Chicken, archosaur…same difference


My daughter is learning about evolution in high school right now, and the problem isn’t with the instructor, who is fine, but her peers, who complain that they don’t see the connections. She mentioned specifically yesterday that the teacher had shown a cladogram of the relationships between crocodilians, birds, and mammals, and that a number of students insisted that there was no similarity between a bird and an alligator.

I may have to send this news article to school with her: investigators have found that a mutation in chickens causes them to develop teeth—and the teeth resemble those of the common ancestor of alligators and chickens, an archosaur.

The mutant chickens Harris studied bear a recessive trait dubbed talpid2. This trait is lethal, meaning that such mutants are never born, but some incubate in eggs as long as 18 days. During that time, the same two tissues from which teeth develop in mammals come together in the jaw of the mutant chicken–and this leads to nascent teeth, a structure birds have lacked for at least 70 million years. “They don’t make a molar,” explains development biologist John Fallon, who oversaw Harris’s work. “What they make is this conical, saber-shaped structure that is clearly a tooth. The other animal that has a tooth like that is an alligator.”

Previous efforts to produce teeth in chickens had relied on introducing genetic information from mice, resulting in chickens growing mammalian molars. But a chicken’s underlying ability to grow teeth derives from a common ancestor with alligators–archosaurs–that is more recent than the one linking birds and mammals. Nevertheless, the underlying genetic mechanism that produces teeth in mice, alligators and mutant chickens remains the same.

Schematic of gene expression seen in early development of the
wild-type and ta2 mutant jaw showing coordinated changes in
fgf8, bmp4, and shh expression in outlining the boundary of the
oral/aboral boundary.
The following abbreviations are used: mxp, maxillary; mdp, mandib-
ular; fnp, frontonasal processes; and orl, oral cavity.

The mutant is interesting: it’s not one that was expected to directly affect teeth, but it does illustrate how genes have many downstream effects. What the authors propose is that birds retain a tooth signaling pathway and center, but that the way they’ve turned off tooth expression is by shifting its domain out of the oral mesoderm and into aboral mesoderm, where the overlying ectoderm is not competent to respond. The effect of the talpid2 mutant is to disrupt various crucial genes, shh, fgf8, and bmp4, which will lead to the embryo’s death, but they also have the side effect of shifting other domains of gene expression, sliding that tooth signaling center into contact with oral ectoderm, and as a side effect exposing a hidden developmental program. In the diagram to the right you can see how the colored domains of gene expression (especially bmp4, in blue) are shifted near the maxillary and mandibular processes (mxp and mdp), where the teeth form.

This, I think, is a productive explanation that explains many phenomena.

We hypothesize that the loss of teeth in birds was due to the loss of direct apposition between an epithelial signaling center at the oral/aboral boundary and the underlying mesenchyme of the oral cavity competent to form integumentary appendages. Our model provides a unique developmental mechanism for understanding how specific structures are lost and reinitiated and goes beyond contemporary models of selective gene loss or loss of signaling capability during tooth ontogeny in evolution. Importantly, the control of this inductive event in different facial prominences during development would permit the regional, or modular, loss of teeth as seen in many nonavialan dinosaurs and avialans while allowing them to retain the ability to form teeth on separate regions of the jaw derived from different facial prominences.

It’s telling us something about how birds lost their teeth in evolution. It wasn’t by throwing away the parts of the toolkit responsible for generating teeth, but by changing the patterns of expression of those genes in time and space so that they no longer interact properly. That makes sense; the genes involved, shh, fgf8, and bmp4, are major players in many developmental processes, so their loss would represent a sweeping and destructive change…but delaying one at one point in development so that it doesn’t influence one tissue at one particular time is feasible.

Harris MP, Hasso SM, Ferguson MWJ, Fallon JF (2006) The Development of Archosaurian First-Generation Teeth in a Chicken Mutant. Current Biology 16(4):371-377