Oh, Grandma, what big Scales you have!

One of the more interesting challenges in  biology is to explain the genetic basis of important traits in a given species, and how the trait arose. There are always evolutionary origins, we assume, but they can be difficult to work out. A classic example is teeth: we depend on them for eating and survival.  Teeth are hard, repetitive structures, produced by a wave of repeated use of the genetic mechanisms that produce each one.  But our earliest vertebrate ancestors didn't have teeth, or jaws for that matter. What they did have at an early stage in vertebrate evolution, was scales--hard repetitive structures over their bodies.

A long-standing issue is where teeth came from developmentally, and whether teeth are a recruitment of scale-generating genetic mechanisms.  While the issues are a bit technical, one of the leaders in work on this area from a genetic point of view is Dr Kazuhiko Kawasaki, a senior research scientist in our own group here at Penn State.   We asked Kazz if we could post his up-to-date exploration of this issue, and he kindly agreed.  Here it is:

Contributed by Kazuhiko Kawasaki

The Developmental and Evolutionary Origins of the Tooth

Among the most important innovations in the evolution of vertebrates is the tooth, which enabled active feeding. It has long been thought that oral teeth arose from scales on the skin surface, based on the similarities in these two structures in the shark (1). However, an extinct jawless vertebrate, called Loganellia scotica, was found to have scales on the body and tooth-like structures (called denticles) in the oropharyngeal cavity (the back of the mouth). Analysis of these structures led to a new hypothesis: oral teeth originated by co-opting the developmental control used in the oropharyngeal denticles (2). The former theory, that teeth originated from external scales, is called the 'outside-in' hypothesis, whereas the latter, that oral teeth came from oralpharyngeal teeth, the 'inside-out' hypothesis. The tooth and the denticle both develop between two primary tissue layers in the early embryo, epithelium and neural-crest-derived ectomesenchyme; hence a critical difference in these two hypotheses is the tissue origin of the epithelium, either ectoderm (scales) or endoderm (oropharyngeal denticles). In what tissue do these structures originate?

Teeth (left) and scales (right) of the nurse shark.

Until recently, the epithelium involved in oral tooth development was thought to be derived from ectoderm that is located near the border with endoderm. Soukup et al. updated this premise using a transgenic Mexican axolotl that produces green fluorescent proteins (GFP) in the whole body (3). They transplanted GFP producing ectoderm to a normal animal and injected a red dye into endoderm of the transplanted animal at an early developmental stage. The result was that some teeth are labeled in green, others in red, and still others in both green and red, showing that teeth are of ectodermal, endodermal, or a mixed ecto/endodermal origin. Based on this result, the authors suggested "a dominant role for the neural crest mesenchyme over epithelia in tooth initiation and, from an evolutionary point of view, that an essential factor in the evolution of teeth was the odontogenic capacity of neural crest cells, regardless of possible 'outside-in' or 'inside-out' influx of the epithelium".

While the developmental and molecular data demonstrate the essentially identical nature of ectodermal and endodermal teeth, the result does not answer the question about the evolutionary origin. Yet, this study appears to have triggered many subsequent studies, and the outside-in, inside-out, and other modified theories have been proposed as a result (4, 5). A recent analysis showed a gap in the phylogenetic distribution (that is, among different vertebrate lineages) of the internal denticles in Loganellia and oral teeth in jawed vertebrates. Thus, the morphological similarities in these two structures are likely the result of convergence, unrelated evolution of the same trait, refuting the evidence that supports the inside-out hypothesis (6). Further, tooth-like scales were discovered in the cheek and the lip of an Early Devonian jawed vertebrate, suggesting "the existence of a field of gene expression near the mouth margin in which scales could be transformed into teeth" (7). These scales and teeth share a similar structure, and probably used common genetic machinery for mineralization. It is also likely that this transformation was caused by a slight change in the gene regulatory network, responding to a signal from neural crest cells, if the tissue origin does not strictly determine the fate of epithelium.

Here are some references about these issues:

1.         Reif, W.-E., Evolution of dermal skeleton and dentition in vertebrates. Evol Biol, 1982. 15: 287-368.

2.         Smith, M.M. and Coates, M.I., The evolution of vertebrate dentitions: Phylogenetic pattern and developmental models, in Major events in early vertebrate evolution, P.E. Ahlberg, Editor 2001, Taylor & Francis: New York. p. 223-240.

3.         Soukup, V., Epperlein, H.H., Horacek, I., and Cerny, R., Dual epithelial origin of vertebrate oral teeth. Nature, 2008. 455: 795-798.

4.         Fraser, G.J., Cerny, R., Soukup, V., Bronner-Fraser, M., and Streelman, J.T., The odontode explosion: the origin of tooth-like structures in vertebrates. BioEssays, 2010. 32: 808-817.

5.         Huysseune, A., Sire, J.-Y., and Witten, P., A revised  hypothesis on the evolutionary origin of the vertebrate dentition. J App Ichthyol, 2010. 26: 152-155.

6.         Rücklin, M., Giles, S., Janvier, P., and Donoghue, P.C., Teeth before jaws? Comparative analysis of the structure and development of the external and internal scales in the extinct jawless vertebrate Loganellia scotica. Evol Dev, 2011. 13: 523-532.

7.         Blais, S.A., MacKenzie, L.A., and Wilson, M.V., Tooth-like scales in early Devonian Eugnathostomes and the "outside-in' hypothesis for the origin of teeth in vertebrates. J Vert Paleontol, 2011. 31: 1189-1199.