the paper-writing process onwards, present all of the complex data in an analysis like this so someone else can use it. My past modelling papers have not done this, but I aim to backtrack and bring them up to snuff like this. We couldn’t publish open access in Nature, but we achieved reasonably open data at least, and to me that’s as important. I am really excited at a personal level, and intrigued from a professional standpoint, to see how our data and tools get used. We’ll be posting refinements of our (Matlab software-based) tools, which we’re still finding ways to enhance, as we proceed with future research.

Velociraptor-model-min Dilophosaurus-model-min00

Above: Two of the 17 archosaur 3D models (the skinny “mininal” models; shrinkwrapped for your protection) that you can download and examine and do stuff with! Dilophosaurus on the left; Velociraptor on the right. Maybe you can use these to make a Jurassic Park 4 film that is better, or at least more scientifically accurate, than Hollywood’s version! ;-) Just download free software like Meshlab, drop the OBJ files in and go!

Now, to bring the story full circle, the paper is out at last! A 4 year journey from Viv’s PhD thesis to the journal, and for me a ~14 year journey from my mind’s eye to realization. Phew! The real fun begins now, as we see how the paper is received! I hope you like it, and if you work in this area I hope you like the big dataset that comes with it, too. Perhaps more than any other paper I’ve written, because of the long voyage this paper has taken, it has a special place in my heart. I’m proud of it and the work our team did together to produce it. Now it is also yours. And all 3200ish words of this lengthy blog post are, as well!

Last but not least, enjoy the wonderful digital painting that Luis Rey did for this paper (another of my team’s many failed attempts to get on the cover of a journal!); he has now blogged about it, too!

Dinosaur posture and body shape evolving up the evolutionary tree, with example taxa depicted.

Dinosaur posture and body shape evolving up the evolutionary tree, with example taxa depicted. By Luis Rey.


News stories about this paper will be added below as they come out, featuring our favourites:

1) NERC’s Planet Earth, by Harriet Jarlett: “Dinosaur body shape changed the way birds stand

2) Ed Yong on Phenomena: “Crouching  bird, hidden dinosaur

3) Charles Choi on Live Science: “Crouching bird, hidden evolutionary purpose?

4) Brian Handwerk on Nat Geo Daily News: “Birds’ “Crouching” Gait Born in Dinosaur Ancestors

5) Jennifer Viegas on Discovery News: “Heavier dino arms led evolution to birds

6) Puneet Kollipara on Science News: “Birds may have had to crouch before they could fly

And some superb videos- we’re really happy with these:

1) Nature’s “Crouching Turkey, Hidden Dragon

2) Reuters TV’s “3D study shows forelimb enlargement key to evolution of dinosaurs into birds

Synopsis: Decent coverage, but negligible coverage in the general press; just science-specialist media, more or less. I think the story was judged to be too complex/esoteric for the general public. You’d think dinosaurs, evolution, computers plus physics would be an “easy sell” but it was not, and I don’t think we made any big errors “selling” it. Interesting– I continue to learn more about how unpredictable the media can be.

Regardless, the paper has had a great response from scientist colleagues/science afficionados, which was the target audience anyway. I’m very pleased with it, too– it’s one of my team’s best papers in my ~18 year career.

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frontcover

The Unfeathered Bird book by Katrina van Grouw proclaims immediately in its Introduction that it “is not an anatomy of birds.”  True– it is far more than that, and it would be a shame if it had just been a dry, technical avian osteology reference book. It is a unique blend of art and science- particularly avian anatomy, evolution, taxonomy, natural history and more. The Unfeathered Bird is written for a general audience; birders/twitchers or just natural history buffs would be ideal targets of its unfettered passion for all things avian. A 12-year-old who is very keen on animals could enjoy it, and it may ignite the flames of ornithological excitement in many young or older readers. I am glad it was not called “The Naked Bird” as that would have caused some serious misconceptions (badum-tish!). The book is dripping with illustrations (at least one every two pages, often more). Almost all of the illustrations (except some paintings in the style of the cover) are in the same brownish sketch style that, like much of the book, evokes a bygone era of dark wooden cabinets and shadowed halls packed with skeletons, with nary an interactive graphics display, animatronic dinosaur or hyperdetailed cladogram in sight. It feels like an homage to the Victorian naturalists’ joy for anatomical detail conveyed through painstakingly detailed woodcuts. And while many still think of feathers as “the defining feature of birds,” enough about feathers already. Seriously. This is a book is about what lies beneath, and how all that non-fluffy stuff is important for birds’ lives, too.

(image-intense post; all can be clicked to embiggritate)

Katrina with peacock feather headdress? (back cover pic and rear view of same skeleton)

Katrina with peacock feather headdress? (back cover pic and rear view of same skeleton)

Katrina with front cover framed pic and the peacock skeleton that went with it.

Katrina with front cover framed pic and the peacock skeleton that went with it.

The Introduction continues to explain that the book is truly about how the external anatomy of birds is linked to the bony anatomy, which might remind astute readers of modern approaches like the extant phylogenetic bracket. The rest of the book uses both skeletal and unfeathered, quasi-myological illustrations to get this point across vividly. The explanatory text is written at a basic enough level for the average reader and is just the right length, with interesting anecdotes and natural history facts that even the expert reader will find interesting or even inspirational (e.g. possibly a goldmine for research ideas). First there is a 26 page “Basic” section with an introduction to avian osteology, with bountiful sketches to illustrate key organs and text explaining how it all fits together in the fully accoutered bird. The decision to use classical Linnean taxonomy (defunct or re-arranged taxa from the Systema Naturae like Accipitres, Picae, Anseres, Grallae, Gallinae and Passeres; which are the six “Specific” chapters in the second section of the book) was a good one- it enhances the classical feel of the tome and gives the author a great opportunity to discuss convergent evolution and how that misled past ornithologists.

But for me, the book is most pleasurable for the visualizations and the passion for all things birdy that weaves through them and the accompanying text. The removal of feathers, or even all soft tissues, from bird bodies (posed in naturalistic behaviours) that van Grouw renders in her illustrations shows birds in a new light, emphasizing the strangeness and diversity that lie beneath. The author begins the book with a touching Acknowledgments section in which her husband Hein van Grouw, curator of birds at the Natural History Museum’s Tring collection, features very prominently, making it clear that the book was a team operation and comes from the heart after a 25-year journey. This gives the book a special warmth that is preserved throughout the remainder- although the illustrations are of flayed bodies or boiled / beetle-macerated skeletons, the tone is nothing less than an earnest love for birds of all kinds, and a zest for portraying those feelings to the reader in sketches and prose. It is a joyous celebration, not a somber litany, of the wonder of birds that can be gleaned from dead bodies. There is so much powerful, awesome imagery stuffed into those pages that it is hard to summarize. I’ll let five of my favourite images from the book (more are in her gallery and her book’s Facebook page; but even these are just the tip of the icebird) help get this across (used with permission of the author):

Naked kiwi in action.

Naked kiwi in action.

The unscaled bird: guineafowl feet.

The unscaled bird: guineafowl feet.

Deplumed sparrowhawk with dove trophy, exalting in its triumph.

Deplumed sparrowhawk with dove trophy, exalting in its triumph.

Budgerigar has made a friend? Or came to grips with its own mortality?

Budgerigar has made a friend? Or came to grips with its own mortality?

Trumpet Manucode WTF anatomy! Spiraling tracheal coil made me gasp in awe when I saw this image in the book.

Trumpet Manucode’s WTF anatomy! Spiraling tracheal coil made me gasp in awe when I saw this image in the book.

Now I’ll depart from this post just being a book review. I went to the Tring collection to do some research, and arranged my trip so I’d also get to see the debut of a Tring special exhibit featuring The Unfeathered Bird, and also to meet Katrina as well as Hein van Grouw. The placement of the exhibit at Tring is apropos, because Katrina was a curator at the museum until a few years ago and Hein still is. But the inspiration for the work and the specimens used (with a few exceptions, including from other museums) are Katrina’s. She (with Hein’s help) procured bodies of birds to dissect, macerate and sketch for the book over its 25 year fledging period, noting in the Acknowledgments that “no birds were harmed” to do this– do read those acknowledgments, as there are some amusing tales there of how she obtained some specimens.

I was fortunate to be able to take some photos of the exhibit while they set it up, and grabbed some candid images of Katrina and colleagues during that process. The following images show off the exhibit, which is all in one clean, bright, simply adorned room in the Tring that lets Katrina’s framed sketches be the focus. Here are some examples:

Poster advert for the book in the Tring collections.

Poster advert for the book in the Tring collections.

Tring exhibit setup, with Katrina, husband Hein, and helper finishing it up.

Tring exhibit setup, with Katrina, husband Hein, and helper finishing it up.

Tring exhibit now ready.

Tring exhibit now ready.

Tring exhibit case.

Tring exhibit case.

Framed sketches at Tring exhibit.

Framed sketches at Tring exhibit.

Framed sketches at Tring exhibit.

More framed sketches at Tring exhibit.

The exhibit is fun for people who are already Unfeathered Bird fans, and a good way of drawing in new ones. The book is a precious thing that any fan of birds, especially scientists, really needs to have a hard copy of. While it claims not to be an anatomy text, its illustrations provide ample opportunities to use it for that purpose. But really the point of owning all 287-plus pages is to bask in the warmth of true, pure appreciation for classic ornithology, which I found infectious. It is a book by and for bird lovers, but also for those that find the interface of art and science to be fascinating.

I confess I used to hate birds. I found them annoying and boring; all that flitting and twitting and pretentious feathers. “Get over yourselves, already, and calm down too!” was my reaction to them. When I started grad school, I had an open disdain for birds, even moreso than for mammals (OK, except cats). I was a “herp” fan through and through, for most of my life (childhood spent catching anoles in Florida, or stalking frogs in Ohio; during visits to my grandparents). What won me over was studying birds (and eventually mammals, too) as a young scientist, and learning how incredible they are– not just as endpoints in the story of theropod dinosaur evolution, as my thesis focused on, but as amazing animals with spectacular form-function relationships.  The Unfeathered Bird is saturated with that amazement, so we’re birds of an unfeather.

Framed sketch of dodo head at Tring exhibit.

Framed sketch of dodo head at Tring exhibit.

Entirely unfeathered Indian peafowl in matching views.

Entirely unfeathered Indian peafowl in matching views.

Painted Stork and Toco Toucan sketches.

Painted Stork and Great Hornbill sketches.

Red junglefowl, wild ancestor of domestic chickens (and the book ends with several such breeds illustrated),

Red junglefowl, wild ancestor of domestic chickens (and the book ends with several such breeds illustrated).

Katrina told me that she is already deep into writing the next book, whose subject I won’t spoil for you here but maybe we will be lucky enough to have her appear in the Comments and plug it? :) (Her website does say “It was Hein’s stroke of genius to include domestic birds and they’ve provided the inspiration for my next project.” so the cat is out of the bag and amongst the pigeons!) It is great to hear that the book has done quite well sales-wise and critically, such as ~#67 on the Amazon sales list at one point– I hope this paves the way for more such books not only from Katrina, but from others engaged in lateral thinking (and still others) on the boundaries of science-art.

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If you want to see a new/reinvigorated, exciting direction that palaeoart is headed, check out the All Yesterdays book by Conway, Kosemen and Naish. This review is fully cognizant that I’m late to the party of hailing this book as part of a palaeoart renaissance. I confess I haven’t read any of the many reviews of this book; I just know it is highly regarded and popular, from excitement on social media sites I frequent. So if my review covers ground others have too, so be it; it’s purely my own thoughts but I expect that mine fall in line with many others’. I’m reviewing the book on this blog because I love the interface between science and art (which is very important in anatomy), and because anatomy, and how one infers it when it is unknown, is the fundamental theme of the book.

You can buy All Yesterdays for around £18 (ASIDE: oddly, used copies (“May not include CD, access code, or DJ”– ???) are around £42 on the same site; perhaps those are artist-signed??? I have no idea!). It is a good deal at that price. While you’re at it, get “Dinosaur Art: The World’s Best Paleoart” by White et al. (including Conway) for a similar price. My review will return to some comparisons between these two books, released just a few months apart.

All-Yesterdays-coverworlds-greatest-paleoart

All Yesterdays is about not only how we reconstruct dinosaurs and other prehistoric animals, but also about thinking outside-the-box in the ways we reconstruct them and thereby bucking some recent clichés and tropes. Some of those outside-the-box ideas might seem ludicrous, and some probably are. But one of the main points of All Yesterdays is that there is plenty about extinct animals, and even living animals, that we don’t know, even though the field of paleoart has matured into greater scientific rigor than in the days of Knight, Zallinger and others (1920s-1950s). There is a focus on uncertainties about integument (e.g. feathering, spines, colour/patterning, body contours) and behaviour (e.g. avoiding stereotypes like perpetually aggressive predators and frightened prey animals– amen to that!). And the capstone of the book, which in some ways I loved the most, is turning the issue on its head and pretending that we only had skeletons of extant animals, then proceeding to reconstruct those animals (elephants, whales, horses and swans stand out prominently in this section; some of these are shown below). I wish more scientists in my general area would practice this; e.g. validation of a methodology used to reconstruct extinct animals in science.

The ‘speculative zoology’ of All Yesterdays deserves favourable comparison to one of my favourite science-art books, 1981’s After Man by Dougal Dixon. I fell so in love with that book as a 10-year-old that I wouldn’t let my parents return it to the library and I made them pay the hefty lost-book-fee (yes, I was a little bastard!). I still have it, too. (Sorry, Sequoya Branch Public Library of Madison, WI!) Likewise, the whimsy of the Rhinogrades is evoked by this work, and of course Tetrapod Zoology blog readers will be no strangers to it, either.

The book begins with a clear, succinct (7 page) summary of the history and science of reconstructing animals, with a focus on paleoart’s approach rather than science’s. I would have found it interesting (but space constraints presumably precluded) to feature more of the interface/parallels with scientists at the same time, such as the careful reconstructions of musculature in A.S. Romer’s masterful work in the 1920s (e.g. below), or later efforts by palaeontologists like Alick Walker and Walter Coombs. Many of these luminaries sought not to reconstruct animals for artistic purposes, but for almost purely scientific ones: to understand what skeletal anatomy meant in terms of broader biology (e.g. comparative anatomy) and phylogeny (e.g. origin of birds or archosaur evolution). The quality of their own artistic representations as well as scientific interpretations varied a lot. Indeed, sometimes the choice of model organisms (crocodile for Romer; lizard for Walker; birds in the post-1960’s) reveals much about the author’s preconceptions about phylogeny, marshalled towards a favoured hypothesis (e.g. a crocodile origin of birds for Walker; or an avian origin amongst dinosaurs for Bakker, Paul and others), rather than a circumspect assessment of all relevant evidence.

Romer1923-fig6

Figure 6 from Romer, 1923; very crocodylian T. rex right hindlimb muscles.

But eventually the “model organism” approach to reconstructing extinct animals gave way to the extant phylogenetic bracket; very popular today; which itself is an adaptation of the outgroup method for polarity assessment in phylogenetic systematics (cladistics). I am sure many modern paleoartists explicitly consider the “EPB” in their reconstructions, although this leaves many ambiguities (e.g. integument of crocodiles and birds being totally different!) that they must overcome, whereas scientists might just give up. This interface of art and science is part of what make palaeontology so enjoyable.

The EPB mindset has been a big step forward for evolutionary morphology and palaeontology, but still some of the greatest questions (e.g. what were the actual sizes, colour patterns, or behaviours of extinct animals? How did novelties arise and which novelties did dinosaurs have that extant relatives lack?) are left ambiguous by the EPB. This is because either the EPB itself is ambiguous (crocodiles or other taxa do one thing; birds do something altogether different), or because features leave no osteological correlates (e.g. muscle/tendon/ligament scars) on fossils that can be compared with the EPB.  This quandary leads to the fun side of this book– filling in the huge gaps left by both basic anatomical interpretation and the restrictions imposed by the EPB, and then playing with the frontiers of anatomical, behavioural and ecological reconstruction, using informed speculation.

The extant phylogenetic bracket for archosaurs.

The extant phylogenetic bracket for archosaurs.

In addition to the startling, bizarre “All Todays” reconstructions at the end of the book, the highlights for me were the camouflaged Majungasaurus and plesiosaur, the “feathered mountain” (below) of a therizinosaur (can anyone illustrate a plausible therizinosaur and make it normal and boring? I wager not!) and the neck-swinging elasmosaurs engaged in “honest signalling” of their fitness. Many of the illustrations riff on notions popular in the modern palaeo-zeitgeist (and subject of many conversations at conferences, or even publications), such as evidence for the spiny integument of some ornithischians, fat ornithopods, Microraptor of somewhat-known-colouration, and so on. But plenty of other images riff on a “well why not?” theme, challenging the viewer to consider that extinct animals could have many surprises left in store for us with future discoveries, or else plausible features that we’ll never know of but might seem laughable or unfashionable to illustrate now. Each image has text explaining the logic behind it- this is not just a montage of pictures. This is a thinking person’s book- you should buy it for rumination, to challenge your preconceptions, not to have a flashy coffee table book. It’s not eye candy — it’s more like brain jerky.

John Conway's mountain-of-feathers therizinosaurs: eerily beautiful.

John Conway‘s mountain-of-feathers therizinosaurs: eerily beautiful.

I think this is a bold, fun (re)new(ed) direction for palaeoart. There’s always a place for rigorous, conservatively evidence-based, by-comparison-almost-uncreative scientific illustration of extinct organisms. The World’s Best Paleoart presents loads of this, often in vividly colourful, photo-realistic, lavish, glossy detail, whereas the approach in All Yesterdays tends toward a more soft, matte, informal style including sketches or abstractions, toning down the serious and intense (even cluttered?) approach that can characterize modern palaeoart, including The World’s Best Paleoart.  Sometimes those reconstructing life of the past (scientists included!) may emphasize that detailed realism too much and lose some of the joyful playfulness that palaeoart can revel in, at its best, most inspirational or thought-provoking. The former style might be considered the more “safe” or technical practice; the latter more risky or unconstrained.

Memo Kosemen's "All Todays" swans, with tadpolefish, might haunt your nightmares.

C.M. Kosemen‘s “All Todays” swans, with tadpolefish, might haunt your nightmares.

I’m not casting negative judgement on either style; both are absolutely wonderful — and valuable. I love both books! I’m glad we’re in a new age where the fun is waltzing back into palaeoart, that’s all. All Yesterdays doesn’t just waltz, either. It pounces into your field of view, wiggles its rainbow-coloured, mandrill-esque ankylosaurid bottom at you with a cheeky grin, and proceeds to make you smirk, be bemused, and even gasp at its adventurousness in rapid succession as you turn its pages. At 100 pages it doesn’t overstay its welcome either– that kaleidoscopic thyreophoran rump cartwheels off into the sunset at an opportune moment.

You won't forget Memo Kosemen's "All Todays" elephant.

You won’t forget C.M. Kosemen‘s “All Todays” elephant.

If All Yesterdays makes someone uncomfortable with its swashbucklerish daring, they’re probably taking palaeontology way too seriously– and maybe missing not only some good fun, but also some potential truths. Dogma is a terrible thing, and All Yesterdays slaughters it with delightful relish. Bring on the next installment! If you have  All Yesterdays too, what’s your favourite part? Or if you don’t have it, I’d be happy to answer queries in the Comments.

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To kick off the New Year just right, our tetrapod team has a new paper in Nature, following up on last year’s Ichthyostega not-so-good-at-walking study (also see here). Yet this paper has a more anatomically descriptive — and also an “evo-devo” — twist to it. For brevity, I’ll let our press release tell the story, since I think it does a good job of it (like I always preach scientists should do, we worked with our PR company to write this together, so we’re happy with how the press release came out). In a nutshell, our study used some very fancy synchotron radiation techniques to image the 3D anatomy of the backbone in early land vertebrates. Our findings surprised even us, and ended up turning around palaeontology/comparative anatomy’s view of how the backbone evolved, giving us a new glimpse into our inner tetrapod.

Stick around for the videos at the end, which are the first four supplementary movies from the paper and are rather pretty (there are two more, for imaging/segmenting afficionados, but they are not as pretty or interesting for most of this blog’s readership). The final figure (Figure 1 from our paper) gives some extra visual context.

The paper is:

Pierce, S.E., Ahlberg, P.E., Hutchinson, J.R., Molnar, J.L., Sanchez, S., Tafforeau, P., Clack, J.A. 2013. Vertebral architecture in the earliest stem tetrapods. Nature, published online [here].

I should note that I’m just 3rd author, so I deserve only modest credit. But I helped. Even though no freezers were involved, or harmed, in the process.

Ichy_vertebrae_final_sm-01

Above image: Julia Molnar‘s illustration of Ichthyostega showing anatomical changes of its spine from front to back, with neural arch/spine in pink, twin pleurocentra in yellow, and intercentrum in green. These four parts, three kinds of bones, made up the backbone of the first land vertebrates. These parts evolved in different ways in later animals, but formed one main bone in all living lineages of vertebrates.

RVC PRESS RELEASE:

Scientists reassemble the backbone of life using a particle accelerator

Research published today (Sunday 13 January 2013) in the journal Nature documents, for the first time, the intricate three-dimensional structure of the backbone in the earliest four-legged animals (tetrapods).

The international team of scientists, led by Dr Stephanie E. Pierce from The Royal Veterinary College and Professor Jennifer A. Clack from the University of Cambridge, bombarded 360 million year old early tetrapod fossils with high energy synchrotron radiation. The resulting high resolution X-ray images allowed the researchers to reconstruct the backbones of the extinct animals in exceptional detail.

The backbone, also known as the spine or vertebral column, is a bony structure found in all tetrapods, along with other vertebrates such as fish. It is formed from many elements or vertebrae all connected in a row – from head to tail. Unlike the backbone of living tetrapods (e.g. humans), in which each vertebra is composed of only one bone, early tetrapods had vertebrae made up of multiple parts.

Lead author Dr Pierce says: “For more than 100 years, early tetrapods were thought to have vertebrae composed of three sets of bones – one bone in front, one on top, and a pair behind. But, by peering inside the fossils using synchrotron X-rays we have discovered that this traditional view literally got it back-to-front.”

For the analysis, the European Synchrotron Radiation Facility (ESRF) in France, where the three fossil fragments were scanned with X-rays, used a new protocol to reveal tiny details of the fossil bones buried deep inside the rock matrix.

Using this new technology, the team of scientists discovered that what was thought to be the first bone – known as the intercentrum – is actually the last in the series. And, although this might seem like a trivial oversight, this re-arrangement in vertebral structure has over-arching ramifications for the functional evolution of the tetrapod backbone. (see here for a now out-of-date image from Wikipedia)

Dr. Pierce explains: “By understanding how each of the bones fit together we can begin to explore the mobility of the spine and test how it may have transferred forces between the limbs during the early stages of land movement”.

But, the findings didn’t end there. One of the animals – known as Ichthyostega – was also found to have an assortment of hitherto unknown skeletal features including a string of bones extending down the middle of its chest.

Professor Clack says: “These chest bones turned out to be the earliest evolutionary attempt to produce a bony sternum.  Such a structure would have strengthened the ribcage of Ichthyostega, permitting it to support its body weight on its chest while moving about on land.”

This unexpected discovery supports recent work done by the same authors that showed Ichthyostega probably moved by dragging itself across flat ground using synchronous ‘crutching’ motions of its front legs – much like that of a mudskipper or seal.

Dr Pierce adds: “The results of this study force us to re-write the textbook on backbone evolution in the earliest limbed animals.”

The next step, the researchers say, is to understand how the backbone aided locomotion in these early tetrapods using sophisticated biomechanical analysis.

The study was funded by the Natural Environment Research Council.

Additional support was provided by the European Research Council and the ESRF, of which the Science and Technology Facilities Council (STFC) is the UK shareholder.

MOVIES:

These are rotating images of the anatomy, colour-coded, of the four species of early tetrapod that we examined for this study. Each shows the same basic pattern of having a “reverse rhachitomous” (pleurocentra in the front, intercentrum in the back; trying to think of a mullet joke…) anatomy. This is opposite the pattern that essentially all studies since famed evolutionary biologist/palaeontologist Edward Drinker Cope coined the term “rhachitomous” in 1878 have portrayed these and related animals as having. And this realization forces a re-examination of how the backbone structures first evolved in tetrapods and which parts (intercentra? pleurocentra? And where?) formed the spines of later animals.

For once, as authors we all felt that this finding really deserved the painfully hackneyed “rewrite the textbooks” label. It changes a lot of what we thought we knew about this classic evolutionary transition of anatomy. Check a vertebrate palaeontology/comparative anatomy textbook and you’ll likely find rhachitomous vertebrae and/or changes of pleurocentra vs. intercentra told in a way that we now are pretty sure is wrong.

You can also see the “sternebrae” (sternal elements; parts of the sternum that evolved independently in later land animals) in the first movie.  This, to my knowledge, is by far the oldest such evidence. I know of ossified sternal plates in Early Permian mesosaurs like Stereosternum, but nothing earlier although perhaps in some synapsid I don’t know, or a basal diapsid of some kind? Chime in in the comments if you know of something I missed. Regardless, the sternebrae in Ichthyostega have nothing to do directly with those convergently evolved in lissamphibians, lepidosaurs, synapsids and archosaurs, although there may be some parallel developmental mechanisms involved and at least similar dermal tissues recruited into ossification patterns. Even so, these sternebrae are further evidence of how that taxon, at least, was beginning to make forays onto land, as they’d have helped it to support its belly on land and breathe.

The segmented PPC-SRµCT of Ichthyostega stensioi MGUH VP 6115 spinning in yaw and roll.

The segmented PPC-SRµCT of Ichthyostega eigili MGUH VP 29017a spinning in yaw and roll.

The segmented PPC-SRµCT of Acanthostega gunnari MGUH f.n. 1227 spinning in yaw.

The segmented µCT of Pederpes finneyae GLAHMS 100815 spinning in yaw.

FIGURE:

Figure 1_Pierce et al

Above: (a,b) How we used to think the vertebrae were composed in early tetrapods like Ichthyostega. (c) How we found that Ichthyostega‘s posterior thoracic vertebrae actually tend to look. (d) Ichthyostega‘s anterior lumbar vertebral morphology. (e) Acanthostega according to Coates’s important description. (f) Our revision of the anatomy of Acanthostega (anterior dorsal). (g) Our new interpretation of Pederpes‘s morphology, from a posterior dorsal. Focus on the yellow vs. green elements. In a,b and e they are in different positions (reversed) compared with our new versions in c,d,f,g.

To put the above figure and movies into broader context, check this Wikipedia image. We think the red/pink bones (pleurocentra) are in the wrong place relative to the blue ones (intercentrum); the ones currently there in this image actually belong to the vertebral unit behind that one, so the pleurocentra should be moved to the front (left end) of each unit. But also look down toward the bottom of the figure. Some of those vertebrae may need to have their blue/pink bits re-examined and interpreted, too. Is it turtles intercentra all the way down?

There you have it! Welcome to your new, revised, irradiated, reverse-rhachitomous inner tetrapod’s vertebrae. Propagation phase-contrast X-ray synchrotron microtomography FTW!!!!

Science media articles arising from this study–

I like to keep track of media stories covering our research, using this blog, so here are some of the stories about this paper. It’s funny… this was one of the most broadly important papers I’ve ever been on, but the coverage was relatively scant. It was too technical. We knew that would be a problem, and really had a hard time putting into words why the study was so surprising even to us! Most writers wanted the “how did the animals move?” angle, which was not what the study was about. I still feel that this angle was not even needed; the study (and again I take minimal credit for it) is exciting without it. To comparative anatomy and evo-devo specialists, anyway. Well, that’s science for you; sometimes it is just too hard to explain its value to the outside world, even when you feel its importance in your very spine… And the press coverage was not terrible by any means; no sour grapes from me. Regardless, we’re glad it has been well received by specialist researcher colleagues we’ve spoken to, and that matters a lot.

NERC’s Planet Earth (nice story from our funder)- “Scientists had fossil backbone backwards”

BBC online (the only story aside from NERC’s that did more than read the press release) “Tetrapod anatomy: Backbone back-to-front in early animals”

Discovery News online- “First Land Animals Shuffled Like Seals” (good, but is sort of mixing up our this study, our 2012 one and Ahlberg et al’s 2005 seal-analogue study; latter two were more about movement. As often happens, a lot of other media stories basically copied this one’s headline/angle.)

Discover 80beats- “Paleontologists Use 3-D Models to Rewrite Evolution” (also in “top stories”)

Popsci- “Particle Accelerator Reveals That First Land Animals Walked Like Seals”

Daily FMail (nice pics)- “Astonishing 3D images reveal the first four-legged land animals in amazing detail – and overturn a century of research” (wins longest headline award)

Red Orbit- “Study Reveals First Ever Images Of Early Tetrapod Backbone And How It Helped In Land Evolution”

Examiner.com- “X-ray study rewrites tetrapod backbone evolution (Photos)”

Everything Dinosaur- “Ichthyostega Gets a Re-Think”

Business Standard- “Scientists recreate earliest quadraped’s backbone” (Proofread, editors! Quadruped.)

Geekosystem- “Early Land-Dwelling Animals Moved About Like Seals, Probably Didn’t Balance Balls on Their Noses” (scores some pts for humour)

…and the PR-copying, non-spellchecking fail of the week award goes to… Physorg! “Scientists reassemble the backbone of life with a particle acceleratorynchrotron [sic] X-rays”

Warming up the acceleratorynchrotron for our next study… :)

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Party time! Let the media onslaught begin! We’ve published a paper in Nature on the limb motions of Ichthyostega (and by implication, some other stem tetrapods). Since we did use some crocodile specimens from Freezersaurus (see below) in this study, I figured WIJF could cover it to help celebrate this auspicious event. Briefly. Particularly since we already did a quasi-blog on it, which is here:

http://www.rvc.ac.uk/SML/Research/Stories/TetrapodLimbMotion.cfm

and some juicy fossily images at:

http://www.rvc.ac.uk/SML/Research/Stories/TetrapodImages.cfm

However I want to feature our rockin’ cool animations we did for the paper, to squeeze every last possible drop of science communicationy goodness out of them. So here they are in all their digital glory. Huge credit to Dr. Stephanie Pierce, the brilliant, hardworking postdoc who spearheaded the work including these videos! Dr. Jenny Clack is our coauthor on this study and the sage of Ichthyostega and its relatives- her website is here. Also, a big hurrah for our goddess of artsy science, Julia Molnar, who helped with the videos and other images. Enjoy!

The computer model

The forelimb model

The hindlimb model

We used some of my Nile crocodile collection to do a validation analysis of our joint range of motion (ROM) methods, detailed in the Supplementary info of the paper, which I encourage anyone interested to read since it has loads more interesting stuff and cool pics. We found that a bone-based ROM will always give you a greater ROM than an intact fleshy limb-based ROM. In other words, muscles and ligaments (and articular cartilage, etc.). have a net effect of reducing how far a joint can move. This is not shocking but few studies have ever truly quantitatively checked this with empirical data from whole animals. It is an important consideration for all vert paleo types. Here is a pic of one of the crocodiles from the study, with (A) and without muscles (B; ligaments only):

I’ll close with Julia Molnar’s jaw-droppingly awesome flesh reconstruction from our model. Why Nature wouldn’t use this as a cover pic, I’ll never understand, but I LOVE it! When I first saw it enter my email inbox and then opened it to behold its glory, my squeal of geeky joy was deafening.

(edit: Aha! Fellow Berkeley alum Nick Pyenson’s group made the Nature cover, for their kickass study of rorqual whale anatomy, including a “new” organ! Well, we don’t feel so bad then. Great science– and a win for anatomy!!!)

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In case you missed the story about this paper released just before Xmas, here are some links to stories about “From flat foot to fat foot: Structure, ontogeny, function and evolution of elephant “sixth toes,” in Science, 2011:

1. The paper (free download from my publications list; nice policy, Science!)

2. Our website about the paper (more imagery goodness!)

3. Ed Yong’s first (Nature News) and second (more detailed blog) article

4. BBC News’s story

5. Reuters TV‘s excellent video

6. Science Now/Wired’s story

7. Daily Mail‘s story (not a daily fail, in this case)

Clarification: it’s not a real sixth toe in elephants; it’s a false, toe-like structure (“predigit”) made from other tissue. That confusion seeped into some media stories. But this whole story ties into the thorny question of what a digit (finger/toe) is and how we can tell (e.g., notions of homology). Regardless, the elephant predigits are present in all four feet, and are super duper cool!

Most importantly for this blog, that research relied, and still relies, on our fabulous freezers to keep the elephant “toes” in snuggly cold conditions until we wanted to study them.

The research is continuing- I’ll post more about that later. We’ve been doing lots more histology to explore the complex ways that these predigits are formed, and also studying how they function (ex vivo) in more 3D detail than before (with new comparisons to rhino feet). Also, a new paper of ours will come out in J Experimental Biology very soon. It elaborates on how whole elephant feet function, across ontogeny, using in vivo pressure patterns.

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