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Deck the ‘Nets With PeerJ Papers– please sing along!

♬Deck the ‘nets with PeerJ papers,
Fa la la la la, la la la la.
‘Tis the day to show our labours,
Fa la la la la, la la la la.

Downloads free; CC-BY license,
Fa la la, la la la, la la la.
Read the extant ratite science,
Fa la la la la, la la la la.

See the emu legs before you
Fa la la la la, la la la la.
Muscles allometric’ly grew.
Fa la la la la, la la la la.

Follow the evolvin’ kneecaps
Fa la la la la, la la la la.
While we dish out ratite recaps 
Fa la la la la, la la la la.

Soon ostrich patellar printing
Fa la la la la, la la la la.
Hail anat’my, don’t be squinting
Fa la la la la, la la la la.

Dissections done all together
Fa la la la la, la la la la.
Heedless of the flying feathers,
Fa la la la la, la la la la♪

(alternate rockin’ instrumental version)

Stomach-Churning Rating: 5/10: cheesy songs vs. fatty chunks of tissue; there are no better Crimbo treats!

Today is a special day for palaeognath publications, principally pertaining to the plethora of published PeerJ papers (well, three of them anyway) released today, featuring my team’s research! An early Crimbo comes this year in the form of three related studies of hind limb anatomy, development, evolution and biomechanics in those flightless feathered freaks of evolutionary whimsy, the ratites! And since the papers are all published online in PeerJ (gold open access), they are free for anyone with internet access to download and use with due credit. These papers include some stunning images of morphology and histology, evolutionary diagrams, and a special treat to be revealed below. Here I’ll summarize the papers we have written together (with thanks to Leverhulme Trust funding!):

1) Lamas, L., Main, R.P., Hutchinson, J.R. 2014. Ontogenetic scaling patterns and functional anatomy of the pelvic limb musculature in emus (Dromaius novaehollandiae). PeerJ 2:e716 http://dx.doi.org/10.7717/peerj.716 

My final year PhD student and “emu whisperer” Luis Lamas has published his first paper with co-supervisor Russ Main and I. Our paper beautifully illustrates the gross anatomy of the leg muscles of emus, and then uses exhaustive measurements (about 6524 of them, all done manually!) of muscle architecture (masses, lengths, etc.) to show how each of the 34 muscles and their tendons grew across a more than tenfold range of body mass (from 6 weeks to 18 months of age). We learned that these muscles get relatively, not just absolutely, larger as emus grow, and their force-generating ability increases almost as strongly, whereas their tendons tend to grow less quickly. As a result, baby emus have only about 22% of their body mass as leg muscles, vs. about 30% in adults. However, baby emus still are extremely athletic, more so than adults and perhaps even “overbuilt” in some ways.

This pattern of rapidly growing, enlarged leg muscles seems to be a general, ancestral pattern for living bird species, reflecting the precocial (more independent, less nest-bound), cursorial (long-legged, running-adapted) natural history and anatomy, considering other studies of ostriches, rheas, chickens and other species close to the root of the avian family tree. But because emus, like other ratites, invest more of their body mass into leg muscles, they can carry out this precocial growth strategy to a greater extreme than flying birds, trading flight prowess away for enhanced running ability. This paper adds another important dataset to the oft-neglected area of “ontogenetic scaling” of the musculoskeletal system, or how the locomotor apparatus adapts to size-/age-related functional/developmental demands as it grows. Luis did a huge amount of work for this paper, leading arduous dissections and analysis of a complex dataset.

Superficial layer of leg muscles in an emu, in right side view.

Superficial layer of leg muscles in an emu, in right side view. Click any image here to emu-biggen. The ILPO and IC are like human rectus femoris (“quads”); ILFB like our biceps femoris (“hams”); FL, GM and GL much like our fibularis longus and gastrocnemius (calf) muscles, but much much bigger! Or, perhaps FL stands for fa la la la la?

Data for an extra set of emus studied by coauthor Russ Main in the USA, which grew their muscles similarly to our UK group. The exponents (y-axis) show how much more strongly the muscles grown than isometry (maintaining the same relative size), which is the dotted line at 1.0.

Data for an extra set of emus studied by coauthor Russ Main in the USA, which grew their muscles similarly to our UK group. The exponents (y-axis) show how much more strongly the muscles grew than isometry (maintaining the same relative size), which is the dotted line at 1. The numbers above each data point are the # of individuals measured. Muscle names are partly above; the rest are in the paper. If you want to know them, we might have been separated at birth!

2) Regnault, S., Pitsillides, A.A., Hutchinson, J.R. 2014. Structure, ontogeny and evolution of the patellar tendon in emus (Dromaius novaehollandiae) and other palaeognath birds. PeerJ 2:e711 http://dx.doi.org/10.7717/peerj.711

My second year PhD student Sophie Regnault (guest-blogger here before with her rhino feet post) has released her first PhD paper, on the evolution of kneecaps (patellae) in birds, with a focus on the strangeness of the region that should contain the patella in emus. This is a great new collaboration combining her expertise in all aspects of the research with coauthor Prof. Andy Pitsillides‘s on tissue histology and mine on evolution and morphology. This work stems from my own research fellowship on the evolution of the patella in birds, but Sophie has taken it in a bold new direction. First, we realized that emus don’t have a patella– they just keep that region of the knee extensor (~human quadriceps muscle) tendon as a fatty, fibrous tissue throughout growth, showing no signs of forming a bony patella like other birds do. This still blows my mind! Why they do this, we can only speculate meekly about so far. Then, we surveyed other ratites and related birds to see just how unusual the condition in emus was. We discovered, by mapping the form of the patella across an avian family tree, that this fatty tendon seems to be a thing that some ratites (emus, cassowaries and probably the extinct giant moas) do, whereas ostriches go the opposite direction and develop a giant double-boned kneecap in each knee (see below), whereas some other relatives like tinamous and kiwis develop a more “normal”, simple flake-like bit of bone, which is likely the state that the most recent common ancestor of all living birds had.

There’s a lot in this paper for anatomists, biomechanists, palaeontologists, ornithologists, evo-devo folks and more… plenty of food for thought. The paper hearkens back to my 2002 study of the evolution of leg tendons in tetrapods on the lineage that led to birds. In that study I sort of punted on the question of how a patella evolved in birds, because I didn’t quite understand that wonderful little sesamoid bone. And now, 12 years later, we do understand it, at least within the deepest branches of living birds. What happened further up the tree, in later branches, remains a big open subject. It’s clear there were some remarkable changes, such as enormous patellae in diving birds (which the Cretaceous Hesperornis did to an extreme) or losses in other birds (e.g., by some accounts, puffins… I am skeptical)– but curiously, patellae that are not lost in some other birds that you might expect (e.g., the very non-leggy hummingbirds).

Fatty knee extensor tendon of emus, lacking a patella. The fatty tissue is split into superficial (Sup) and deep regions, with a pad corresponding to the fat pad in other birds continuous with it and the knee joint meniscus (cushioning pad). The triceps femoris (knee extensor) muscle group inserts right into the fatty tendon, continuing over it. A is a schematic; B is a dissection.

Fatty knee extensor tendon of an emu, showing the absence of a patella. The fatty tissue is split into superficial (Sup) and deep regions, with a pad corresponding to the fat pad in other birds continuous with it and the knee joint meniscus (cushioning pad). The triceps femoris (knee extensor) muscle group inserts right into the fatty tendon, continuing on over it. A is a schematic; B is a dissection.

Sectioning of a Southern Cassowary's knee extensor tendon, showing: A Similar section  as in the emu image above. revealing similar regions and fibrous tissue (arrow), with no patella, just fat; and B, with collagen fibre bundles (col), fat cells (a), and cartilage-like tissue (open arrows) labelled.

Sectioning of a Southern Cassowary’s knee extensor tendon, showing: A, Similar section as in the emu image above. revealing similar regions and fibrous tissue (arrow), with no patella, just fat; and B, With collagen fibre bundles (col), fat cells (a), and cartilage-like tissue (open arrows) labelled.

Evolution of patellar form in birds. White branches indicate no patella, blue is a small flake of bone for a patella, green is something bigger, yellow is a double-patella in ostriches, and grey is uncertain. Note the uncertainty and convergent evolution of the patella in ratite birds, which is remarkable but fits well with their likely convergent evolution of flightlessness and running adaptations.

Evolution of patellar form in birds. White branches indicate no patella, blue is a small flake of bone for a patella, green is something bigger, yellow is a double-patella in ostriches, black is a gigantic spar of bone in extinct Hesperornis and relatives, and grey is uncertain. Note the uncertainty and convergent evolution of the patella in ratite birds (Struthio down to Apteryx), which is remarkable but fits well with their likely convergent evolution of flightlessness and running adaptations.

3) Chadwick, K.P., Regnault, S., Allen, V., Hutchinson, J.R. 2014. Three-dimensional anatomy of the ostrich (Struthio camelus) knee joint. PeerJ 2:e706 http://dx.doi.org/10.7717/peerj.706

Finally, Kyle Chadwick came from the USA to do a technician post and also part-time Masters degree with me on our sesamoid grant, and proved himself so apt at research that he published a paper just ~3 months into that work! Vivian Allen (now a postdoc on our sesamoid bone grant) joined us in this work, along with Sophie Regnault. We conceived of this paper as fulfilling a need to explain how the major tissues of the knee joint in ostriches, which surround the double-patella noted above, all relate to each other and especially to the patellae. We CT and MRI scanned several ostrich knees and Kyle made a 3D model of a representative subject’s anatomy, which agrees well with the scattered reports of ostrich knee/patellar morphology in the literature but clarifies the complex relationships of all the key organs for the first time.

This ostrich knee model also takes Kyle on an important first step in his Masters research, which is analyzing how this morphology would interact with the potential loads on the patellae. Sesamoid bones like the patella are famously responsive to mechanical loads, so by studying this interaction in ostrich knees, along with other studies of various species with and without patellae, we hope to use to understand why some species evolved patellae (some birds, mammals and lizards; multiple times) and why some never did (most other species, including amphibians, turtles, crocodiles and dinosaurs). And, excitingly for those of you paying attention, this paper includes links to STL format 3D graphics so you can print your own ostrich knees, and a 3D pdf so you can interactively inspect the anatomy yourself!

(A) X-ray of an ostrich knee in side view, and (B) labelled schematic of the same.

Ostrich knee in side view: A, X-ray, and (B) labelled schematic.

3D model of an ostrich knee, showing: A, view looking down onto the top of the tibia (shank), with the major collateral ligaments (CL), and B, view looking straight at the front of the knee joint, with major organs of interest near the patella, sans muscles.

3D model of an ostrich knee, showing: A, View looking down onto the top of the tibia (shank), with the major collateral ligaments (CL), and B, View looking straight at the front of the knee joint, with major organs of interest near the patella, sans muscles.

You can view all the peer review history of the papers if you want, and that prompts me to comment that, as usual at PeerJ (full disclosure: I’m an associate editor but that brings me £0 conflict of interest), the peer review quality was as rigorous at a typical specialist journal, and faster reviewing+editing+production than any other journal I’ve experienced. Publishing there truly is fun!

Merry Christmas and Happy Holidays — and good Ratite-tidings to all!

And stay tuned- the New Year will bring at least three more papers from us on this subject of ratite locomotion and musculoskeletal anatomy!

♬Should auld palaeognathans be forgot, 
And never brought for scans? 
Should publications be soon sought, 
For auld ratite fans!♪

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I’ll let the poll (prior post) run for a while but as it winds down I wanted to explain why I posted it:

In the past, I’ve often run into scientists who, when defending their published or other research, respond something like this:

“Yeah those data (or methods) might be wrong but the conclusions are right regardless, so don’t worry.”

And I’ve said things like that before. However, I’ve since realized that this is a dangerous attitude, and in many contexts it is wrong.

If the data are guesses, as in the example I gave, then we might worry about them and want to improve them. The “data are guesses” context that I set the prior post in comes from Garland’s 1983 paper on the maximal speeds of mammals– you can download a pdf here if this link works (or Google it). Basically the analysis shows that, as mammals get bigger, they don’t speed up as a simple linear analysis might show you. Rather, at a moderate size of around 50-100kg body mass or so, they hit a plateau of maximal speed, then bigger mammals tend to move more slowly. However, all but a few of the data points in that paper are guesses, many coming from old literature. The elephant data points are excessively fast in the case of African elephants, and on a little blog-ish webpage from the early 2000s we chronicled the history of these data– it’s a fun read, I think. The most important, influential data plot from that paper by Garland is below, and I love it– this plot says a lot:

Garland1983

I’ve worried about the accuracy of those data points for a long time, especially as analyses keep re-using them– e.g. this paper, this one, and this one, by different authors. I’ve talked to several people about this paper over the past 20 years or so. The general feeling has been in agreement with Scientist 1 in the poll, or the quote above– it’s hard to imagine how the main conclusions of the paper would truly be wrong, despite the unavoidable flaws in the data. I’d agree with that statement still: I love that Garland paper after many years and many reads. It is a paper that is strongly related to hypotheses that my own research seeks out to test. I’ve also tried to fill in some real empirical data on maximal speeds for mammals (mainly elephants; others have been less attainable), to improve data that could be put into or compared with such an analysis. But it is very hard to get good data on even near-maximal speeds for most non-domesticated, non-trained species. So the situation seems to be tolerable. Not ideal, but tolerable. Since 1983, science seems to be moving slowly toward better understanding of the real-life patterns that the Garland paper first inferred, and that is good.

But…

My poll wasn’t really about that Garland paper. I could defend that paper- it makes the best of a tough situation, and it has stimulated a lot of research (197 citations according to Google; seems low actually, considering the influence I feel the paper has had).

I decided to do the poll because thinking about the Garland paper’s “(educated) guesses as data” led me to think of another context in which someone might say “Yeah those data might be wrong but the conclusions are right regardless, so don’t worry.” They might say it to defend their own work, such as to deflect concerns that the paper might be based on flawed data or methods that should be formally corrected. I’ve heard people say this a lot about their own work, and sometimes it might be defensible. But I think we should think harder about why we would say such things, and if we are justified in doing so.

We may not just be making the best of a tough situation in our own research. Yes, indeed, science is normally wrong to some degree. A more disconcerting situation is that our wrongs may be mistakes that others will proliferate in the future. Part of the reasoning for being strict stewards of our own data is this: It’s our responsibility as scientists to protect the integrity of the scientific record, particularly of our own published research because we may know that best. We’re not funded (by whatever source, unless we’re independently wealthy) just to further our own careers, although that’s important too, as we’re not robots. We’re funded to generate useful knowledge (including data) that others can use, for the benefit of the society/institution that funds us. All the more reason to share our critical data as we publish papers, but I won’t go off on that important tangent right now.

In the context described in the latter paragraph and the overly simplistic poll, I’d tend to favour data over conclusions, especially if forced to answer the question as phrased. The poll reveals that, like me, most (~58%) respondents also would tend to favour data over conclusions (yes, biased audience, perhaps- social media users might tend to be more savvy about data issues in science today? Small sample size, sure,  that too!). Whereas very few (~10%) would favour conclusions, in the context of the poll. The many excellent comments on the poll post reveal the trickier nuances behind the poll’s overly simplistic question, and why many (~32%) did not favour one answer over the other.

If you’ve followed this blog for a while, you may be familiar with a post in which I ruminated over my own responsibilities and conundrums we face in work-life balance, personal happiness, and our desires to protect ourselves or judge/shame others. And if you’ve closely followed me on Twitter or Facebook, you may have noticed we corrected a paper recently and retracted another. So I’ve stuck by my guns lately, as I long have, to correct my team’s work when I’m aware of problems. But along the way I’ve learned a lot, too, about myself, science, collaboration, humanity, how to improve research practice or scrutiny, and the pain of errors vs. the satisfaction of doing the right thing. I’ve had some excellent advice from senior management at the RVC along the way, which I am thankful for.

I’ve been realizing I should minimize my own usage of the phrase “The science may be flawed but the conclusions are right.” That can be a more-or-less valid defence, as in the case of the classic Garland paper. But it can also be a mask (unintentional or not) that hides fear that past science might have real problems (or even just minor ones that nonetheless deserve fixing) that could distract one away from the pressing issues of current science. Science doesn’t appreciate the “pay no attention to the person behind the curtain” defence, however. And we owe it to future science to tidy up past messes, ensuring the soundness of science’s data.

We’re used to moving forward in science, not backward. Indeed, the idea of moving backward, undoing one’s own efforts, can be terrifying to a scientist– especially an early career researcher, who may feel they have more at risk. But it is at the very core of science’s ethos to undo itself, to fix itself, and then to move on forward again.

I hope that this blog post inspires other scientists to think about their own research and how they balance the priorities of keeping their research chugging along but also looking backwards and reassessing it as they proceed. It should become less common to say “Yeah those data might be wrong but the conclusions are right regardless, so don’t worry.” Or it might more common to politely question such a response in others. As I wrote before, there often are no simple, one-size-fits-all answers for how to best do science. Yet that means we should be wary of letting our own simple answers slip out, lest they blind us or others.

Maybe this is all bloody obvious or tedious to blog readers but I found it interesting to think about, so I’m sharing it. I’d enjoy hearing your thoughts.

Coming soon: more Mystery Anatomy, and a Richard Owen post I’ve long intended to do.

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A short post that guest-tweeting at the  Biotweeps account on Twitter got me thinking about– featuring a poll.

Imagine this: two scientists (colleagues, if you’re a scientist) are arguing thusly. Say it’s an argument about a classic paper in which much of the data subjected to detailed statistical analyses are quantitative guesses, not hard measurements. This could be in any field of science.

Scientist 1: “Conclusions are what matter most in science. If the data are guesses, but still roughly right, we shouldn’t worry much. The conclusions will still be sound regardless. That’s the high priority, because science advances by ideas gleaned from conclusions, inspiring other scientists.”

Scientist 2: “Data are what matter most in science. If the data are guesses, or flawed in some other way, this is a big problem and scientists must fix it. That’s the high priority, because science advances by data that lead to conclusions, or to more science.”

Who’s right? Have your say in this anonymous poll (please vote first before viewing results!):

link: http://poll.fm/4xf5e

[Wordpress is not showing the poll on all browsers so you may have to click the link]

And if you have more to say and don’t mind being non-anonymous, say more in the Comments- can you convince others of your answer? Or figure out what you think by ruminating in the comments?

I’m genuinely curious what people think. I have my own opinion, which has changed a lot over the past year. And I think it is a very important question scientists should think about, and discuss. I’m not just interested in scientists’ views though; anyone science-interested should join in.

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[This is the original, unedited text of my shorter, tighter (and I think actually better) News & Views piece for Nature, on the paper described below)

Ambitious experimental and morphological studies of a modern fish show how a flexible phenotype may have helped early “fishapods” to make the long transition from finned aquatic animals into tetrapods able to walk on land.

Stomach-Churning Rating: 1/10. Cute fish. Good science. Happy stomachs!

Photo by Antoine Morin, showing Polypterus on land.

Photo by Antoine Morin, showing Polypterus on land.

Napoleon Bonaparte’s military excursions into Egypt in 1798-1799 led a young French naturalist, Ètienne Geoffroy Saint-Hilaire, to cross paths with a strange fish that had paired lungs and could “walk” across land on its stubby, lobelike fins. In 1802, he dubbed this fish “Polyptère bichir”1, today known as the Nile bichir, Polypterus bichir La Cepède 1803. The bichir’s mélange of primitive and advanced traits helped to catapult Geoffroy into scholarly conflict with the reigning naturalist Georges Cuvier back in France and to establish Ètienne as a leading anatomist, embryologist and early evolutionary researcher of repute even today2. Now, on their own excursion under the very “evo-devo” flag that the discoverer of Polypterus helped raise, Canadian scientists Standen et al.3 suggest how the remarkable plasticity of the skeleton of Polypterus (the smaller west African relative of P. bichir, P. senegalus or “Cuvier’s bichir”) reveals a key part of the mechanism that might have facilitated the gradual transition from water to land and thus from “fishapods” to tetrapods (four-limbed vertebrates).

In a bold experiment, the authors raised 149 young bichirs on land and in water for eight months, then studied how they moved on land vs. in water, and also how the ultimate shape of the skeletal elements of the paired front fin bases differed between the land- and water-raised bichirs. Standen et al.3 discovered that both the form and function of the fins’ foundations transformed to better satisfy the constraints of moving on land. Land-acclimated bichirs took faster steps on land, their fins slipped across the substrate less, they held their fins closer to their body, their noses stayed more aloft and their tails undulated less, with less variable motions overall—behaviours that the authors had predicted should appear to enhance walking abilities on land. In turn, the bones of the neck and shoulder region altered their shape to produce a more mobile fin base with greater independence of fin from neck motion, along with improved bracing of the ventral “collarbone” region. These environmentally-induced traits should have fostered the locomotor changes observed in “terrestrialized” fish and aided the animals in resisting gravity, and they represent a common biological phenomenon termed developmental plasticity4,5. Interestingly, the land-reared fish could still swim about as well as the wholly aquatic cohort, so there was not a clear trade-off between being a good swimmer and a good walker, which is surprising.

Considered alone, the developmental plasticity of bichir form and function shows how impressive these amphibious fish are. But Standen et al.’s study3  ventured further, to apply the lessons learned from bichir ontogeny to a phylogenetic context and macroevolutionary question. The phenotypic plasticity during bichir development, they infer, could have been harnessed during the evolutionary transformation of fins for swimming into limbs for walking, in the “fishapod” ancestors of tetrapods. Indeed, bichirs are close to the base of the family tree of fishes6, and other living relatives of tetrapods have reduced or lost their fins (lungfishes) or adapted to strange deep-sea swimming lifestyles, never walking on land (coelacanths). Thus perhaps bichirs and the “fishapod” lineage share what Geoffroy would have called “unity of type”, today termed homology, of their developmental plasticity in response to a land environment. Surveying the fossil record of early “fishapods” and tetrapods, Standen et al.3 found that the macroevolutionary changes of neck and shoulder anatomy in these gradually more land-adapted animals parallel those they observed in terrestrialized Polypterus, providing ancillary support for their hypothesis.

A further test of the application of Polypterus’s plasticity to fossil tetrapods is naturally difficult. However, the “fishapod” lineage has some exceptional examples of fossil preservation. With sufficient sample sizes (e.g. fossil beds that reveal growth series, such as the Late Devonian Miguasha site in Canada7) and palaeoenvironmental gradients in fish or tetrapods, one could imagine performing a rigorous indirect test. Even small samples could be helpful– for example, the early tetrapod Ichthyostega exhibits some developmental changes in its forelimb suggesting that it became more terrestrial as it grew, whereas the related Acanthostega does not evidence such changes8– this hints at some developmental plasticity in the former animal.

During the Devonian period (~360-420 million years ago), were the “fishapod” ancestors of tetrapods floundering about on land now and then, gradually shifting from anatomy and behaviours that were more developmentally plastic (as in bichirs) to ones that were more canalized into the terrestrialized forms and functions that more land-adapted tetrapods retained? An attractive possibility is that the developmental plasticity could have led to fixation (reduction of plasticity), an evolutionary phenomenon called genetic assimilation, which another intellectual descendant of Geoffroy, Conrad Hal Waddington, promoted from the 1950s onwards9, a concept that now enjoys numerous cases of empirical support10 that this one may eventually join.

The nature of the genetic and developmental mechanism that bichirs use to achieve the observed developmental plasticity is still unclear. If it has a high enough degree of heritability, then it could be selected for in cross-generational experiments with bichirs. With sufficient time and luck raising these unusual fish, the hypothesis that their plastic response to a terrestrial environment can become genetically assimilated could be directly tested. This study could thus become an epic exemplar of how genetic assimilation can contribute not only to microevolutionary change but also to major macroevolutionary events, as was presciently suggested in a seminal review of developmental plasticity4.

This genetic assimilation is the Polypterus study’s reasonable speculation, and one that Geoffroy likely would have applauded, all the more for involving his beloved bichirs. Much as Napoleon’s landfall in Egypt was not a lasting success, bichirs never left wholly terrestrial descendants despite their malleable locomotor system. But the same type of plastic developmental mechanism that bichirs use today to make tentative, floppy incursions of the terrestrial realm might have been harnessed by our own “fishapod” forebears, leaving a far more revolutionary dynasty upon the Earth.

 

References

  1.  Geoffroy, E. (1802). Histoire naturelle et description anatomique d’un nouveau genre de poisson du Nil, nommé polyptère. Annales du Muséum d’Histoire Naturelle 1:57-68.
  2. Le Guyader, H., & Grene, M. (2004) Geoffroy Saint-Hilaire: A Visionary Naturalist. Univ. Chicago Press.
  3. Standen, E. M., Du, T. Y., & Larsson, H. C. E. (2014). Developmental plasticity and the origin of tetrapods. Nature, published online.
  4. West-Eberhard, M. J. (1989). Phenotypic plasticity and the origins of diversity. Annual Review of Ecology and Systematics 20:249-278.
  5. Pigliucci, M., Murren, C. J., & Schlichting, C. D. (2006). Phenotypic plasticity and evolution by genetic assimilation. Journal of Experimental Biology 209(12):2362-2367.
  6. Near, T. J., Dornburg, A., Tokita, M., Suzuki, D., Brandley, M. C., & Friedman, M. (2014). Boom and bust: ancient and recent diversification in bichirs (Polypteridae: Actinopterygii), a relictual lineage of ray‐finned fishes. Evolution 68:1014-1026.
  7. Cloutier, R. (2013). Great Canadian Lagerstätten 4. The Devonian Miguasha Biota (Québec): UNESCO World Heritage Site and a Time Capsule in the Early History of Vertebrates.Geoscience Canada40:149-163.
  8. Callier, V., Clack, J. A., & Ahlberg, P. E. (2009). Contrasting developmental trajectories in the earliest known tetrapod forelimbs.Science324:364-367.
  9. Waddington, C. H. (1953). Genetic assimilation of an acquired character. Evolution 7:118-126.
  10. Crispo, E. (2007). The Baldwin effect and genetic assimilation: revisiting two mechanisms of evolutionary change mediated by phenotypic plasticity. Evolution 61:2469-2479.

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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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