Tetrapod Zoology

If asked “Why do giraffes have such long necks?”, the majority of people – professional biologists among them – will answer that it’s something to do with increasing vertical reach and hence feeding range. But while the ‘increased vertical reach’ or ‘increased feeding envelope’ hypothesis has always been the most popular explanation invoked to explain the giraffe’s neck, it isn’t the only one.

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ResearchBlogging.org

In 1996, Robert Simmons and Lue Scheepers argued that the giraffe neck functions as a sexual signal: they said that the necks of males are bigger and thicker than those of females, that the necks of males continue growing throughout life, that females prefer males with bigger necks, and that giraffe necks don’t provide any obvious benefit in vertical reach or foraging range, contra the ‘traditional’, ‘increased feeding envelope’ hypothesis (Simmons & Scheepers 1996). This has become known as the ‘necks for sex’ hypothesis [obvious sexual dimorphism in giraffes (Giraffa camelopardalis angolensis/G. angolensis) shown above; image by Hans Hillewaert, from wikipedia].

‘Necks for sex’ visits the Mesozoic

It was only a matter of time before someone published the idea that the ‘necks for sex’ hypothesis might apply to another group of tetrapods famous for their long necks – namely, the sauropod dinosaurs.

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In a well argued and extremely popular* Journal of Zoology article, Phil Senter wondered whether sauropod necks might also have evolved under pressure from sexual selection, and not because of any ecological benefit that they might have incurred (Senter 2007) [adjacent figure – from Senter (2007) – shows that surprise!! sauropods have long necks relative to theropods**. The reconstructions are by Greg Paul]. Senter put forward six predictions that – if validated – would indicate the importance of sexual selection in the evolution of the sauropod neck, most of which related to the possibility of sexual dimorphism, the use of the neck in dominance or courtship displays, its redundancy as an adaptation for increased reach in feeding, and allometric increase in neck length across ontogeny and phylogeny. His conclusion was essentially that, yes, the sauropod neck likely evolved primarily under sexual selection pressure (Senter 2007).

* The Journal of Zoology website lists the article as one of the ‘top 3 downloaded papers from 2007 and 2008′.

** Senter (2007) actually used this diagram to show that “acetabular height is a good proxy for the height of the base of the neck in a sauropod and for the height of the mouth in a large theropod” (p. 47) (his implication being that the neck incurred a significant survival cost).

The montage below could be seen as a contrast between the two supposedly competing hypotheses. At top, we have some displaying Sauroposeidons (by Brian Engh of dontmesswithdinosaurs.com), perhaps imagined as per the ‘necks for sex’ hypothesis, while at bottom we have high-browsing Morrison Formation sauropods (by Greg Paul), imagined as per the ‘increased feeding envelope’ hypothesis.

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Senter (2007) has been widely read and also cited in favourable contexts both in the dinosaur literature (Sander & Clauss 2008, Mateus et al. 2009, Siegwarth et al. 2010) and in the general literature on sexual selection (Swallow et al. 2009). Surprisingly, no one has said anything negative about it in print; I say that this is surprising because the data does not support Senter’s predictions at all, and it’s for this reason that I worked together with Mike P. Taylor, Dave Hone and Matt Wedel to produce a counter-argument (Taylor et al. 2011). These three authors will be rather familiar names if you follow the palaeo-blogosphere… and that Naish guy, I think he blogs too.

Anyway, the fruit of our labours has just been released to the world (in digital form, anyway) in the online version of Journal of Zoology (Taylor et al. 2011). Given that this is where Senter’s original article appeared, it seems obviously fitting that our response appear there too.

When disagreements arise

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Before I discuss our new paper further, one more bit of preamble. There are two perspectives on what to do when you encounter a published paper that you disagree with. Some people say that you should ignore the offending bit of research entirely and hope that it will simply sink into the morass of obscurity. This can work, since there are hundreds of academic articles out there that are hardly read by anyone, are mostly un-cited, and just aren’t influential enough to mislead future students. Furthermore, even an unfavourable citation is still a citation, and in today’s world this apparently means something.

The second perspective is that researchers have a duty to use the peer-reviewed literature to correct errors and misinterpretations in the works of others. Naïve readers might otherwise see the offending published item, find that it’s unchallenged, and then assume that it represents the state-of-play in the respective field. The result is that an erroneous or spurious claim can become widespread ‘common knowledge’, or even ‘textbook dogma’. The following quote is relevant to so-called scientific creationism and most certainly not to Phil’s ‘necks for sex’ paper, but it always sticks in my mind: “If knowledgeable people keep quiet, it only helps those who spread nonsense” (Aykut Kence, quoted in Koenig (2001)).

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My perspective is that – if time and opportunity allows (if) – scientists should indeed take the time to respond appropriately to literature that they find fault with, otherwise it does become ‘accepted’. Furthermore, I’m of the (possibly naïve) opinion that scientists have a moral obligation to engage with both their research community and human consciousness as a whole, not to simply work in isolation while pushing out their own cherished technical contributions. The fact that it took us about five years to respond to Phil’s paper shows that we didn’t – and, indeed, couldn’t – prioritise our response (one reason for the delay is that we wanted to get the neck posture paper (Taylor et al. 2009) published first), but I hope you agree that we did the right thing in responding eventually (Taylor et al. 2011). Phil has been a complete gentleman about it and is pleased that his hypothesis has been critically examined.

The data we have does not support the ‘necks for sex’ hypothesis

Without discussing the ins and outs of the paper in entirety, we go through all of Phil’s proposals and show either (1) that they don’t support the sexual selection hypothesis, but are actually more consistent with the ‘feeding envelope’ hypothesis, (2) that they just can’t be tested, because we don’t have enough evidence, or (3) are equivocal, and aren’t necessarily linked with sexual selection. [Diagram below, from Taylor et al. (2011), shows some of the variation in neck length present across Sauropoda, mapped onto a phylogeny. The alternating vertical bands mark one-meter increments. That crappy little animal at bottom left is Giraffa].

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So, we have no evidence whatsoever of sexual dimorphism in sauropod necks. We can’t say anything about use of the sauropod neck in courtship or dominance. The presence of positive allometry in neck length is not – contra Senter (2007) – indicative of sexual selection since positive allometry occurs all over the shop in animal morphology, and positive allometry is far from ubiquitous in sexually selected features anyway (Taylor et al. 2011).

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And while Senter (2007) argued that the long necks of sauropods didn’t pose an obvious foraging benefit (he followed Martin (1987) and Stevens & Parrish (1999) in assuming that sauropod necks were mostly semi-horizontal), newer work (Taylor et al. 2009) has shown that the assumptions underlying these studies were in error. Even better, even if Martin (1987) and Stevens & Parrish (1999) are correct, their conclusions are still consistent with the notion of an increased ‘feeding envelope’. In fact, Martin (1987) very specifically framed his notion of subhorizontal-necked sauropods within the ‘feeding envelope’ hypothesis (one of John Martin’s ‘feeding envelope’ diagrams is shown here).

Giraffes and giant tortoises – together at last!

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The backbone to Senter’s ‘necks for sex’ idea comes from the hypothesis as originally formulated for giraffes (Simmons & Scheepers 1996). But in recent years it hasn’t been doing all that well, and in fact has been widely questioned in the giraffe literature (Cameron & du Toit 2007, Mitchell et al. 2009, Simmons & Altwegg 2010, Van Sittert et al. 2010). In fact some authors (though – note – not all) would go as far as saying that it’s been falsified. Regardless, most authors who specialise on giraffes have concluded that the ‘increased feeding envelope’ hypothesis is more likely to have been the main pressure affecting neck elongation in these animals [adjacent image of high-browsing giraffe by Steve Garvie, from wikipedia].

So, to emphasise: the hypothesis that sexual selection was/is the primary selective mechanism acting on the giraffe neck has been found wanting (I wrote about this on Tet Zoo in February 2007). This work is recent, so naturally Senter (2007) couldn’t and didn’t cite it. Incidentally, Senter (2007) was available in online form in August 2006; it’s only the printed version that appeared in 2007. In the paper, we opted to recognise the date of digital publication – hey, Mike P. Taylor is first author – but, in this article, I’ve followed the citation as given on the Journal of Zoology website.

One problem that Senter (2007) could have addressed, however, is the implication throughout his paper that the ‘feeding envelope’ hypothesis is mutually inconsistent with the sexual selection hypothesis. In other words, that it’s one or the other. As we argue in our paper, living animals show that dichotomies such as this are rare, with many/most structures being co-opted for more than one role (Taylor et al. 2011). This isn’t just true for such sexually-selected organs as horns, antlers, tusks and so on, it’s also definitely the case for long necks.

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Giraffe necks are used in increasing foraging range, but they have a sociosexual role too. In our paper we draw special attention to long-necked Galápagos giant tortoises, partly because I continue to be frustrated by the fact that people ignore these long-necked, high-reaching browsers just about whenever they discuss long necks and high browsing. Work shows that Galápagos giant tortoises use the neck to increase feeding range, but they also use their vertical reach to intimidate other tortoises when fighting or establishing status (Fritts 1984) (as shown here: this image is redrawn from a photo and is not a hypothetical scene).

And mentioning Galápagos giant tortoises gave me the excuse to produce some fine, kick-ass pictures of tortoises doing battle, stomping iguanas, chasing off giant hawks… naah, kidding, I drew them feeding and staring at each other. People should definitely talk about Galápagos giant tortoises more whenever they consider long necks and high browsing. And it still seems all too poorly known that even longer-necked giant tortoises existed until very recently: I’m referring to the Cylindraspis species of the Mascarenes [life-sized model of Rodrigues saddle-backed tortoise C. vosmaeri shown below. Model created by Nick Bibby of Rungwe Kingdon and Claude Koenig’s sculpture foundry Pangolin Editions].

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Incidentally, we made a dreadful error that I don’t think we’ll ever live down… we spoke of Galápagos tortoises as if they belong to Geochelone whereas – as everyone knows – Geochelone of tradition is “rampantly polyphyletic” (Le et al. 2006). Consequently, Galápagos tortoises are nowadays classified within Chelonoidis (Le et al. 2006). We also refer to the Galápagos giant tortoise taxa as if they’re ‘subspecies’. That arrangement is still preferred by some, but workers increasingly prefer to regard them as ‘species’ (e.g., Russello et al. 2010). I dropped the ball on this one and apologise profusely to my co-authors. That well known expert on testudine phylogeny and taxonomy, Thomas R. Holtz, jr., is warmly thanked for bringing all of this to our attention. In the photo below, Tom demonstrates his turtle credentials (he’s the one on the right, with the hat. And glasses).

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As I’ve said, the paper is actually rather complex and we went into an appropriate amount of detail in responding to Phil’s original paper. That isn’t because we’re wordy writers; it’s because the arguments involved are complex and there are various diversions and dead-ends that we needed to explore (I mostly haven’t mentioned those here… cough cough blood pressure, mutual sexual selection cough cough). It must be said that we were able to formulate a clearly structured, (hopefully) easy-to-follow argument because we followed the eloquent structure used beforehand in Senter (2007). We evidently don’t agree with Phil’s reasoning, but we admire the way he crafted his hypothesis.

It may not be well known outside of Mesozoic archosaur research, but a minor renaissance on sexual selection and the evolution of display structures is currently underway in the dinosaur and pterosaur literature. Our paper is merely the latest volley in what is turning out to be an increasingly interesting debate. To conclude, Taylor et al. (2011) show – pretty convincingly, we hope – that sexual selection was not (so far as we can tell) the primary pressure driving the remarkable elongate necks of sauropods, but this is far from the last word on the subject.

My co-authors have covered Taylor et al. (2011) too. See Dave Hone’s take over at Archosaur Musings and the SV-POW! perspective here. You can download the paper yourself here.

And for previous articles on giraffe necks, sauropod necks and the debates surrounding them, please see…

Refs – –

Cameron, E. Z. & du Toit, J. T. 2007. Winning by a neck: tall giraffes avoid competing with shorter browsers. The American Naturalist 169, 130-135.

Fritts, T. H. 1984. Evolutionary divergence of giant tortoises in Galapagos. Biological Journal of the Linnean Society 21, 165-176.

Koenig, R. 2001. Creationism takes root where Europe, Asia meet. Science 292, 1286-1287.

Le, M., Raxworthy, C. J., McCord, W. P. & Mertz, L. 2006. A molecular phylogeny of tortoises (Testudines: Testudinidae) based on mitochondrial and nuclear genes. Molecular Phylogenetics and Evolution 40, 517-531.

Martin, J. 1987. Mobility and feeding of Cetiosaurus (saurischia, sauropoda [sic]) – why the long neck? In Currie, P. J. & Koster, E. H.(eds) Fourth Symposium on Mesozoic Terrestrial Ecosystems, Short Papers. Boxtree Books (Drumheller, Alberta), pp. 154-159.

Mateus, O., Maidment, S. C. R. & Christiansen, N. A. 2009. A new long-necked ‘sauropod-mimic’ stegosaur and the evolution of the plated dinosaurs. Proceedings of the Royal Society, London B 276, 1815-1821.

Mitchell, G., van Sittert, S. J. & Skinner, J. D. 2009. Sexual selection is not the origin of long necks in giraffes. Journal of Zoology 278, 281-286.

Russello, M. A., Poulakakis, N., Gibbs, J. P., Tapia, W., Benavides, E., Powell, J. R. & Caccone, A. 2010. DNA from the past informs ex situ conservation for the future: an ”extinct” species of Galápagos tortoise identified in captivity. PLoS ONE 5(1): e8683. doi:10.1371/journal.pone.0008683

Sander, P. M. & Clauss, M. 2008. Sauropod gigantism. Science 322, 200-201.

Senter, P. 2007. Necks for sex: sexual selection as an explanation for sauropod dinosaur neck elongation. Journal of Zoology 271, 45-53.

Siegwarth, J. D., Smith, C. N. & Redman, P. D. 2010. An alternative sauropod physiology and cardiovascular system that eliminates high blood pressures. Lethaia 44, 46-57.

Simmons, R. E. & Altwegg, R. 2010. Necks-for-sex or competing browsers? A critique of ideas on the evolution of giraffe. Journal of Zoology 282, 6-12.

– . & Scheepers, L. 1996. Winning by a neck: sexual selection in the evolution of giraffe. The American Naturalist 148, 771-786.

Stevens, K. A. & Parrish, J. M. 1999. Neck posture and feeding habits of two Jurassic sauropod dinosaurs. Science 284, 798-800.

Swallow, J. G., Hayes, J. P., Koteja, P. & Garland, T. Jr. 2009. Selection experiments and experimental evolution of performance and physiology. In Garland, T. Jr & Rose, M. R. (eds). Experimental Evolution: Concepts, Methods, and Applications of Selection Experiments. California University Press, Berkeley, pp. 301-352.

Taylor, M. P., Wedel, M. J. & Naish, D. 2009. Head and neck posture in sauropod dinosaurs inferred from extant animals. Acta Palaeontologica Polonica 54, 213-220.

Taylor, M. P., Hone, D. W. E., Wedel, M. J., & Naish, D (2011). The long necks of sauropods did not evolve primarily through sexual selection Journal of Zoology : 10.1111/j.1469-7998.2011.00824.x (pdf here)

Van Sittert, S. J., Skinner, J. D & Mitchell, G. 2010. From fetus to adult – an allometric analysis of the giraffe vertebral column. Journal of Experimental Zoology Part B: Molecular and Developmental Evolution 314, 469-479.

Comments

  1. #1 DMA
    May 18, 2011

    Is this from Tet Zoo Version 1. I remember this article, especially that picture of all attacking each other.

  2. #2 Bill
    May 18, 2011

    Excellent stuff – this paper (Senter) was a particular bug bear of mine (not enough that I did anything about it of course, apart from mutter into my beer). JZO also published a paper recently examining the sexual selection claim for giraffes and I was hoping that someone would do the same for the ‘necks for sex’ paper. I’d like to second Darren here that this does not mean that the original papers on both giraffes and sauropods weren’t excellent too; just not, in the end, scientifically convincing. I’m so glad that you report the author as happy to see his idea tested further, even if found wanting in the end. That’s the way it should be.

  3. #3 Darren Naish
    May 18, 2011

    Thanks, Bill. On your latter sentiment, there’s a brilliant anecdote related by Richard Dawkins where a former Oxford lecturer – well known for promoting a particular heterodox hypothesis – was eventually given what you might call an atomic smackdown at a seminar. He stood up, and confronted the speaker with “My dear fellow, I wish to thank you. I have been wrong these fifteen years”.

  4. #4 Mike Taylor
    May 18, 2011

    Thanks for this write-up, Darren — very nicely done. And especially thanks for mentioning Phil Senter’s gracious response to being informed about our paper. (I have a bunch more papers in the pipeline that are basically about contradicting models that have been proposed for sauropod palaeobiology, and sometimes worry about seeming too negative. It helps to see a positive response from someone like Phil.)

    DMA, have you been paying attention? This article is about a paper that came out five days ago; so, no, it’s not from Tet Zoo Version 1!

  5. #5 Patrick Murphy
    May 18, 2011

    Ever since I first read the Tet Zoo, “Necks for Sex,” article way back, it was always creeping in the back of my mind whether the argument had been made for sauropod necks. Seeing Brian Engh’s awesome illustration only reinforced the notion that Necks for Sex was out there for sauropods. Glad to see that thorough examinations of the hypothesis are out there. I agree that increased feeding range was the driving force behind the evolution of the neck’s elongation, but the paleoartist in me still finds Necks for Sex appealing (and as Darren mentioned in the article, the two are not mutually exclusive).

    Also…

    “The backbone to Senter’s ‘necks for sex’ idea…”

    Great Pun!

  6. #6 Marcus Good
    May 18, 2011

    I feel bad for giggling at some unintentional innuendo, hidden in the references..

  7. #7 derek
    May 18, 2011

    [from Darren: sorry, delayed by spam filter]

    You know the old joke “Why are [animal’s] legs so long? They have to be that long to reach the ground!” I thought that was an important reason for giraffe necks. Given that their legs are long (presumably for good and sufficient reason of their own), the giraffe needs to be able to reach down to the water to drink, as in these images.

    I admit this says nothing about sauropods or tortoises.

  8. #8 DMA
    May 18, 2011

    You know, I just realized that nobody’s ever applied this theory to azdarchid necks. Mark Witton did show the males with more hair on their necks but thats about it.

  9. #9 John Harshman
    May 18, 2011

    I’m fairly shocked not to find “Is the Guinea Pig a Rodent?” in your wastebasket.

  10. #10 metridia
    May 18, 2011

    “In fact, Martin (1987) very specifically framed his notion of subhorizontal-necked sauropods within the ‘feeding envelope’ hypothesis (one of John Martin’s ‘feeding envelope’ diagrams is shown here).”

    Of course, also there is the lateral expansion of the feeding envelope with a long neck- one pictures sort of the Weedeater (TM) of the dinosaur world swinging back and forth, at least for the diplodicoids.

  11. #11 heteromeles
    May 18, 2011

    “Cough cough blood pressure” indeed! While I liked the paper, I’m still trying to figure out how something with that much hollow bone dealt with those presumably enormous blood pressure shifts when it goes from drinking to feeding. “We’re working on it” is scarcely the most elegant response.

    I haven’t read the Siegwarth et al. paper, and so far I’ve figured out two explanations:

    1.Sauropods had such tough, pressure-vessel hides that theropod teeth bounced off when they tried to bite them, and Stegosaurs evolved their tail spikes specifically to make sauropods pop like punctured car tires. (This to insure that there was more browse for the stegosaurs). Or

    B. Sauropod brains did in fact cease functioning (pass out) as their heads rose. However, sauropods had so much neural matter in other parts of their bodies that this temporary shutdown in the cephalic segment wasn’t fatal. The rest of the nervous system would simply take over thinking for it for a while. The sauropod’s head would eventually recover consciousness to find its head at eating level, at which point it would simply start feeding. Call this one the thinking with your pelvic neurons, or some such.

  12. #12 Mike Taylor
    May 18, 2011

    Heteromeles, I agree that “we’re working on it” isn’t a particularly compelling rebuttal of Seymour’s haemodynamic limits argument. Unfortunately, it’s the nature of this kind of work that we can’t say much more without giving the game away — and we do want to get a publication out of this! If it’s any consolation, the manuscript as we submitted it was a little more emphatic, citing “Taylor and Wedel in prep.”, but J. Zoo doesn’t allow in-prep citations, so we downgraded it.

    This blood-pressure issues has been rumbling on for a long time, and I know that Seymour is finding it understandably frustrating that we keep saying “Oh, we’re not so sure about that” but not backing it up. I’m afraid all we can do at this point is ask you (and him!) to keep being patient.

  13. #13 heteromeles
    May 18, 2011

    Harumph! Well, I guess I’ll just have to wait then.

    (grumble, grumble. Just so long as it doesn’t involve using the anus for pressure equilibration…)

  14. #14 Dave Hone
    May 18, 2011

    “Harumph! Well, I guess I’ll just have to wait then.”

    Well you could fill some time reading the Siegwarth et al paper couldn’t you?

  15. #15 heteromeles
    May 18, 2011

    “Well you could fill some time reading the Siegwarth et al paper couldn’t you?”

    Not unless someone sends me a copy. I’m not at a research institution, and the local university only has it online, where I can’t access it.

    The abstract is less than informative–“A large sauropod needs a way to deal with very high blood pressure when high browsing. Arterial pumping is suggested here as a means of avoiding the need for high blood pressure.” Really? Are there animals that do arterial pumping?

    This also suggests that sauropod heads explode when the animal drops its head to drink. Or, alternatively, their brains runs low on oxygen while they drink, because the arteries stop pumping blood when the head is down.

  16. #16 Dave Hone
    May 18, 2011

    [from Darren: sorry, delayed by spam filter]

    Well you can ask people for a copy. Authors *like* people reading their papers – ask them. Or check out various online indices, or ask other interested parties.

    http://svpow.wordpress.com/2010/11/09/tutorial-9-how-to-get-copies-of-academic-papers/

  17. #17 Owlmirror
    May 18, 2011

    Naïve readers might otherwise see the offending published item, find that it’s unchallenged, and then assume that it represents the state-of-play in the respective field.

    Naïve reader? That would be me…

    And hey, I recognize the title one of the papers in that bin! (I would guess that the ornithological one is by BANDits).

    A few years back, I read a summary of hybridogenesis in Acquiring genomes: A theory of the origins of species by Lynn Margulis and Dorion Sagan. But while my first thoughts were “Wow! That is so weird! How interesting!”, these were countered by noting, in the book itself, a certain degree of eccentricity of expression, and later finding out that Margulis had developed, ahem, a certain reputation as a rather extreme eccentric (to put it as politely as possible).

    Then I started wondering… wouldn’t it be kinda obvious that two sets of genomes were in these organisms? Wouldn’t someone else have noticed this?

    Anyway, Williamson’s 2009 paper was followed by a full smackdown…

    Hart, M. W. and Grosberg, R. K. 2009. Caterpillars did not evolve from onychophorans by hybridogenesis. PNAS. 106(47):19906-19909.

  18. #18 Thomas R. Holtz, Jr.
    May 18, 2011

    Good stuff.

    And to be fair, if I didn’t have to teach Galapagos natural history I wouldn’t have known about the current situation with Geochelone.

    Of course, my home institution has a mascot in a diamondback terrapin named… Testudo. Hmmm…

  19. #19 Tor G. Bertin
    May 18, 2011

    Apparently, the giraffe weevil uses its long neck for multiple functions as well, including intraspecific combat.

    http://en.wikipedia.org/wiki/Giraffe_weevil

  20. #20 Jura
    May 18, 2011

    [from Darren: sorry, delayed by spam filter]

    I was very happy to see the use of the tortoises as extant analogues. I, too, have felt that these guys have been an oft overlooked example of extreme neck evolution. All the more so in light of photos like these:

    http://c.photoshelter.com/img-get/I0000xTvu2ORc7bs/s/650/650/Giant-Tortoise-Doing-Yoga-20070611.jpg

    http://cdn1.arkive.org/media/56/56D4B7B9-7E7C-4068-B2F9-18D29CFC86F5/Presentation.Large/Aldabra-giant-tortoise-grazing-on-tree.jpg
    http://www.photomazza.com/IMG/jpg_La_Dipsochelys_elephantina_e_la_piu_grande_testuggine_terrestre_c_Giuseppe_Mazza.jpg

    Maybe this will create some interest into figuring out how these guys are able to raise their heads so far above their (presumably) three chambered hearts.

  21. #21 heteromeles
    May 18, 2011

    To be somewhat far to Dr. Margulis, she’s had to put up with a lot. She had to deal with a couple of decades of “that’s a stupid idea,” and then “we know that already, shut up,” without getting much credit for demonstrating a pretty fundamental characteristic of cell biology and evolution.

    This isn’t a defense of hybridogenesis, but I find it fascinating that what used to be called “good science” is now called a “smackdown.” After all “not even wrong” (see Pauli) is considered by some scientists to be the ultimate condescension. If something isn’t falsifiable, is it even science? Caterpillars from onychophorans is a weird hypothesis, but it was a testable prediction, it was proven false, it generated two papers, and the disproof is trackable. What was wrong here again?

  22. #22 David Marjanović
    May 18, 2011

    Some of the shoulder blades in the figure from your paper are parallel to the vertebral column, others are very close. They’re also all very high on the ribcage, almost lateral to the vertebral column. In short, they all look like pygostylians. Is that deliberate, or did you just copy the reconstructions from somewhere?

  23. #23 Darren Naish
    May 18, 2011

    David – I would think it pretty obvious that we nabbed and adapted our sauropod pics from other sources, yes, and that this explains the variation in scapula orientation. As you may know, there has been a long history of people putting the scapulae in the (probably) wrong place. A sub-vertical orientation is favoured by most of the people I speak to – but the reconstructions of Apatosaurus (from Lovelace et al.) and Camarasaurus (from Osborn & Mook) shown above aren’t looking too bad.

  24. #24 Jerzy
    May 18, 2011

    Sexual selection doesn’t necessary mean female choice. It can also mean sperm competition or male-male competition, and the latter is the case in most ungulates.

    Also: sexual selection doesn’t manifest outside mating period, so proposing sexual selection for the trait which has also practical functions is often unscietific hypothesis. One can propose that factor driving sharpness of teeth of Tyrannosaurus was primary females preference of big-toothed males. Or that pterosaurs evolved flight not for feeding, but because females preferred males which displayed in mating flight. Scientific?

  25. #25 Allen Hazen
    May 18, 2011

    Amazing! My first thought, when I saw the title “Caterpillars evolved from onychophorans by hybridogenesis” was “Does PNAS have April Fool’s articles?” (Proposed experiment: present the Williams paper and Darren’s post about the Amphisbaenian ancestry of mammals to a sample of readers and see how many can tell which one was meant as a joke!)

    I’ve seen — just seen, leafing through books at bookstores and the like, not read at all carefully — proposals that hybridogenesis or lateral gene transfer is responsible for the similar larval forms found in a range of marine invertebrate phyla. Is this idea just Williamson and a few friends, or is it widespread? And do invert zoo-ists in general think it is a live hypothesis or crank stuff?

  26. #26 Lucy
    May 19, 2011

    Would it be particularly difficult, in the face of strong evolutionary pressure, to form a couple of basic “accessory hearts” out of a carotid artery? All you’d need would be a few valves (don’t giraffes have valved carotids?) plus some rhythmically pulsating striated muscle in the walls. I suppose the hard bit would be synchronising them with the actual thoracic heart, but how about large fast myelinated axons running back and forth between them? (Could have evolved from some highly specialised bit of the sympathetic nervous system…) Or maybe something with pressure transduction?

    Is that a sensible hypothesis?

    (Be hellishly difficult to test – you’d need a pretty good lagerstatte to find fossilised carotids!)

  27. #27 Jura
    May 19, 2011

    Not to encourage these comments to continue to diverge from the actual post, but the PNAS hybridogenesis paper is mostly interesting for the failure of peer review at PNAS. The only reason it was published in that journal was because the author was friends with a member of the National Academy of Science, so it was possible to simply “recommend” the paper for publishing. It caused a bit of controversy and pointed out the weakness of that particular journal when it came to rigour.

  28. #28 Christopher Taylor
    May 19, 2011

    I’ve seen — just seen, leafing through books at bookstores and the like, not read at all carefully — proposals that hybridogenesis or lateral gene transfer is responsible for the similar larval forms found in a range of marine invertebrate phyla. Is this idea just Williamson and a few friends, or is it widespread?

    For “just Williamson and a few friends”, read “just Williamson”. Williamson was going on about the hybridogenesis idea long before the PNAS paper. In fact, he’s even managed to get a couple of ‘reviews’ into the pages of (how? why?) the Zoological Journal of the Linnean Society, in 1999 and 2006.

    Most of his claims sit firmly in the realm of the hypothetical (where ‘hypothetical’ means ‘pulled out of one’s arse’), though he did claim to have produced larvae from a successful hybridisation of a sea urchin and a sea squirt. The larvae looked like normal sea urchin larvae, but failed to reach maturity. Most other researchers think that if you received eggs from a sea urchin, and they develop into something that looks like a sea urchin, then what you probably have is a sea urchin.

  29. #29 heteromeles
    May 19, 2011

    Hybridogenesis works. For bacteria and plants, that is. The bacterial case is pretty obvious. In plants, a number of groups are prone to allopolyploidy. The wheat tribe is a great example, and bread wheat is a hexaploid with two Triticum species genomes and one Aegilops genome (and probably a massive amount of gene silencing). I love showing this one to rigid cladists, just because there’s something about promiscuous reticulations in a cladogram that seems to annoy them.

    That said, tunicate/sea urchin hybrid? Duuuuude.

  30. #30 heteromeles
    May 19, 2011

    @26: the problem with supplementary pressurization is that it’s got to work when the head is up AND when the head is down. It has to keep the sauropod from blacking out at the top and getting an aneurysm when drops its head to drink.

    To be fair, I don’t have a good answer for the problem. I’d suggest it is also compounded (or possibly fixed?) by the extensive pneumatic cavities in sauropod bones. After all, if these cavities are vascularized, how do you keep the capillaries from bursting under the pressure changes caused by that giant neck going up or down?

    I sometimes wonder if air sacs were used for arterial pressure regulation. I don’t know if it would work, but air is compressible and blood isn’t, so it seems possible. The air sacs would have to be compressed as the neck lowered and inflated as the head went up, sort of like one of those g-suits fighter pilots wear. Hmmmmm.

  31. #31 Warren B.
    May 19, 2011

    Heteromeles:

    “Call this one the thinking with your pelvic neurons, or some such.”

    I heard Simon Mayo on Radio 2 the other day, asking his co-presenters if they knew how Stegosaurus could cope with a small brain. I immediately thought “Please don’t be the pelvic brain thing. Please don’t be the pelvic brain thing.” Three guesses what it turned out to be.
    Does Radio 2 have a web forum where people can go harrumph a bit?

    Also: I knew of Nick Bibby back when he sculpted fantasy wargame figures. Only a few of the hobby’s creature models of the past couple of decades can match his more naturalistically-designed efforts from the ’80’s (the early days of fantasy miniatures). Even in that nerdy niche of the nonexistant, Akyut Kence’s quote is relevant.

  32. #32 heteromeles
    May 19, 2011

    @31: Is there something about their hosts that makes people think about pelvic brains?

  33. #33 Matt Wedel
    May 19, 2011

    I’d suggest it is also compounded (or possibly fixed?) by the extensive pneumatic cavities in sauropod bones. After all, if these cavities are vascularized, how do you keep the capillaries from bursting under the pressure changes caused by that giant neck going up or down?

    The answer is that diverticula in general, and especially those inside the bones, are very poorly vascularized. We know this from both dissection and from the fact that in birds, gas exchange outside the lungs accounts for only about 5% of the total, and almost all of that 5% occurs in the (immense) abdominal air sacs.

    From an earlier comment:

    This also suggests that sauropod heads explode when the animal drops its head to drink. Or, alternatively, their brains runs low on oxygen while they drink, because the arteries stop pumping blood when the head is down.

    Or they did what giraffes do, and use a rete mirabile. I also recommend reading the section “Blood pressure drop across major arteries to capillaries” in the Wikipedia article on blood pressure; I’d throw in a link but the spam filter often catches those.

  34. #34 heteromeles
    May 20, 2011

    @33: Thanks for the note on the rete mirabile.

    Since I seem to be the designated gadfly on this one, I’d point out that if it was that simple, why don’t giraffes have sauropod-length necks?

    I also think you missed one point: In the statement you quoted above,I was talking about having some sort of supplementary pumping in the aorta. That’s only a solution for when the head is too high. It works against the animal when the head is below the heart. Additionally, I’m not sure how well it scales, and sauropods go through fairly massive changes in scale as they mature. It’s also a fairly energetic solution in animals that generally seemed to be adapted to efficiencies of scale.

    Just to be clear, I’m agnostic on whether sauropods lifted their heads high or not. If they did go in for high browsing, I’d bet they had some very clever pressure-compensation structures built all through their bodies, and these structures were energetically efficient.

  35. #35 David Marjanović
    May 20, 2011

    In plants, a number of groups are prone to allopolyploidy. The wheat tribe is a great example, and bread wheat is a hexaploid with two Triticum species genomes and one Aegilops genome (and probably a massive amount of gene silencing).

    Triticum and Aegilops are close relatives. As you say:

    That said, tunicate/sea urchin hybrid? Duuuuude.

    * * *

    I love showing this one to rigid cladists, just because there’s something about promiscuous reticulations in a cladogram that seems to annoy them.

    …what? What should be annoying about overlapping clades?

    I’d throw in a link but the spam filter often catches those

    ScienceBlogs allows up to four links (not counting SB-internal ones which lack the “http://scienceblogs.com” part but not the following slash). Comments with five or more links get sent to moderation.

    Since I seem to be the designated gadfly on this one, I’d point out that if it was that simple, why don’t giraffes have sauropod-length necks?

    Because they have a dead-space problem in the trachea.

    They have solved this problem by having a narrower trachea than would be expected for a mammal their size. The limitation of this approach is obvious.

    In a bird-style respiration system, this problem simply does not occur, because the volume of the air sacs is much larger than that of trachea and lungs together.

  36. #36 Michael P. Taylor
    May 20, 2011

    Hereromeles asked: “Since I seem to be the designated gadfly on this one, I’d point out that if it was that simple, why don’t giraffes have sauropod-length necks?”

    You’ll be wanting to look at the slides of my talk from last year’s SVPCA, entitled Why giraffes have such short necks. Abstract at http://www.miketaylor.org.uk/dino/pubs/svpca2010/abstract.html, PowerPoint linked from there.

    The short answer is: 1, limited cervical count; 2, big heavy head; 3, tiny torso; 4, primitive respiratory system; 5, lumpen vertebral architecture. Giraffes are rubbish.

    (This talk should be submitted as a paper within a month or so, so hopefully out some time in 2011 … but you never know.)

  37. #37 Michael P. Taylor
    May 20, 2011

    Darn, ScienceBlogs included that trailing comma in the URL to my talk’s abstract, rendering it invalid. Here is that URL again, without the comma this time. Enjoy.
    http://www.miketaylor.org.uk/dino/pubs/svpca2010/abstract.html

  38. #38 Dave Hone
    May 20, 2011

    “Since I seem to be the designated gadfly on this one, I’d point out that if it was that simple, why don’t giraffes have sauropod-length necks?”

    Mike I think the answer you gave errs more towards why in their current mould they couldn’t necessarily evolve longer necks. Far more pertinently, they don’t have them because they presumably don’t need them. While they can’t reach the tallest trees, they can reach much more than any of their competitors, so that’s probably enough for now.

    True, their form might limit them a bit and a much longer neck might impose more constraints than it provides benefits, but I suspect they could evolve a longer neck. Certainly the record sizes for giraffe are way above the norm, so they can at least be significantly bigger than they are now without too many issues.

  39. #39 heteromeles
    May 20, 2011

    Thanks for the link, Mike. Personally, I don’t think giraffes are rubbish, but I get your point.

    Hopefully I’m not exposing any unpublished hypotheses, but I’m increasingly wondering about cervical air sacs as the internal equivalent of a human G-suit and partial pressure breathing by pilots to reduce gravity-induced loss of consciousness (G-LOC. http://aeromedical.org/Articles/g-loc.html). The sauropod would use inhalation and muscle tension as a blood pressure regulator as it raised its head.

    The nice thing is that this trick would involve using something that sauropods really developed (a huge respiratory system with lots of subsidiary sacs) to ameliorate blood pressure issues. The test in the bones would be whether some of the odd bony bits (bifid cervical ribs, etc) would function to as part of a flexible pressure vessel, assisting the air sacs in maintaining pressure in the aorta.

  40. #40 jdmimic
    May 20, 2011

    I want to thank you for mentioning Siegwarth’s paper. They were classmates of mine when we all took a class on dinosaurs. That paper grew out of discussions we had about dinosaur physiology. If anyone wants a copy of it and has a hard time finding it, feel free to contact me and I can send a pdf.

  41. #41 Jerzy
    May 20, 2011

    “Since I seem to be the designated gadfly on this one, I’d point out that if it was that simple, why don’t giraffes have sauropod-length necks?”

    Possibly because they lack sauropod air sac system. Longer neck increases dead volume of windpipe during breathing. BTW, anybody checked giraffe’s lung capacity and dead volume, with all these publicized giraffe dissections and all?

  42. #42 Darren Naish
    May 21, 2011

    Giraffe lung volume is actually rather controversial. This is from Henderson & Naish (2010)…

    There exists some controversy about the exact lung volume in the giraffe, with estimates ranging from as low as 10 l (Patterson et al., 1957) to as high as 47 l (Robin et al., 1960).

    We initially used a lung volume relationship established for horses, but this resulted in a suspiciously large lung volume of over 140 l so seems not to work for giraffes (unsurprising, perhaps, in view of their peculiar shape). Harrison (1980) suggested that giraffe lung volume was about eight times that of a human: this suggests a giraffe lung volume of 48 l.

    Refs – –

    Harrison, D. F. N. 1980. Biomechanics of the giraffe larynx and trachea. Acta Otolaryngologica 89, 258–264.

    Henderson, D. M. & Naish, D. 2010. Predicting the buoyancy, equilibrium and potential swimming ability of giraffes by computational analysis. Journal of Theoretical Biology 265, 151-159.

    Patterson, J. L., Warren, J. V., Doyle, J. T., Gauer, O. H., Keen, E. N. & Goetz, R. H. 1957. Circulation and respiration in the giraffe. The Journal of Clinical Investigation 36, 919.

    Robin, E. D., Corson, J. M., Dammin, G. J. 1960. The respiratory dead space of the giraffe. Nature 186, 24–26.

  43. #43 Andreas Johansson
    May 22, 2011

    Giraffes are pretty small by sauropodal standards. Impressionistically, I’d say they’ve actually got bigger necks than most sauropods in relative terms – anyone got numbers at hand to confirm/refute this impression?

  44. #44 Michael P. Taylor
    May 24, 2011

    Dave Hone, who really should know better, wrote:

    “Mike I think the answer you gave errs more towards why in their current mould [giraffes] couldn’t necessarily evolve longer necks. Far more pertinently, they don’t have them because they presumably don’t need them. While they can’t reach the tallest trees, they can reach much more than any of their competitors, so that’s probably enough for now.”

    Dave, let me quote from a little paper I like to call Taylor, Hone, Wedel and Naish 2011 (page 5):

    Senter implicitly assumed that increases in neck length due to survival benefits were driven only by interspecific competition; but one of the tenets of natural selection is that an organism competes most intensely with the organisms to which it is most similar, that is, the other members of its own population (Darwin, 1859). So even members of a single sauropod species with no close competing taxa — for example, Sauroposeidon proteles in the fauna of the Antlers Formation (Wedel et al., 2000) — would still benefit from neck elongation due to intraspecific competition.

    Needless to say, the same is also true of giraffes.

  45. #45 Dave Hone
    May 27, 2011

    As but Mike, while they might compete most strongly with their conspecifics, it doesn’t necessarily follow that their necks are the limiting factor in their competition with others. Males (which being taller and having longer necks are presumably the key issue about giraffe total height / neck length) are much rare than females. So in a given population, males will be under less competition for high browse with other males. So as long as they are tall enough to out reach the females, they may not need to compete with each other (and their low numbers will enhance that). So in fact they may not require longer necks than they have rather than not being able to evolve them.

  46. #46 Dave Hone
    May 27, 2011

    And I should of course add (doh!) that this hypothesis of mine works because there is dimoprhism in giraffes and population / behavioural differences for males vs females, none of which appears to be true or can be inferred for sauropods. males and females with equal length necks would very much be in competition.

  47. #47 heteromeles
    May 27, 2011

    Not to poke on you evolutionary types, but there is a thing called environmental constraints.

    Since we don’t have sauropod-scale giraffes grazing down the Ituri rainforest (or even grazing on the tops of the tallest Serengeti acacias), I think we can safely say that there are some pretty strong constraints on maximum giraffe neck length, whatever it is they’re competing with.

    It’s also pretty clear that the sauropods had a different set of constraints than giraffes do, because the buggers were so much bigger, if nothing else. It could be lung anatomy, it could be giraffe brains are more energy intensive, it could be that giraffes have ants and other insect herbivores to contend with, and there’s simply less vegetation for them to eat.

  48. #48 Dave Hone
    May 28, 2011

    Well you asked the question why don’t they have longer necks and we provided possible explanations. Obviously there are others.

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