The origin and evolution of developmental novelties
Evolutionary biologists are aware that adaptations are constrained by historical features, especially by phylogenies, so that evolutionary changes are more akin to an erratic tinkering than a general directional trend (Jacob 1977, Gould 1996). From a functional point of view, we easily understand a loss of function, for example the origin of snakes from lizard-like ancestors. We also understand the transformation of an anterior leg into a wing, especially because we recognise the same bones in both organs. It is far more difficult to imagine how a tetrapod vertebrate might evolve into a hexapod. Most scientists will consider such a change as impossible. In other words, once the tetrapod state was acquired in terrestrial vertebrates, it became a strong developmental constraint which did not permit eventual major changes.
The observation of such constraints has led many authors to say that Darwinian theory explained microevolution (that is small adaptive variations) but not macroevolution, defined as the appearance of major novelties, such as limbs or head. This opposition still remains a debate among evolutionists, but it is progressively solved by a better understanding of both phylogenies and comparative developmental genetics.
In the Chordate phylum, it is likely that an ancestral state was like the extant Amphioxus, deprived of limbs. Then limbs appeared presumably as lateral expansions along the body. Why only two pairs and not three have been retained in the derived groups is not understood.
We have more information concerning the origin of the head in Vertebrates. Again, the Amphioxus-like ancestor was presumably deprived of a differentiated head, without eyes or mouth and with only a slight anterior dilatation of the neural tube. In the course of evolution, a major developmental novelty appeared, that is, a special derivative of the nervous tube, the neural crest. Modern developmental investigations have shown that the neural crest plays a major role in the organisation of the nervous system in Vertebrates and especially in the building of the head (Le Douarin and Kalcheim 1999), including the brain and the skull. Without the neural crest, the evolution of Vertebrates toward a bigger size and the acquisition of a complex brain would have been impossible. How the neural crest itself originated during chordates evolution is not known. Future progresses of developmental genetics should shed some light upon this major problem.