Ontogenetic allometry in the fang in the front-fanged Causus rhombeatus (Viperidae) displaces the fang along the upper jaw. Scale bars, 1 mm. We note the change in relative size of the upper jaw subregions: i, anterior; ii, fang; iii, posterior. d.a.o., days after oviposition.
I keep saying this to everyone: if you want to understand the origin of novel morphological features in multicellular organisms, you have to look at their development. "Everything is the way it is because of how it got that way," as D'Arcy Thompson said, so comprehending the ontogeny of form is absolutely critical to understanding what processes were sculpted by evolution. Now here's a lovely piece of work that uses snake embryology to come to some interesting conclusions about how venomous fangs evolved.
Basal snakes, animals like boas, lack venom and specialized fangs altogether; they have relatively simple rows of small sharp teeth. Elapid snakes, like cobras and mambas and coral snakes, are at the other extreme, with prominent fangs at the front of their jaws that act like injection needles to deliver poisons. Then there are the Viperidae, rattlesnakes and pit vipers and copperheads, that also have front fangs, but phylogenetically belong to a distinct lineage from the elapids. And finally there are other snakes like the grass snake that have enlarged fangs at the back of their jaws. It's a bit confusing: did all of these lineages independently evolve fangs and venom glands, or are there common underpinnings to all of these arrangements?
Let's start by looking at the phylogenetic tree and different fang arrangements. As you can see, those snakes with fangs at the back of their jaws (Natrix natrix, second from top) are interposed between one group of snakes with front fangs (the elapids, top), and another group with fangs in front (the vipers, third from top). We can imagine all kinds of scenarios that would produce that condition — front fangs are primitive, and Natrix secondarily lost them, or the fangs of all three are of independent origin and this is an example of convergence — but to resolve the question we need to look at some evidence. We need to examine embryos.
(Click for larger image)
a, Phylogeny. b, c, Adult skulls: lateral views (b); palate, schematic ventral views (c; maxilla coloured, fangs circled). Asterisks indicate species studied by electron microscopy. The evolutionary changes leading from an unmodified maxillary dentition to the different fang types in advanced snakes are indicated at the nodes: (1) continuous maxillary dental lamina, no specialized subregions—ancestral condition for advanced snakes; (2) evolution of posterior maxillary dental lamina—developmental uncoupling of posterior from anterior teeth; (3) starting differentiation of the posterior teeth with the venom gland; (4) loss of anterior dental lamina and development of front fangs.
This is where we begin to see some underlying unity. Vonk and others used sonic hedgehog staining to visualize the dental primordia in snake embryos (O Sonic Hedgehog, is there no process in which you are not involved, nothing in which your expression is not enlightening?) and mapped out the pattern of tooth generation. They identify an odontogenic band, a thin strip of tissue that gives rise to teeth, and note an interesting peculiarity: there are subdivisions into independent anterior and posterior dental lamina, and ablating the anterior lamina does not perturb the development of the posterior lamina. In essence, the snakes simply have a couple of separate tooth-generating zones in their embryonic jaws.
The cool observation is that even in front-fanged snakes, it is the posterior zone that generates the fangs. It is also this same primordium that buds off a tube and a sac that will make the post-orbital venom gland — even in the front-fanged snakes, they have a gland located way back behind the eye to produce venom.
These observations are diagramed below. The unspecialized dental lamina, the part that sprouts the generic small pointy teeth, is in green; the specialized posterior dental lamina, which makes fangs and the venom gland, is in orange. In all the venomous snakes, the venom gland is a tube that first extends forward, and then curls back to make the bulk of the gland even more posteriorly. The important point is that all of these snakes use the same small posterior scrap of embryonic odontogenic tissue to make fangs and glands — we can make a pretty solid argument that these structures are all homologous.
(Click for larger image)
Derived from serial sections. Left-hand side of the upper jaw is depicted, and only epithelial components are shown. Purple, shh expression; grey, tooth buds; green, unspecialized maxillary dental lamina; orange, specialized maxillary dental lamina that bears fangs. The specialized dental lamina is dilated into a bifurcated epithelial sac, the lateral part giving rise to the venom duct and venom gland by growing rostrad, then turning caudad to reach the post-orbital region. In Elaphe obsoleta (a–c) and Natrix natrix (data not shown), fangs develop rostrally and caudally alongside the base of the venom duct; in Naja siamensis (d–f) and Trimeresurus hageni (g–i) the rostral part regresses, remaining visible only as the dental ridge, whereas in b and c this part bears fangs and fuses with the anterior dental lamina. The unspecialized dental lamina in E. obsoleta (a–c) and the outgroup Liasis mackloti (j–l) starts developing anterior and grows caudad.
Now hang on, you may be thinking, if all the fangs develop at the back of the jaw, how do they end up out front in the front-fanged snakes? We can find the answer in development, too. Remember that the two tooth generating zones, front and back, are independent, and the front one can be repressed without disturbing the development of the posterior zone. In the front-fanged snakes, the anterior part of the upper jaw lacks sonic hedgehog expression, and the posterior teeth move forward naturally as part of the allometric expansion of the jaw in embryonic growth. This is sweet: not only does development reveal a homology, it also exposes the process that led to a morphological difference.
Here is the authors' summary:
Our results suggest a new model for the evolution of snake fangs. A posterior subregion of the ancestral tooth-forming epithelium became developmentally uncoupled from the remaining dentition, resulting in posterior and anterior dental laminae that are developmentally independent. This condition is retained in the non-front-fanged snakes, such as the grass and rat snake. This model would imply that the front-fanged elapids and viperids have independently lost the anterior dental lamina, which is supported by the lack of shh expression anterior in their upper jaws.
…
The developmental uncoupling of the posterior from the anterior tooth region could have allowed the posterior teeth to evolve independently and in close association with the venom gland. Subsequently, the posterior teeth and venom gland could have become modified and formed the fang-gland complex—an event that underlies the massive radiation of advanced snakes during the Cenozoic era.
The key innovation in snake evolution was a subtle one, an uncoupling of two tooth-generating regions that opened the door to more flexibility in the modification of the jaws. The fang/venom gland complex probably evolved once in the common ancestor of these groups, but the elapids and vipers independently stumbled on a secondary change, the suppression of the anterior region, that allowed the posterior fangs to move forward to make a more effective poison delivery system.
Vonk FJ, Admiraal JF, Jackson K, Reshef R, de Bakker MAG, Vanderschoot K, van den Berge I, van Atten M, Burgerhout E, Beck A, Mirtschin PJ, Kochva E, Witte F, Fry BG, Woods AE, Richardson MK (2008) volutionary origin and development of snake fangs. Nature 454:630-633.
26 Comments
David vun Kannon, FCD · 31 July 2008
And the ID explanation is...
MememicBottleneck · 31 July 2008
I love reading your posts Prof. Myers. They are consistantly understandable to us non biologists, and enlightening as well. Subjects like the evolution of snake fangs and blind fish are things I never really thought of before, but now find very interesting. Keep them coming.
JLT · 31 July 2008
David Stanton · 31 July 2008
Thanks PZ. Another fascinating and insightful post.
This is a great example of the way to study biology. First you find some feature that needs to be explained. Then you develop a reliable phylogeny for the group in which it evolved. Then you find the developmental and genetic mechanisms that underlie the feature. Then you plot the evolution of the feature onto the phylogeny. This demonstrates the central importance of phylogenetics in all biological research.
Just one small nitpick. I really don't like the term "advanced" when referring to snakes with fangs. The term "derived" is much more appropriate, phylogenetically speaking. Just imagine the embaressment 10 million years form now when some students laugh at the idea of fanged snakes being "advanced". Seriously, it is important to keep in mind that the current state of evolution is not the end point.
Damian · 31 July 2008
Dr. Bryan Grieg Fry, one of the authors of the paper, has been commenting on Pharyngula all day, if anyone wants to ask a question. If not, just read some of the answers that he has given — absolutely fascinating!
He is apparently on a tropical beach in Colombia, at the moment, taking time out from catching snakes. As he put it, "Its a dirty job but someone's gotta do it! :D"
Dr. Bryan Grieg Fry · 31 July 2008
>Just one small nitpick. I really don’t like the term “advanced” when referring to snakes with fangs.
The advanced part refers to the entire major clade, rear and front, not just the ones with front-fangs. I agree with your sentiments though. Boas and pythons, for example, were once thought of but certainly are not primative snakes in any sense. They are actually extremely derived in their own manner, with powerful constriction having been perfected independently in both lineages and even some very special clades convergently evolving heat seeking pits. 'Pit-pythons' and 'pit-boas' as I like to call them, for example in the Python and Corallus genera respectively.
Cheers
B
Wheels · 31 July 2008
Nentuaby · 31 July 2008
I love how the one gene any interested layman can name off the tip of his tongue is named after a little blue video game sprite.
(Cool science, too.)
Mike Elzinga · 31 July 2008
This is the kind of stuff that makes research so exciting. It is now possible to study the emergent characteristics of complex organisms and systems and track their most probable origins and trajectories.
I can’t help but note that this is such an important continuation of the kinds of activities physicists and chemists have been doing in studying the emergent properties of condensed matter. Properties like superconductivity, hardness, stickiness, corrosion resistance, and just about any properties of interest are being elaborated, designed, and manipulated, and this has been going on scientifically for well over a hundred years.
Yet, for many decades the emergent characteristics of the most complex systems we know (namely, living organisms) seemed far beyond our reach to study and elaborate in detail. Now we are seeing how it is done.
Take it from a physicist; biologists rock!
woodsong · 31 July 2008
David Stanton · 31 July 2008
Bryan,
Thanks so much for responding. I certainly did not mean to be critical of your work in any way. I think it is a wonderful piece of research that shows the real power of evolutionary developmental studies.
The "advanced" and "primitive" thing is just a pet peeve of mine. I much prefer "basal" and "derived" as descriptors for placement in phylogenetic trees.
Keep up the good work and thanks for stopping in at PT. I will be going over to Pharyngula to read more about this work. Thanks to Damian for the tip.
Dean Wentworth · 31 July 2008
Given that the phylogeny presented is accurate, if elapids and vipers independently developed suppression of the anterior tooth-generating region, doesn't it follow that they did so via different genetic mutations? (Analogous to primates and guinea pigs having Vitamin C synthesis genes that are "broken" in different ways.)
Henry J · 31 July 2008
Mike Elzinga · 31 July 2008
wolfwalker · 1 August 2008
An excellent post, Dr. Myers. This sort of thing is what keeps me interested in evolutionary theory.
Woodsong, your post about types of venom reminds me of some research I read about somewhere recently, say a year or so ago: snake venom is evolving before our eyes. Rattlesnake populations which were once observed to produce almost exclusively hemotoxic venom are now producing dangerous neurotoxic effects as well.
hoary puccoon · 1 August 2008
On a really basic level, way below the biologists here, the evolution of snake fangs is an interesting example of a "must have been designed, couldn't have evolved in gradual stages" feature that creationists love so much. After all, what use could a fang with a hole that only goes half way down the tooth? Surely it would be more prone to abcess, and blah, blah, blah....
But snake fangs which evolved because a groove in the tooth got deeper and deeper over generations until the edges wrapped around and closed in on themselves offered an improvement every step of the way, starting, presumably, with a round tooth with a mutation that left it just slightly flattened on one side.
This is a really clear cut example for me of why the theory of evolution is one of the most powerful tools in science, while creationism, including ID, is a science-stopper.
David Stanton · 1 August 2008
Hoary,
Good point. Or, as a wise man once said:
"Reality is not constrained by your lack of imagination."
And I was right!
woodsong · 1 August 2008
Dr. Bryan Grieg Fry · 1 August 2008
>Rattlesnake populations which were once observed to produce almost exclusively hemotoxic venom are now producing dangerous neurotoxic effects as well
This is quite debateable. A better explanation is that people are getting bitten by snakes from populations that the spreading human habitation centers are now encroaching upon and that neurotoxic components in rattlesnake venoms are more prevalant that previously appreciated.
Cheers
Bryan
woodsong · 1 August 2008
stan · 10 August 2008
PZ: "I keep saying this to everyone: if you want to understand the origin of novel morphological features in multicellular organisms, you have to look at their development."
oops....and all these years I was told to look at random mutations. So PZ, does this mean that you are admitting that the origin of novel morphological features has nothing to do with ToE?...I mean this is a theory of random mutation and natural selection, yet you're telling me to look at the development of individuals. What gives?....do only populations evolve, or are you saying individuals evolve as well?....confused.
Stanton · 10 August 2008
Henry J · 10 August 2008
Stan,
The mutation affects the individual's development in some way - that's what makes it subject to selection, rather than neutral.
It doesn't conflict with the current theory, it's part of it.
Henry
stan · 10 August 2008
can someone show me an example of a mutation that, say, creates a fang?
stan · 10 August 2008
and I never got an answer: do individuals evolve (during development -- where new morphological features originate -- as PZ says), or do only populations evolve via mutations...?
which is it?
Stanton · 10 August 2008