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.
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.
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.
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
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)).
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].
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).
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!
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.
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].
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).
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.
And for previous articles on giraffe necks, sauropod necks and the debates surrounding them, please see…
- Dammit, and I sooo loved the ‘necks for sex’ hypothesis
- Junk in the trunk: why sauropod dinosaurs did not possess trunks
- Sauropod dinosaurs held their necks in high, raised postures
- Thunder-Lizards: the Sauropodomorph Dinosaurs (a book review)
- Getting scansoriopterygids, terrestrial-stalking azhdarchids, sauropod pneumaticity and the word palaeontography into a kid’s book
- Neck Wars, flightlessness in azhdarchids and more filling of Romer’s Gap: SVPCA 2010
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., 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.