One of the greatest fallacies held about evolutionary theory is that fossils are essential in demonstrating the existence of change (don't believe me? Look at 'creation science' books like Duane Gish's Evolution: the Challenge of the Fossil Record and Evolution: the Fossils Say No!). Of course, fossils do indeed show how characters were accrued and modified over time, and it's that 'time' aspect of the data that they shed crucial information on. But we most certainly do not need fossils to demonstrate the fact of evolution, as we are surrounded by evolutionary intermediates right here in the modern world. In fact, if we didn't have any fossils at all we would still conclude - from the living organisms that surround us - that evolution happens...
I was hoping, back in 2006 when writing for Tet Zoo ver 1, to cover the full diversity of the agamid lizards, or agamas. Agamids belong to the group of iguanian lizards called acrodonts, and most of the world's 400-odd agamid species belong to the Australo-Papuan amphibolurine clade, to the southern Asian draconine clade, or to the Afro-Asian agamine clade. For further introductory stuff on agamids please visit the ver 1 post here. In that ver 1 post, I spent some time looking at the toad-heads or toad-headed agamas Phrynocephalus, a mostly Asian, mostly desert-dwelling group of short-headed agamine agamas [P. arabicus shown below].
It's reasonably well known, and well established, that the closest relatives of agamids are the chameleons, and traditionally both groups have been regarded as separate, closely related 'families'. However, some workers have found evidence indicating that agamids are paraphyletic with respect to chameleons (Estes et al. 1988): in other words, that chameleons are actually a specialised agamid sub-group. This is not, however, the currently accepted 'consensus' view. In view of this it's of special interest that some characters generally thought unique to chameleons are seen in agamids, and specifically in toad-heads.
Schwenk & Bell (1988) showed that one of the toad-heads, Phrynocephalus helioscopus, practises an extreme form of tongue protrusion highly similar to that of chameleons [image at top, from Schwenk & Bell (1988), shows feeding P. helioscopus compared to the chameleon Chamaeleo zeylanicus]. P. helioscopus is a small Chinese species restricted to the north-west Xinjiang Uygur Autonomous Region. Individuals were observed and filmed extending their tongues to procure insect prey in what was, surprisingly, an essentially chameleon-like manner: the dorsal, glandular part of the tongue was extended and formed a large 'pad' wrapped around the tongue's muscular stem, and this was then shot forward in a fraction of a second. Sure, no toad-head has a tongue that can be extended for a length equivalent to anything like its own body length (as can the tongues of chameleons), but Schwenk & Bell (1988) argued that the tongue morphology and feeding behaviour of P. helioscopus is homologous with that of chameleons. That's neat, as chameleons have always been thought to have a totally unique tongue.
If what P. helioscopus does is homologous with what chameleons do (and not just convergent with it), then there are two interpretations of this evidence. One is that this sort of tongue protrusion and prey apprehension is primitive for the agamid-chameleon clade: in other words, that tongue protrusion of the P. helioscopus type was present in the common ancestor of both agamids and chameleons. If this is true, then what P. helioscopus does with its tongue should be typical for agamids (unless there are species that have secondarily reverted to the typical form of prey apprehension used by lizards). To test this idea we need more information on the tongue anatomy and feeding behaviour of other agamids.
The second interpretation is that P. helioscopus is particularly closely related to chameleons, and that the form of tongue protrusion it shares with chameleons is a late-evolved novelty restricted to an agama subgroup that includes chameleons. For this to be correct, agamas (and, perhaps, toad-heads) have to be paraphyletic with respect to chameleons. As noted above, the idea that chameleons are a specialised agama sub-group has been proposed on occasion. In their mtDNA-based phylogenetic study of the Chinese toad-heads, Pang et al. (2003) found P. helioscopus to be the most recently evolved member of a small clade that was itself part of the oviparous 'Clade B' toad-head clade. Could chameleons actually be members of the toad-head 'Clade B'? Given the large number of unique morphological characters that differentiate toad-heads from other agamas (Arnold 1999), it is actually highly unlikely that chameleons (which lack these characters) fit in there.
So if chameleons aren't modified toad-heads, the (apparently homologous) form of tongue protrusion shared by some toad-heads and chameleons must, presumably, be more widely distributed within agamids: again, we need more information on the tongue anatomy and feeding behaviour of agamids to test this further. Has anyone studied tongue protrusion in agamids to see how widespread this behaviour is? While writing this article I learnt about Smith's (2005) study of agamid tongue morphology and function (I wrote the article you're reading now in 2006 and, here in 2008, am updating and modifying it). In agreement with the data on P. helioscopus, Smith (2005) showed that the mechanism of tongue protrusion present in chameleons is not unique but should be considered an exaggerated version of the style of tongue protrusion present in agamids [adjacent image shows Mary Blanchard with Parson's chameleon Calumma parsonii].
If current phylogenies positing a sister-group relationship between agamids and chameleons are correct, then the common ancestor of the two groups exhibited an unusual protrusible tongue. What would be really neat now is if we could show how the remarkable arboreal features of chameleons evolved in concert with their increasingly modified tongue apparatus - but for this of course we do need to look at the fossils for our data. Alas, I don't have time now to embark on a discussion of chameleon evolutionary history, but I must do so at some time.
Coming soon: squirrels of the world unite, a good year for phorusrhacids, and the history of tree-climbing dinosaurs!
Refs - -
Arnold, E. N. 1999. Phylogenetic relationships of Toad-headed lizards (Phrynocephalus, Agamidae) based on morphology. Bulletin of British Museum of Natural History (Zoology) 65, 1-13.
Estes, R., de Queiroz, K. & Gauthier, J. 1988. Phylogenetic relationships within Squamata. In Estes, R. & Pregill, G. (eds). The Phylogenetic Relationships of the Lizard Families. Stanford University Press, Palo Alto, pp. 119-281.
Pang, J., Wang, Y., Zhong, Y., Hoelzel, A. R., Papenfuss, T. J., Zeng, X., Ananjeva, N. B. & Zhang, Y.-p. 2003. A phylogeny of Chinese species in the genus Phrynocephalus (Agamidae) inferred from mitochondrial DNA sequences. Molecular Phylogenetics and Evolution 27, 398-409.
Schwenk, K. & Bell, D. A. 1988. A cryptic intermediate in the evolution of chameleon tongue projection. Experientia 44, 697-700.
Smith, K. K. 2005. Form and function of the tongue in agamid lizards with comments on its phylogenetic significance. Journal of Morphology 196, 157-171.
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As always, informative, explanatory and interesting.
Coming soon: squirrels of the world unite, a good year for phorusrhacids, and the history of tree-climbing dinosaurs!
The preview list is back! YAY!!
Nice stuff on lizard tongues. I'm sure you already have an article on tongue protrusion in miniaturized plethodontid salamanders in prep.
Didn't Bakker remark in The Dinosaur Heresies that dino tongues were horribly understudied? Maybe I should get away from these vulgar overstudied air sacs and become Dino Tongue Dude. Although that name has multiple interpretations, not all of them nice. And now I'm just protruding my tongue, metaphorically, and to no good end. So good night. And good work.
BTW <broad grin>, here is a thesis about temnospondyls and their phylogenetic position. It contains a couple of surprises.
Chameleons also lost some of their auditory structures, such as the tympanum. I've wondered if the protrusable tongue, arboreality, head casque and occular changes all evolved in concert such that the tympanum and other auditory structures were 'sacrificed'.
Ooo Phorusrhacids! Im rather interested in them, as you probably gathered when I borrowed the papers off you when I was an undergrad. look forward to that :)
David, two of the PDFs in that link are not accessible outside of LTU.
Yes, but both the one on Eryops and the one on Trimerorhachis have meanwhile been published.
Oops, wrong name selection.
Chameleons fascinate me. Toadheads now too I guess (new to me; so thanks Darren!)
I wonder whether chameleon casques and horns (in the horned species) are homologous with ceratopsian crests and horns, as well as visually reminiscent of them? And if so, can we deduce anything significant about ceratopsians from these structures in chameleons?
Separately- Do the independently mobile eye-turrets of chameleons have orbits that are distinctive in any way, and did any extinct species show similar features?
That leads me on to the more general question of what we can tell about eyes and faces - and tongues - from skulls.
I have noted the work of Lawrence Witmer with great interest...
Draconine agamids are pretty common here in Singapore (native Bronchocela cristatella) and Draco spp. in forests, introduced Calotes versicolor in most non-forest habitats. I'll try and see if I can observe any of them feeding; they're extremely skittish around people.
One quick comment on Draco: pet peeve no. 114 is that the only Draco species ever mentioned in books, popular literature, TV etc. is Draco volans, as if it's the ONLY species. Err, hell-o-o, it's one of about 40 species, yet you'd think that none of these others exist. So I started an article called 'Why Draco volans is boring' in which I planned to at least mention all the others.. as yet I haven't finished it, dammit.
Tree-climbing dinosaurs? Pfft. Show me tree-climbing plesiosaurs.
Graham: Chameleon horns are not at all homologous to ceratopsian horns. The two structures evolved independantly, as the two groups are not at all closely related. However, the horns of Jackon's chameleon (Chamelaeleo jacksonii), as well as the frill, are very reminiscent of Triceratops. The two probably use(d) their horns for similar purposes, that is, intraspecific display and jousting.
As far as I'm aware, the eyes of chameleons are no different than other agamid lizards, except that the eyelid is enormously overgrown over the eye, which is itself very large. The difference, of course, is that chameleons can see in two different directions at once.
I have kept two Jacksons over the years (not at the same time), and I've found them to be docile overall, but grumpy and paranoid. Also, young chameleons are ridiculously hard to keep alive, as I learned (by reading, later) that chameleons are overly-sensitive to infection. I recommend leopard, wonder, or fat-tailed geckos. Much hardier lizards, and hyper-cute, to boot.
Now, here's a question: Are chameleons restricted to Madagascar and Africa, or do they exist in Asia, too?
Zach: Chameleons are known from the Mediterranean and Middle East (Chamaeleo chamaeleon), the Arabian Peninsula (the veiled chameleon Chamaeleo calyptratus is from Yemen), all the way to India and Sri Lanka (Chamaeleo zeylanicus)
Darren: Yes indeed, in fact, Singapore itself has 3 different species of Draco: D. quinquefasctiatus, D. melanopogon, and D. sumatranus. And what I find fascinating is how various species of Draco can coexist within the same area through exploiting different microhabitats.
I went looking for the KK Smith article, and note that 2005 is the online date, actual publication was 1988. Sadly, my e-library access doesn't get me that far back. Can anyone help with a pdf?
And that temnospondyl thesis looks like it'd be quite useful, if youre into lower vertebrates (anamniotes). Probably also for basal amniote relationships, so I can see why David's excited; though when looking at one of those basal-tetrapod cladograms I find I have to squint quite a bit before locating the relatively obscure token amniotes, without which I'm disoriented. (Re. squinting; I did a lot of fossil sorting last year - stuff too big for a microscope and too small for comfort - and my spectacle prescription changed considerably over the same period; now I really need bifocals, dammit!)
The agamids in my backyard (Lophognathus) look like they're effectively using jaw prehension, usually getting over the top of the prey and plunging the open jaws downward with tongue partly protruded; I'd need video to be sure whether there's a tongue-retraction before they first bite down, but I suppose it would be a good idea (those front teeth are sharp).
Funnily enough, the thesis uses the term "lower vertebrates" for everything except birds and mammals...
No, that's not it. Amniote phylogeny with emphasis on turtle origins is one of my supervisor (Michel Laurin)'s pet projects; the other is tetrapod oopsie stegocephalian phylogeny with emphasis on lissamphibian origins. Guess what my first paper is about, what my in-press paper is about, what my in-review paper is about, and what the side project to my thesis is about. Also, Damien Germain's recently defended thesis likewise had a chapter on tetrapod phylogeny and found the same result (lissamphibians as lepospondyls, temnospondyls closer to amniotes + lepospondyls than the anthracosaurs are).
That said, Pawley found out something very interesting about Casineria. I won't spoil the surprise. I'm still laughing :-D
Zach: Thanks. Yeah I realised it could sound a strange question because of the distance between groups but Jackson's chamaeleon looks just so suggestive of Triceratops, (and not all chamaeleons have such horns, just as ceratopsian endowments vary widely), that I couldn't help but wonder if the same (homologous) bones bore the modified structures in each group, and whether there was some simple gene-switching common to various reptile groups - switching bones from 'no horns here' to 'grow horns here', and to varying degrees.
Is Styracosaurus' frill of horns a hypertrophied homologue to Triceratops' epoccipital nubbins? (I've seen them labelled epoccipitals, those little points around the neck-frill margin, but not sure if it's a generally-used term).
I'm wondering now too whether ceratopsians may also have had prehensile tongues (to haul shrubbery into the beak)...?!
Hmmm...good question on Styracosaurus' frill horns. I'd like to say they're giant epoccipitals. I suppose they'd have to be. Ceratopsids like Centrosaurus, Einiosaurus, and Pachyrhinosaurus have singular enlarged, curved (or straight) epoccipitals while the rest of them are normal, so I can only imagine that such is the case in Styracosaurus, only taken to an extreme degree.
I can vouch for tongue protrusion in the feeding habits of one other agamid lizard at least, having owned a bearded dragon for the past couple of years. I don't know if [i]Pogona[/i] tongue morphology/usage is at all homologous to that found in chameleons, but I do know that the tip of Bowser's tongue is sticky, and whatever it adheres to invariably ends up in her mouth.
Also, she has a surprisingly painful bite for a little lizard.