Folks,

You may know that the inaugral TetZooCon is set to take place next Saturday (12 July) at the London Wetland Centre. It’s an informal convention that’s condensed around occasional SV-POW!sketeer Darren Naish’s absurdly informative blog Tetrapod Zoology, and features a day of talks, a palaeoart workshop and a quiz. At £40 for the day, it’s a bit of a bargain.

Among the speakers is my own good self, and I will be talking about why giraffes are rubbish.

Taylor and Wedel 2013a: Figure 3. Necks of long-necked sauropods, to scale. Diplodocus, modified from elements in Hatcher (1901, plate 3), represents a “typical” long-necked sauropod, familiar from many mounted skeletons in museums. Puertasaurus, Sauroposeidon, Mamenchisaurus and Supersaurus modified from Scott Hartman’s reconstructions of Futalognkosaurus, Cedarosaurus, Mamenchisaurus and Supersaurus respectively. Alternating pink and blue bars are one meter in width. Inset shows Fig. 1 to the same scale.

Taylor and Wedel 2013a: Figure 3. Necks of long-necked sauropods, to scale. Diplodocus, modified from elements in Hatcher (1901, plate 3), represents a “typical” long-necked sauropod, familiar from many mounted skeletons in museums. Puertasaurus, Sauroposeidon, Mamenchisaurus and Supersaurus modified from Scott Hartman’s reconstructions of Futalognkosaurus, Cedarosaurus, Mamenchisaurus and Supersaurus respectively. Alternating pink and blue bars are one meter in width. Inset shows Fig. 1 to the same scale.

If that sounds like your idea of a good time, then you need to move fast! Booking closes at 4pm this evening. Better get on it now!

 

Order up!

Sauroposeidon OMNH 53062 articulated right lateral composite with giraffe

Sauroposeidon is stitched together from orthographic views of the 3D photogrammetric models rendered in MeshLab. Greyed out bits of the vertebrae are actually missing–I used C8 to patch C7, C7 to patch C6, and so on forward. The cervical ribs as reconstructed here were all recovered and they are in collections, but they’re in several jackets and boxes and therefore not easily photographed.

The meter bars are both one meter as advertised. The giraffe neck is FMNH 34426 (from this post), which is actually 1.7 meters long, but I scaled it up to 2.4 meters to match that of the tallest known giraffe. I think it’s cool that a world-record giraffe neck is roughly as long as two vertebrae from the middle of the neck of Sauroposeidon.

There are loads of little morphological details in the Sauroposeidon vertebrae that are clearer now than they were in our old photographs, but those will be stories for other posts.

Giraffe neck FMNH 34426 articulatedThe cervical series of Giraffa camelopardalis angolensis FMNH 34426, articulated by Mike and me and photographed by Mike back in the summer of 2005, cropped and composited by me recently, not previously posted because there’s just too much cool stuff, man. But we’re working on it.

By the way, if you want the details on this critter:

FMNH 34426 specimen tag

UPDATE April 23, 2014: What a maroon–I completely forgot to report the size of this thing! When we articulated all the centra and measured them (without cartilage, obviously), we got a length of 171 cm. When we measured the centra individually, leaving off the anterior condyles, we got a length of 164 cm. I think the discrepancy can be explained by the relative shallowness of the posterior cotyles of the vertebrae–as you can see in the big image above, the condyles do not nest completely within the cotyles, so each one does contribute a little bit to the length of the neck.

The measurements of each vertebra, as recorded by Mike in my notebook in the FMNH mammalogy collections in 2005, are here:

Giraffa FMNH 34426 cervical and dorsal measurements

Just for completeness, I should note that in our neck cartilage paper (Taylor and Wedel 2013b), we found that cartilage added considerably to the length of the articulated neck in many amniotes. Based on the intervertebral spacing in horses, 1-2 cm of cartilage between these giraffe vertebrae doesn’t seem unreasonable, which would bring the length of the neck to perhaps 1.8 meters. Amazingly, this is only 75% of the longest giraffe necks on record, which are up to 2.4 meters (Toon and Toon 2003).

References

supersaurus-vs-giraffe

At the top: our old friend BYU 9024 — the cervical vertebra that’s part of the Supersaurus vivianae holotype. At the bottom, C2 (the longest cervical) of Giraffa camelopardalis angolensis FMNH 34426.

The Supersaurus vertebra is 138 cm long. We don’t know which cervical it is, but there’s no reason to think it’s the longest. The giraffe vertebra is 31 cm long. Not only is the Supersaurus vertebra four times as long as that of the giraffe, it’s one of more than twice as many cervicals as the giraffe has.

Did we cheat by using an unusually small giraffe? Not really. When we articulated all seven cervicals as best we could, the sequence measured 171 cm, which is a fairly healthy 71% of the 2.4 m neck of the world-record giraffe. It’s not a monster, but it’s a decent-sized adult.

Bottom line, giraffes are just lame.

Having taken time to discuss at length why we posted our neck-anatomy paper on arXiv, let’s now return to the actual content of the paper. You may remember from the initial post, or indeed from the paper itself, that Table 3 of the paper summarises its conclusions:

Table 3. Neck-elongation features by taxon.

Needless to say, we puny humans lack all seven of the features that were discussed as contributing to long necks, while sauropods have them all. But it’s interesting to look at the giraffe and Paraceratherium, the two longest-necked mammals, and see what they have in common. They share quadrupedal stance; the giraffe has elongated cervical vertebrae; and Paraceratherium has absolutely large body size. But they both lack all four of the other features:

  • Small, light head
  • Numerous cervical vertebrae
  • Air-sac system
  • Vertebral pneumaticity

And they lack them for the same reason: because they are mammals. The same is true of all mammals, and the individual reasons for those four missing long-neck features are all the same: because mammals have hit local maxima, and can’t evolve away from them.

Mammals’ heads, for example, are all set up for extensive oral processing of food — certainly among large herbivores. (I think pretty much all the toothless mammals are insectivores.) They’ve got very good at it, and there’s no evolutionary pathway that can take a giraffe from its current lifestyle to a sauropod-like crop-and-swallow strategy without passing through an adaptive valley on the way. That means they are stuck with big, solid teeth and heavily engineered jaws, which means they can’t have light heads.

In the same way, mammals have much more efficient lungs than those of their reptile-like forebears, the common ancestors that they share with birds. They have evolved to a point where their lungs are too complex and effective to easily evolve into a different shape — yet by doing so, they have cut themselves off from the yet more efficient avian lung (shared by sauropods) that is capable of extracting twice as much oxygen as our lungs.

And of course in the absence of an avian-style lung, there can be no soft-tissue diverticula or air-sacs, and so no pneumatic invasion of the vertebrae.

A final nail in the coffin of mammal neck length is that we seem to be strongly wired to have exactly seven cervical vertebrae — no more, no less. The exceptions are very few and far between: sloths and sirenians, and even then they don’t vary from the seven-cervical pattern by more than one or two vertebrae.

Skull and cervical skeleton of the three-toed sloth, Bradypus tridactylus, taken at the University Museum of Zoology, Cambridge (UK). Note the nine cervical vertebrae — the most of any mammal.

As for why we can’t get past seven, or at most nine, cervicals — that’s harder to answer. There’s no reason why seven should be an adaptive maximum, so it seems that the reason is genetic: the instructions to produce seven cervicals are part of the same gene complex that gives us an advantage in some other way. I have vague memories of an excellent talk at the Bristol SVP suggesting that cervical-count is linked to cancer resistance, but I can’t remember any of the details.

Anyone able to elaborate?

Anyway: this is how evolution works, and why it doesn’t make organisms (including us) as perfect as we might wish. It has no goal in mind — such as a long neck — and blindly follows the path that at that moment gives the organism the best chance of reproducing successfully. That means an animal like a giraffe, even though it is clearly selecting for neck length, is trapped on an adaptive hill and can’t get down across the valley to a higher peak.

Why giraffes have short necks

September 26, 2012

Today sees the publication, on arXiv (more on that choice in a separate post), of Mike and Matt’s new paper on sauropod neck anatomy. In this paper, we try to figure out why it is that sauropods evolved necks six times longer than that of the world-record giraffe — as shown in Figure 3 from the paper (with a small version of Figure 1 included as a cameo to the same scale):

Figure 3. Necks of long-necked sauropods, to the same scale. Diplodocus, modified from elements in Hatcher (1901, plate 3), represents a “typical” long-necked sauropod, familiar from many mounted skeletons in museums. Puertasaurus modified from Wedel (2007a, figure 4-1). Sauroposeidon scaled from Brachiosaurus artwork by Dmitry Bogdanov, via commons.wikimedia.org (CC-BY-SA). Mamenchisaurus modified from Young and Zhao (1972, figure 4). Supersaurus scaled from Diplodocus, as above. Alternating pink and blue bars are one meter in width. Inset shows Figure 1 to the same scale.

This paper started life as a late-night discussion over a couple of beers, while Matt was over in England for SVPCA back in (I think) 2008. It was originally going to be a short note in PaleoBios, just noting some of the oddities of sauropod cervical architecture — such as the way that cervical ribs, ventral to the centra, elongate posteriorly but their dorsal counterparts the epipophyses do not.

As so often, the tale grew in the telling, so that a paper we’d initially imagined as a two-or-three-page note became Chapter 5 of my dissertation under the sober title of “Vertebral morphology and the evolution of long necks in sauropod dinosaurs”, weighing in at 41 1.5-spaced pages. By now the manuscript had metastatised into a comparison between the necks of sauropods and other animals and an analysis of the factors that enabled sauropods to achieve so much more than mammals, birds, other theropods and pterosaurs.

(At this point we had one of our less satisfactory reviewing experiences. We sent the manuscript to a respected journal, where it wasn’t even sent out to reviewers until more than a month had passed. We then had to repeatedly prod the editor before anything else happened. Eventually, two reviews came back: one of them careful and detailed; but the other, which we’d waited five months for, dismissed our 53-page manuscript in 108 words. So two words per page, or about 2/3 of a word per day of review time. But let’s not dwell on that.)

Figure 6. Basic cervical vertebral architecture in archosaurs, in posterior and lateral views. 1, seventh cervical vertebra of a turkey, Meleagris gallopavo Linnaeus, 1758, traced from photographs by MPT. 2, fifth cervical vertebra of the abelisaurid theropod Majungasaurus crenatissimus Depéret, 1896,UA 8678, traced from O’Connor (2007, figures 8 and 20). In these taxa, the epipophyses and cervical ribs are aligned with the expected vectors of muscular forces. The epipophyses are both larger and taller than the neural spine, as expected based on their mechanical importance. The posterior surface of the neurapophysis is covered by a large rugosity, which is interpreted as an interspinous ligament scar like that of birds (O’Connor, 2007). Because this scar covers the entire posterior surface of the neurapophysis, it leaves little room for muscle attachments to the spine. 3, fifth cervical vertebra of Alligator mississippiensis Daudin, 1801, MCZ 81457, traced from 3D scans by Leon Claessens, courtesy of MCZ. Epipophyses are absent. 4, eighth cervical vertebra of Giraffatitan brancai (Janensch, 1914) paralectotype HMN SII, traced from Janensch (1950, figures 43 and 46). Abbreviations: cr, cervical rib; e, epipophysis; ns, neural spine; poz, postzygapophysis.

This work made its next appearance as my talk at SVPCA 2010 in Cambridge, under the title Why giraffes have such short necks. For the talk, I radically restructured the material into a form that had a stronger narrative – a process that involved a lot of back and forth with Matt, dry-running the talk, and workshopping the order in which ideas were presented. The talk seemed to go down well, and we liked the new structure so much more than the old that we reworked the manuscript into a form that more closely resembled the talk.

That’s the version of the manuscript that we perfected in New York when we should have been at all-you-can-eat sushi places. It’s the version that we submitted on the train from New York to New Haven as we went to visit the collections of the Yale Peabody Museum. And it’s the version that was cursorily rejected from mid-to-low ranked palaeo journal because a reviewer said “The manuscript reads as a long “story” instead of a scientific manuscript” — which was of course precisely what we’d intended.

Needless to say, it was deeply disheartening to have had what we were convinced was a good paper rejected twice from journals, at a cost of three years’ delay, on the basis of these reviews. One option would have been to put the manuscript back into the conventional “scientific paper” straitjacket for the second journal’s benefit. But no. We were not going to invest more work to make the paper less good. We decided to keep it in its current, more readable, form and to find a journal that likes it on that basis.

At the moment, the plan is to send it to PeerJ when that opens to submissions. (Both Matt and I are already members.) But that three-years-and-rolling delay really rankles, and we both felt that it wasn’t serving science to keep the paper locked up until it finally makes it into a journal — hence the deposition in arXiv which we plan to talk about more next time.

Table 3. Neck-elongation features by taxon.

In the paper, we review seven characteristics of sauropod anatomy that facilitated the evolution of long necks: absolutely large body size; quadrupedal stance; proportionally small, light head; large number of  cervical vertebrae; elongation of cervical vertebrae; air-sac system; and vertebral pneumaticity. And we show that giraffes have only two of these seven features. (Ostriches do the next best, with five, but they are defeated by their feeble absolute size.)

The paper incorporates some material from SV-POW! posts, including Sauropods were corn-on-the-cob, not shish kebabs. In fact, come to think of it, we should have cited that post as a source. Oh well. We do cite one SV-POW! post: Darren’s Invading the postzyg, which at the time of writing is the only published-in-any-sense source for pneumaticity invading cervical postzygapogyses from the medial surface.

As for the non-extended epipophyses that kicked the whole project off: we did illustrate how they could look, and discussed why they would seem to make mechanical sense:

Figure 10. Real and speculative muscle attachments in sauropod cervical vertebrae. 1, the second through seventeenth cervical vertebrae of Euhelopus zdanskyi Wiman, 1929 cotype specimen PMU R233a-δ(“Exemplar a”). 2, cervical 14 as it actually exists, with prominent but very short epipophyses and long cervical ribs. 3, cervical 14 as it would appear with short cervical ribs. The long ventral neck muscles would have to attach close to the centrum. 4, speculative version of cervical 14 with the epipophyses extended posteriorly as long bony processes. Such processes would allow the bulk of both the dorsal and ventral neck muscles to be located more posteriorly in the neck, but they are not present in any known sauropod or other non-avian dinosaur. Modified from Wiman (1929, plate 3).

But we found and explained some good reasons why this apparently appealing arrangement would not work. You’ll need to read the paper for details.

Sadly, we were not able to include this slide from the talk illustrating the consequences:

Anyway, go and read the paper! It’s freely available, of course, like all arXiv depositions, and in particular uses the permissive Creative Commons Attribution (CC BY) licence. We have assembled related information over on this page, including full-resolution versions of all the figures.

In the fields of maths, physics and computer science, where deposition in arXiv is ubiquitous, standard practice is to go right ahead and cite works in arXiv as soon as they’re available, rather than waiting for them to appear in journals. We will be happy for the same to happen with our paper: if it contains information that’s of value to you, then feel free to cite the arXiv version.

Reference

  • Taylor, Michael P., and Mathew J. Wedel. 2012. Why sauropods had long necks; and why giraffes have short necks. arXiv:1209.5439. 39 pages, 11 figures, 3 tables. [Full-resolution figures]

I have a new paper out:

Wedel, M.J. 2012. A monument of inefficiency: the presumed course of the recurrent laryngeal nerve in sauropod dinosaurs. Acta Palaeontologica Polonica 57(2):251-256.

Update June 6, 2012: the final version was formally published yesterday, so the rest of this paragraph is of historical interest only. Like Yates et al. on prosauropod pneumaticity, it is “out” in the sense that the manuscript has been through peer review, has been accepted for publication, and is freely available online at Acta Palaeontologica Polonica. Technically it is “in press” and not published yet, but all that formal publication will change is to make a prettier version of the paper available. All of the content is available now, and the paper doesn’t include any of those pesky nomenclatural acts, and so, as with the prosauropod pneumaticity paper, I don’t see any reason to pretend it doesn’t exist. Think of the accepted manuscript as the caterpillar to the published version’s butterfly: different look, but same genome.

This one came about because last summer I read a review of Richard Dawkins’s book, The Greatest Show on Earth: The Evidence for Evolution. The review mentioned that the book includes a lengthy discussion of the recurrent laryngeal nerve (RLN) in the giraffe, which is a spectacularly dumb piece of engineering and therefore great evidence against intelligent design creationism. It wasn’t the first time I’d heard of the RLN, of course. It’s one of the touchstones of both human anatomy and evolutionary biology; anatomy because of its clinical importance in thyroid surgery, known for more than two millennia, and evolutionary biology because it is such a great example of a developmental constraint. (Dawkins’s coverage of all of this is great, BTW, and you should read the book.)

No, the reason the book review inspired me to write the paper was not because the RLN was new to me, but because it was overly familiar. It is a cool piece of anatomy, and its fame is justly deserved–but I am sick and tired of seeing the stinkin’ giraffe trotted out as the ultimate example of dumb design. My beloved sauropods were way dumber, and it’s time they got some credit.

But first, let’s talk about that nerve, and how it got to be there.

No necks for sex? How about no necks for anybody!

Embryos are weird. When you were just a month old (counting from fertilization), you had a set of pharyngeal arches that didn’t look radically different from those of a primitive fish. These started out quite small, tucked up underneath your comparatively immense brain, and each pharyngeal arch was served by a loop of artery called an aortic arch. What we call the arch of the aorta in an adult human is a remnant of just one of these embryonic aortic arches, and as you’ve no doubt noticed, it’s down in your chest, not tucked up next to your brain. When you were in the embryonic stages I’m talking about, you didn’t yet have a neck, so your brain, pharyngeal arches, aortic arches, and the upper parts of your digestive system were all smooshed together at your front end.

One thing you did have at that stage was a reasonably complete peripheral nervous system. The nerve cell bodies in and near your central nervous system sent out axons into the rest of your body, including your extremities. Many of these axons did not persist; they failed to find innervation targets and their parent neurons died. Imagine your embryonic central nervous system sending out a starburst of axons in all directions, and some of those axons finding targets and persisting, and others failing and dying back. So the architecture of your nervous system is the result of a process of selection in which only some cells were successful.

Crucially, this radiation and die-off of axons happened very early in development, when a lot of what would become your guts was still hanging under your proportionally immense brain like the gondola on a blimp. This brings us to the recurrent laryngeal nerve.

Going back the way we came

The fates of your embryonic pharyngeal arches are complex and I’m not going to do a comprehensive review here (go here for more information). Suffice it to say that the first three arches give rise to your jaws and hyoid apparatus, the fourth and sixth form your larynx (voicebox), and fifth is entirely resorbed during development. Update: I made a pharyngeal arch cheat sheet.

There are two major nerves to the larynx, each of which is bilaterally paired. The nerve of the fourth pharyngeal arch becomes the superior laryngeal nerve, and it passes cranial to the fourth aortic arch. The nerve of the sixth pharyngeal arch becomes the inferior or recurrent laryngeal nerve, and it passes caudal to the sixth aortic arch. At the time that they form, both of these nerves take essentially straight courses from the brainstem to their targets, because you’re still in the blimp-gondola stage.

If you were a shark, the story would be over. The more posterior pharyngeal arches would persist as arches instead of forming a larynx, each arch would hold on to its artery, and the nerves would all maintain their direct courses to their targets.

The normal fate of the aortic arches in humans. From http://education.yahoo.com/reference/gray/subjects/subject/135

But you’re not a shark, you’re a tetrapod. Which means that you have, among other things, a neck separating your head and your body. And the formation of your neck shoved your heart and its associated great vessels down into your chest, away from the pharyngeal arches. This was no problem for the superior laryngeal nerve, which passed in front of the fourth aortic arch and could therefore stay put. But the inferior laryngeal nerve passed behind the sixth aortic arch, so when the heart and the fourth and sixth aortic arches descended into the chest, the inferior laryngeal nerve went with them. Because it was still hooked up to the brainstem and the larynx, it had to grow in length to compensate.

As you sit reading this, your inferior laryngeal nerves run down your neck into your chest, loop around the vessels derived from the fourth and sixth aortic arches (the subclavian artery on the right, and the arch of the aorta and ductus arteriosus on the left) and run back up your neck to your larynx. Because they do this U-turn in your chest and go back the way they came, the inferior laryngeal nerves are said to ‘recur’ to the larynx and are therefore more commonly referred to as the recurrent laryngeal nerves (RLNs).

An enlightening diversion

The RLN is the poster child for “unintelligent design” because it is pretty dumb. Your RLNs travel a heck of a lot farther to reach your larynx than they ought to, if they’d been designed. Surely an intelligent designer would have them take the same direct course as the superior laryngeal nerve. But evolution didn’t have that option. Tetrapod embryos could not be built from the ground up but had to be modified from the existing “sharkitecture” of ancestral vertebrates. The rules of development could not be rewritten to accommodate a shorter RLN. Hence Dawkins’s love affair with the RLN, which gets 7 pages in The Greatest Show on Earth. He also appeared on the giraffe episode of Inside Nature’s Giants, in which the RLN was dug out of the neck and the continuity of its ridiculous path was demonstrated–probably the most smack-you-in-the-face evidence for evolution that has ever been shown on television (said the rabid fan of large-tetrapod dissections).

Incidentally, the existence and importance of the RLN has been known since classical times. The RLN innervates the muscles responsible for speech, and on either side it passes right behind the thyroid gland, which is subject to goiters and tumors and other grotesque maladies. So a careless thyroidectomy can damage one or both of the RLNs; if one gets snipped, the subject will be hoarse for the rest of his or her life; if both are cut, the subject will be rendered mute. The Roman physician Galen memorably demonstrated this by dissecting the neck of an immobilized but unanesthetized pig and isolating the RLNs (Kaplan et al. 2009). One moment the poor pig was squealing its head off–as any of us would be if someone dug out our RLNs without anesthesia–and the next moment Galen severed the RLNs and the animal abruptly fell silent, still in unbelievable pain but now without a mechanism to vocally express its discomfort.

Galen versus pig. Figure 2 from Kaplan et al. 2009.

The name of the nerve also goes back to Galen, who wrote:

I call these two nerves the recurrent nerves (or reversivi) and those that come upward and backward on account of a special characteristic of theirs which is not shared by any of the other nerves that descend from the brain.

Like at least some modern surgeons, Galen does not seem to have been overly burdened by humility:

All these wonderful things, which have now become common property, I was the first of all to discover, no anatomist before me ever saw one of these nerves, and so all of them before me missed the mark in their anatomical description of the larynx.

Both of those quotes are from Kaplan et al. (2009), which is a fascinating paper that traces the knowledge of the recurrent laryngeal nerve from classical times to the early 20th century. If you’d like a copy and can’t get hold of one any other way, let me know and I’ll hook you up.

Share and share alike

By now you can see where this is going: all tetrapods have larynges, all tetrapods have necks, and all tetrapods have recurrent laryngeal nerves. Including giraffes, much to the delight of Richard Dawkins. And also including sauropods, much to the delight of yours truly.

Now, I cannot show you the RLN in a living sauropod, nor can I imagine a scenario in which such a delicate structure would be recognizably preserved as a fossil. But as tetrapods, sauropods were bound to the same unbreakable rules of development as everything else. The inference that sauropods had really long, really dumb RLNs is as secure as the inference that they had brainstems, hearts, and larynges.

Wedel (2012) Fig. 1. Course of the left vagus nerve and left recurrent laryngeal nerve in a human, a giraffe, and Supersaurus. The right recurrent laryngeal nerve passes caudal to the right subclavian artery rather than the aorta and ductus arteriosus, but otherwise its course is identical to that of the left.

Giraffes have necks up to 2.4 meters long (Toon and Toon 2003), so the neurons that make up their RLNs approach 5 meters in the largest indiividuals. But the longest-necked sauropods had necks 14 meters long, or maybe even longer, so they must have had individual neurons at least 28 meters long. The larynx of even the largest sauropod was probably less than 1 meter away from the brainstem, so the “extra” length imposed on the RLN by its recurrent course was something like 27 meters in a large individual of Supersaurus. Take that, Giraffa.

Inadequate giraffe is inadequate.

One way or another

It is possible to have a nonrecurrent laryngeal nerve–on one side, anyway. If you haven’t had the opportunity to dissect many cadavers, it may come as a surprise to learn that muscles, nerves, and blood vessels are fairly variable. Every fall in Gross Anatomy at WesternU, we have about 40 cadavers, and out of those 40 people we usually have two or three with variant muscles, a handful with unusual branching patterns of nerves, and usually half a dozen or so with some wackiness in their major blood vessels. Variations of this sort are common enough that the better anatomy atlases illustrate not just one layout for, say, the branching of the femoral artery, but 6-10 of the most common patterns. Also, these variations are almost always asymptomatic, meaning that they never cause any problems and the people who have them usually never know (ask Mike about his lonely kidney sometime). You–yes, you, gentle reader!–could be a serious weirdo and have no idea.

Variations in the blood vessels seem to be particularly common, possibly because the vessels develop in situ with apparently very little in the way of genetic control. Most parts of the body are served by more than one artery and vein, so if the usual vessel isn’t there or takes an unusual course, it’s often no big deal, as long as the blood gets there somehow. To wit: occasionally a person does not have a right subclavian artery. This does not mean that their right shoulder and arm receive no blood and wither away; usually it means that one of the segmental arteries branching off the descending aorta–which normally serve the ribs and their associated muscles and other soft tissues–is expanded and elongated to compensate, and looks for all the world like a normal subclavian artery with an abnormal connection to the aorta. But if the major artery that serves the forelimb comes from the descending aorta, and the 4th aortic arch on the right is completely resorbed during development, then there is nothing left on the right side to drag the inferior laryngeal nerve down into the torso. A person with this setup will have an inferior laryngeal nerve on the right that looks intelligently designed, and the usual dumb RLN on the left.

Can people have a nonrecurrent laryngeal nerve on the left? Sure, if they’ve got situs inversus, in which the normal bilateral asymmetry of the internal organs is swapped left to right. Situs inversus is pretty darned rare in the general population, occurring in fewer than 1 in 10,000 people. It is much more prevalent in television shows and movies, where the hero or villain may survive a seemingly mortal wound and then explain that he was born with his heart on the right side. (Pro tip: the heart crosses the midline in folks of both persuasions, so just shoot through the sternum and you’ll be fine. Or, if you’re worried about penetration, remember Rule #2 and put one on either side.) Anyway, take everything I wrote in the preceding paragraph, mirror-image it left to right, and you’ve got a nonrecurrent laryngeal nerve on the left. But just like the normally-sided person who still has an RLN on the left, a person with situs inversus and no remnant 4th aortic arch on the left (double variation alert!) still has an RLN looping around the aorta and ductus arteriosus on the right.

Bottom line: replumb the vessels to your arms, swap your organs around willy-nilly, you just can’t beat the aorta. If you have an aorta, you’ve got at least one RLN; if you don’t have an aorta, you’re dead, and no longer relevant to this discussion.

Nonrecurrent laryngeal nerves–a developmental Hail Mary?

But wait–how do we know that the inferior laryngeal nerve in embryonic sauropods didn’t get rerouted to travel in front of the fourth and sixth aortic arches, so it could be spared the indignity of being dragged into the chest later on?

First of all, such a course would require that the inferior laryngeal nerve take an equally dumb recurrent course in the embryo. Or maybe it should be called a procurrent course. Instead of simply radiating out from the central nervous system to its targets in the sixth pharyngeal arch, the axons that make up the RLN would have to run well forward of their normal course, loop around the fourth and sixth aortic arches from the front, and then run back down to the sixth pharyngeal arch. There is simply no known developmental mechanism that could make this happen.

Even if we postulated some hypothetical incentive that would draw those axons into the forward U-turn, other axons that took a more direct course from the central nervous system would get to the sixth pharyngeal arch first. By the time the forwardly-recurring axons finished their intelligently-routed course and finally arrived at the sixth pharyngeal arch, all of the innervation targets would be taken, and those axons would die off.

Also, at what point in the evolution of long necks would this forwardly-looping course supposedly be called into existence? Ostriches and giraffes have RLNs that take the same recurrent course as those of humans, pigs, and all other tetrapods. The retention of the recurrent course in extant long-necked animals is further evidence that the developmental constraint cannot be broken.

Finally, the idea that a non-recurrent laryngeal nerve would need to evolve in a long-necked animal is based on the perception that long nerve pathways are somehow physiologically taxing or otherwise bad for the animals in which they occur. But almost every tetrapod that has ever lived has had much longer neurons than those in the RLN, and we all get on just fine with them.

In dire extremity

Probably you seen enough pictures of neurons to know what one looks like: round or star-shaped cell body with lots of short branches (dendrites) and one very long one (the axon), like some cross between an uprooted tree–or better yet, a crinoid–and the Crystalline Entity. When I was growing up, I always imagined these things lined up nose to tail (or, rather, axon to dendrite) all down my spinal cord, arms, and legs, like boxcars in a train. But it ain’t the case. Textbook cartoons of neurons are massively simplified, with stumpy little axons and only a few to a few dozen terminals. In reality, each neuron in your brain is wired up to 7000 other neurons, on average, and you have about a hundred billion neurons in your brain. (Ironically, 100 billion neurons is too many for your 100 billion neurons to visualize, so as a literal proposition, the ancient admonition to “know thyself” is a non-starter.)

Back to the axons. Forget the stumpy little twigs you’ve seen in books and online. Except for the ganglia of your autonomic nervous system (a semi-autonomous neural network that runs your guts), all of the cell bodies of your neurons are located in your central nervous system or in the dorsal root ganglia immediately adjacent to your spinal cord. The nerves that branch out into your arms and legs, across your face and scalp, and into your larynx are not made of daisy chains of neurons. Rather, they are bundles of axons, very long axons that connect muscles, glands, and all kinds of sensory receptors back to the nerve cell bodies in and around your brain and spinal cord.

Indulge me for a second and wiggle your toes. The cell bodies of the motor neurons that caused the toe-wiggling muscles to fire are located in your spinal cord, at the top of your lower back. Those motor neurons got orders transmitted down your spinal cord from your brain, and the signals were carried to the muscles of your feet on axons that are more than half as long as you are tall.

Some of your sensory neurons are even longer. Lift your big toe and then set it down gently, just hard enough to be sure that it’s touching down on the floor or the sole of your shoe, but not hard enough to exert any pressure. When you first felt the pad of your toe touch down, that sensation was carried to your brain by a single neuron (or, rather, by several neurons in parallel) with receptor terminals in the skin of your toe, axon terminals in your brainstem, and a nerve cell body somewhere in the middle (adjacent to your sacrum and just a bit to one side of your butt crack, if you want the gory details). That’s right: you have individual sensory neurons that span the distance from your brainstem to your most distal extremity. And so does every other vertebrate, from hagfish to herons to hippos. Including, presumably, sauropods.

I had you set your toe down gently instead of pushing down hard because the neurons responsible for sensing pressure do not travel all the way from toe-tip to brainstem; they synapse with other neurons in the spinal cord and those signals have been through a two-neuron relay by the time they reach your brainstem. Ditto for sensing temperature. But the neurons responsible for sensing vibration and fine touch go all the way.

If you want to experience everything I’ve discussed in this post in a single action, put your fingertips on your voicebox and hum. You are controlling the hum with signals sent from your brain to your larynx through your recurrent laryngeal nerves, and sensing the vibration through individual neurons that run from your fingertips to your brainstem. Not bad, eh?

Wedel (2012) Fig. 2. The longest cells in the bodies of sauropods were sensory neurons that connected receptors in the skin of the extremities with interneurons in the brainstem, a pattern of neural architecture that is present in all extant vertebrates. The nerve cell bodies would have been located in the dorsal root ganglia adjacent to the spinal cord. The diagram of the neuron is based on Butler and Hodos (1996: fig. 2–1B).

Getting back to big animals: the largest giraffes may have 5-meter neurons in their RLNs, but some of the sensory neurons to their hindfeet must be more like 8 meters long. I don’t think anyone’s ever dissected one out, but blue whales must have sensory neurons to the tips of their flukes that are almost 30 meters (98 feet) long (subtract the length of the skull, but add the lateral distance from body midline to fluke-tip). And Supersaurus, Amphicoelias, and the like must have had neurons that were approximately as long as they were, minus only the distance from the snout-tip to the back of the skull. I could be wrong, and if I am I’d love to be set straight, but I think these must have been the longest cells in the history of life.

Oh, one more thing: up above I said that almost every tetrapod that has ever lived has had much longer neurons than those in the RLN. The exceptions would be animals for which the distance from brainstem to base of neck was longer than the distance from base of neck to tip of limb or tail, so that twice the length of the neck would be longer than the distance from base of skull to most distal extremity. In that case, the neurons that contribute to the RLN would be longer than those running from brainstem to tail-tip or toe-tip. Tanystropheus and some of the elasmosaurs probably qualified; who else?

Parting Thoughts

In this post I’ve tried to explain the courses that these amazingly long cells take in humans and other vertebrates. I haven’t dealt at all with the functional implications of long nerves, for which please see the paper. The upshot is that big extant animals get along just fine with their crazy-long nerves, and there’s no reason to assume that sauropods were any more troubled. So why write the paper, then? Well, it was fun, I learned a lot (dude: axoplasmic streaming!), and most importantly I got to steal a little thunder from those silly poseurs, the giraffes.

Department of Frivolous Nonsense: yes, I titled the paper after those TV ads for Chili’s hamburgers from a few years back. If you never saw them, the ads compared mass-produced, machine-stamped fast-food burgers with restaurant burgers painstakingly built by hand, and concluded with, “Chili’s Big-Mouth Burgers: monuments of inefficiency!”

Update: All of this is out of date now that the paper has been formally published. Department of Good Karma: since the paper is at the “accepted manuscript” stage, I still have the chance to make (hopefully minor) changes when I get the proofs. As is always, always, always the case, I caught a few dumb errors only after the manuscript had been accepted. Here’s what I’ve got so far, please feel free to add to the list:

  • Page 1, abstract, line 3: pharyngeal, not pharyngial
  • Page 1, abstract, line 8: substitute ‘made up’ for ‘comprised’
  • Page 6, line 12: substitute ‘make up’ for ‘comprise’
  • Page 9, line 5: citation should be of Carpenter (2006:fig. 3), not fig. 2
  • Page 10, line 7: “giant axons of squid are”, not ‘ares’
  • Page 12, entry for Butler and Hodos should have year (1996)
  • Page 12, entry for Carpenter has ‘re-evaluation misspelled
  • Page 16, entry for Woodburne has ‘mammalian’ misspelled

(Notes to self: stop trying to use ‘comprise’, lay off the ‘s’ key when typing bibliography.)

References

Thanks to everyone who joined in the discussion last time on why sauropods had such long necks.  I’ve discussed this a little with Matt, and we are both amazed that so many different hypotheses have been advanced (even if some of them are tongue-in-cheek).  We’ll probably come back to all these ideas later.

But today, we want to draw your attention to a new contribution to this discussion — a paper in the Journal of Zoology, with the tell-it-like-it-is title “The long necks of sauropods did not evolve primarily through sexual selection”, written by the three of us SV-POW!er rangers together with our buddy Dave “Archosaur Musings” Hone (Taylor et al. 2011).

Taylor et al. (2011), fig. 1: Sauropod necks, showing relationships for a selection of species, and the range of necks lengths and morphologies that they encompass. Phylogeny based on that of Upchurch et al. (2004: fig. 13.18). Mamenchisaurus hochuanensis (neck 9.5 m long) modified from Young & Zhao (1972: fig. 4); Dicraeosaurus hansemanni (2.7 m) modified from Janensch (1936: plate XVI); Diplodocus carnegii (6.5 m) modified from Hatcher (1903: plate VI); Apatosaurus louisae (6 m) modified from Lovelace, Hartman & Wahl (2008: fig. 7); Camarasaurus supremus (5.25 m) modified from Osborn & Mook (1921: plate 84); Giraffatitan brancai (8.75 m) modified from Janensch (1950: plate VIII); giraffe (1.8 m) modified from Lydekker (1894:332). Alternating grey and white vertical bars mark 1 m increments.

This is one of those papers that has been literally years in the making, which is why it’s a rather belated response to the paper that we were responding to — Phil Senter’s (2006) argument that sexual selection was the primary driver of neck elongation in sauropods.

Senter supported his hypothesis by laying out six predictions which he argued should be true for sexually selected necks; then showing that, while the first two could not be assessed, the last four all supported sexual selection.  In our paper, we do three things.  First, we make the point that sexual selection and feeding advantage are not mutually exclusive.  Second, we revisit all six predictions and show that they do not in fact support sexual selection — in fact, most of them provide support for feeding advantage.  Finally, we show that no tetrapod clade comparable with Sauropoda has consistently selected for a single sexual signal.

My email records show that Darren, Matt and I were discussing this as early as 22 September 2006, just six weeks after Senter’s paper was published, and that we started working on a response only a couple of days later.  But as so often happens, it got crowded out by a hundred other things.  Then in November 2007 Dave Hone mentioned that he was independently thinking of writing a response, and we decided to join forces.  And then … we all went back to working on other things again, touching on the necks-for-sex issue every now and then.  It’s mostly due to Dave’s repeated prods that this project wasn’t allowed to wither away, and has now, finally, made it across the finish line.

Like the neck-posture paper (Taylor et al. 2009), this was a true collaboration — one of those where, for many parts of the text, none of us is sure which of us originally wrote it.  It went through the wringer many times before reaching its final form, and most of the text must have been rewritten two or three times along the way.  We hope all the shuffling and polishing has resulted in a paper that reads straightforwardly and even seems obvious.  “When something can be read without effort, great effort has gone into its writing” — Enrique Jardiel Poncela.  That’s the goal, anyway.

The paper itself is available at the link below, so take a look and see whether you find our argument convincing.  As always, comments are open!

Update (the next morning)

Co-author Dave Hone discusses this paper on his own blog.

References

Coombs’s chimaera

April 7, 2011

“Sauropods are basically alien animals . . . What can be said of the habits of an animal with the nose of a Macrauchenia, the neck of a giraffe, the limbs of an elephant, the feet of a chalicothere, the lungs of a bird, and the tail of a lizard? With so many plausible but conflicting interpretations, it is unlikely there will be general agreement on sauropod habits as long as more than one paleontologist has an opinion on the matter.”

–Walter Coombs, 1975, “Sauropod habits and habitats”, page 29

I first encountered that passage at age 9, in The Dinosaurs, by William Stout, William Service, and Bryon Preiss. Peter Dodson quoted it in his introduction to the book, and it really stuck in my head. So much so that I quoted it myself when the opportunity arose, and now present it here for your consideration. More recent investigations have pretty well done in the idea that sauropods had trunks (for more about that, go here [which will lead you to this, which I had completely forgotten that I wrote, but quite like now that I've rediscovered it]), but the rest of Coombs’s comparisons are still apt. I had no idea when I was 9 how long a shadow the “lungs of a bird” part would cast over my life! And certainly there are aspects of sauropod biology that are still contentious, and some may always be so.

But I really feel like a synthetic view of sauropod paleobiology is emerging, and the best evidence of it to date is the massive paper by Sander et al. (2010) in Biological Reviews. That paper is one of the zillion things I’ve been intending to blog about, but have not gotten around to yet (and there’s a book by most or all of the same folks due shortly from Indiana University Press). When I read it right after it came out, I had the very strong feeling that it was a watershed moment for sauropod paleobiology, such that it will be fair to ask of any future study, “How is this an advance beyond Sander et al. (2010)?” I like papers like that–Coombs (1975) was one such–because they inspire me to start figuring out what’s going to come next.

References

This tutorial is based on all the things that I stupidly forgot to do along the way of tearing down the juvenile giraffe neck that Darren, John Conway and I recently got to take to pieces.  At half a dozen different points in that process, I found myself thinking “Oh, we should have done X earlier on!”  So it’s not a tutorial founded on the idea that I know how this should be done; it’s about how I am only now realising how it should be done, off the back of my dumb mistakes.

Cervical vertebra 5 of two-week-old giraffe: left column, anterior; middle column, top to bottom, dorsal, left lateral, posterior, all with anterior to the left; right column, posterior

What you want is to get the maximum possible information out of your specimen.  At each stage of preparation, information is lost — a necessary evil, because of course at the same time new information becomes available.  So don’t miss anything early on.

The whole neck

If you’re lucky, you’ll get the complete, intact neck to work with.  (Ours was not quite intact, having been skinned, and lost an indeteminate amount of superficial muscle and ligament in the process.)  So before you start cutting, photograph the neck in dorsal, ventral, lateral, anterior and posterior aspects.

Next, you want to measure the neck:

  • total mass
  • total length, front of atlas to back of last centrum.
  • maximum flexion (i.e. downwards bend)
  • maximum extension (i.e. upwards bend)
  • maximum deflection (i.e. lateral bend)

These last three are hard to do, because “maximum” flexion, extension and deflection are not exact things.  You can always push or squeeze or bend a bit harder.  These are the unpleasantly messy aspects of working with animals rather than robots — most kinds of tissue are flexible and resilient.  You just have to do the best you can, and supplement your measurements with photographs of the neck bent in each direction.

Skinning

Now you’re ready to start taking that baby apart.  Get the skin off, then redo all your photos and redo all your measurements — yes, even total length, even though you “know” removing the skin can’t affect that.  Because you don’t know what you don’t know.  Does removing the skin affect the maximum range of movement?  How much of the neck’s total mass was due to the skin?  Weigh the skin as well: does its mass added to that of the deskinned neck add up to that of the intact neck?  If not, is the discrepancy due to blood loss?

Stripping muscle

Once the skin is off, you can start removing muscles.  Ideally, you want to identify each muscle as you go, and remove them one by one, so that you leave the major ligaments behind.  In practice this is harder than it sounds, because the muscles in real necks are, inconveniently, not clearly delineated and labelled like the ones in books.  Still, going slowly and carefully, it’s often possible to avoid cutting actual muscles but just the fascia between them, which allows you remove complete muscles.  Done well, this can leave in place not only the nuchal ligament running along the top of all the neural spines, but the shorter ventral ligaments joining adjacent vertebrae.

John (left) and Darren (right) removing muscle from the giraffe neck (in right lateral aspect), while keeping ligaments intact

As you’re doing this, you want to avoid damaging the intercentral joints and the zygapophyseal capsules, so far as possible.  You’ll probably find it easy to preserve the former, which are tough, but harder not to accidentally damage at least some of the latter.  You want to keep them intact as far as possible, so you can see how the react when you manipulate the neck.  (Do these manipulations gently, or you’ll tear those capsules.)

Now that the skin and muscles are both off — at least, so far as you can remove the muscles, which will not be completely — you can redo all your photos and redo all your measurements again.  Yes, all of them.  Because you just can’t tell what you’re going to be interested in later, and curse yourself for missing.

Stripping ligament

Go right ahead.  Remove the short ligaments, and do your best to get the nuchal ligament off all in one chunk — not quite as easy as it sounds, because it doesn’t just sit on top of the neural spines, but sort of encloses them.  Measure the nuchal ligament at rest, then stretch it out as far as you can and measure it extended.  Calculate how far it stretched as a proportion of the rest length.  Compare this with what you learned from Alexander (1989:64-65).  Hmm.  Interesting, no?

You can guess what’s coming now: redo all your photos and redo all your measurements yet again.  You should find that the total length is the same, but who knows what you might find about changing flexibility?  Also, your progressive sequence of mass measurements will tell you what proportion of the whole neck was skin, muscle, ligament, etc.

Separating the vertebrae

This sounds like it should be easy, but it’s not.  The zygapophyses will come apart very easily, but the centra will be held firmly together with very dense connective tissue which has be cut carefully away, piece by piece, with the blade of a scalpel worked between the condyle of one vertebra and the cotyle of the next.  (I’m writing here about a giraffe neck, but I’m confident the same will be true of other artiodactyls and maybe most mammals; bird necks are different.)

Once you’ve got the vertebrae separate, photograph each vertebra separately, from each of the cardinal directions. Also, measure each vertebra separately — especially for centrum length, but you may as well get all the major measurements.  These measurements will include the cartilage caps at the front and back of each centrum.  (This is the step that I most regret missing out.)

Articulate the vertebrae in “neutral pose” by keeping the centra in full contact and rotating each intercentral joint about its midpoint until the corresponding zygapophyses are maximally overlapped.  What does this pose look like?  How does it compare to the animal’s habitual pose in life?  (If possible, compare with the pose shown by an X-ray of the live animal, since necks lie.)

Articulate the vertebrae in positions of “maximal” flexion, extension and deflection by keeping the centra in full contact and rotating each intercentral joint about its midpoint until the corresponding zygapophyses are displaced to a degree of your choosing.  Try it with the zygs allowed to slide until they are 50% disarticulated, then with 75% disarticulation, then displacing until they are just past the point of contacting each other.  Photograph all these poses and measure their deflection.  Compare these variant poses with those obtained when the vertebrae were still joined together, and when the ligaments, muscles and skin were still in place.  What degree of zygapophyseal disarticulation best matches the whole-neck bending ability?  How does this vary along the neck?  How does that this compare with what you may have been led to expect in the literature.  Hmm.

Using your earlier photos of the whole neck’s bending profile, arrange the vertebrae in the exact same pose.  How much do the zygapophyses disarticulate in these poses?  As you rotate the joints about the articulation of their centra, do the zygs just slide neatly past each other, or do they move far apart from each other as the neck bends?  Interesting, yes?

Cleaning the vertebrae

Have you recorded all the information you need from the intact vertebrae with their cartilage in place?  If you’re sure, then …

Lightly simmer the vertebrae for an hour or so, then remove the excess flesh by hand and using a toothbrush.  Repeat as needed to get them clean.  If you can do this really carefully — I couldn’t — you may be able to keep the cartilage firm, and firmly articulated with the bone.  (Bugging the vertebrae is probably a better approach for this purpose, but I find it hard to be that patient.)

Once the vertebrae have dried out — and especially, once their cartilage is dry — re-measure each vertebra.  Does the drying of the cartilage affect the centrum length?

Simmer the vertebrae again and gently peel off the cartilage caps at the front and back of each centrum.  Re-measure the centra: how long are they now?  What proportion of each centrum’s length was cartilage?

Articulate all the centra in a straight line, and measure the total length.  How does this compare with the whole-neck length you started with?  [Crib-sheet answer for our baby giraffe: 41 cm vs. a whole-neck length of 51 cm.  Expect a closer match if you're dealing with an adult animal,which will have proportionally less cartilage.]

Articulate the vertebrae in “neutral pose” as you did back when the individual vertebrae were complete.  How does the new “neutral pose” compare with the old one?  With habitual life posture?  Huh.  Makes you think, doesn’t it?

Nearly done …

Articulate the vertebrae in positions of “maximal” flexion, extension and deflection as you did before, and compare your results with those from when the vertebrae were complete with their cartilage caps.  Well!  Who’d have thought?

Now remember that the fossils we have of, say, sauropod cervicals are those of the dry bone only, with no cartilage.  Think about how different the “neutral pose” and range of movement would be if we had the intact vertebrae with their cartilage.

Dammit all, I’ve given the game away

As I wrote this article, I found myself giving away more and more of a paper I’ve been planning to write, in which I go through essentially this process with a couple of necks, ideally from very different clades, and write up the results.  Say, a giraffe, an ostrich and  a croc.  The extent to which the dry-bone postures and flexibility vary from those of the live animals would give us a reasonable starting point for thinking about how life postures and flexibility of sauropods might have varied from what we’d deduce from the dry bones alone.

Wouldn’t that be a great little paper?

Well, I might still write it when I find the time, but I won’t stand in the way of anyone else who wants to plough straight in and just get it done.  (You might mention me in the acknowledgements if you do.)


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