Bio 205 Lecture 11: A New Head?

A New Head

In 1983, Carl Gans and Glenn Northcutt rocked the comparative vertebrate anatomy world by proposing that the origin of vertebrates was associated with the addition of a "new" head anterior to the old pre-vertebrate head. The old head can be visualized using amphioxus as a model. How is the head of amphioxus organized?

1. notochord extends to anterior border
2. segmented body wall muscles (myomeres) derived from somites extend to anterior boder
3. anterior end of neural tube is a small swelling called the cerebral vesicle
4. no paired sensory organs in the head
5. pharyngeal slits with only a collagenous skeleton and no pharyngeal muscles
6. No bone or cartilage

And what about the head of the vertebrate?

1. notochord extends only to about the developing ears, that is there is a pre-otic and a post-otic head
2. somites are entirely post-otic. Paraxial mesoderm anterior to notochord (head mesoderm) appears unsegmented
3. anterior end of neural tube develops into the tripartite brain (fore, mid, hind). The fore and mid brain especially are organized very differently than the neural tube posterior to them.
4. paired sensory organs that develop from ectodermal, neurogeneic placodes
5. a pharyngeal skeleton derived from neural crest and pharyngeal muscles
6. an anterior head skeleton derived drom neural crest

Clearly the head anterior to the notochord in vertebrates is something that is very different from the head in amphioxus and there seem to be three novel features

1. forebrain (or entire brain)
2. neurogenic placodes and derivatives
3. neural crest and derivatives

So Gans and Northcutt proposed that the evolution of the neurogenic placodes and neural crest allowed the development of a new, unsegmented head derived from these tissues anterior to the old head, and this allowed the neural tube to expand anteriorly into a tripartite brain.

These novel features allowed the vertebrates to transfrom from a passive, filter feeding animal into an active predator with paired sensory organs for moving effectively through the environment, an elaborated brain to process and integrate all the sensory information, a skull to protect the new brain, a muscularized pharynx for pumping water that allowed the pharynx to act as a respiratory organ instead of a filter feeding organ, and ultimately, teeth and jaws.

The Old Model - An Elaborated, Old (and Segmented) Head

Gans and Northcutt's New Head model attempted to overturn the old model that the head is segmented like that in amphioxus, and like the trunk, but the elaboration of the head has masked this segmented organization. Curiously, the segmentation theory of the vertebrate skull began with Johann von Goethe, who is certainly best known for his epic play Faust. Goethe essentially argued that the skull is a series of fused, modified vertebrae. This theory was blasted by Thomas Henry Huxley in a very famous Croonian lecture.

Ever since Huxley, however, comparative anatomists have argued that the head is segmentally organized, like the trunk, and like that of amphioxus, and that the modern vertebrate head.

Some evidence for this included a description of

1. the segmented head in amphioxus
2. somites in the developing head of sharks
3. the presence of pre-somites or somitomeres in the head mesoderm of chicks and frogs (the evidence for this is controversial)

One problem is that that the head mesoderm does not appear segmented (except for maybe the somitomeres) but the pharynx is segmented and the hindbrain is segmented and the segmentation of the hindbrain corresponds with the pharyngeal segmentation.

So there are several competing models to the New Head:

1. The head mesoderm is segmented and these segments correspond to the pharyngeal segments but how many segments there are is a problem
2. The head mesoderm is simply a single pre-chordal segment and is not related to the pharyngeal segments

Some recent tests of these models:

Given that:

1. The homeobox gene Otx is expressed only in the fore and midbrain of vertebrates.
2. Hox 1 and Hox 3 are expressed in the hind brain

we would predict that Otx would not be expressed in the amphioxus neural tube and that Hox 1 and Hox 3 would be at the extreme anterior end. Instead, here is the pattern that we see:

That is, the fore and mid-brain are at the level of the first somite, and the hindbrain is at the level of somites 2-6 in amphioxus. This suggests that the tripartite brain is simply an elaboration of the anterior part of the amphioxus neural tube.

Finally, there are a set of genes called hairy1, hairy2, and lunatic fringe that are expressed cyclically and set the clock of anterior to posterior segmentation in the embryo. Remarkably, even though the head mesoderm does not appear segmented, these genes are expressed first in the head mesoderm. Since each round of expression is related to development of 1 pair of somites, we can conclude that there are two head segments, a prechordal segment (fore and mid brain) and a post chordal segment (hind brain).