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Gegenbaur Revisited: Assessing the “Limbs from Gills” Scenario


Science Daily announces:

Sonic hedgehog gene provides evidence that our limbs may have evolved from sharks’ gills

Latest analysis shows that human limbs share a genetic programme with the gills of cartilaginous fishes such as sharks and skates, providing evidence to support a century-old theory on the origin of limbs that had been widely discounted.

An idea first proposed 138 years ago that limbs evolved from gills, which has been widely discredited due to lack of supporting fossil evidence, may prove correct after all — and the clue is in a gene named for everyone’s favourite blue hedgehog.

Unlike other fishes, cartilaginous fishes such as sharks, skates and rays have a series of skin flaps that protect their gills. These flaps are supported by arches of cartilage, with finger-like appendages called branchial rays attached.

In 1878, influential German anatomist Karl Gegenbaur presented the theory that paired fins and eventually limbs evolved from a structure resembling the gill arch of cartilaginous fishes. However, nothing in the fossil record has ever been discovered to support this.

Now, researchers have reinvestigated Gegenbaur’s ideas using the latest genetic techniques on embryos of the little skate — a fish from the very group that first inspired the controversial theory over a century ago — and found striking similarities between the genetic mechanism used in the development of its gill arches and those in human limbs.

Scientists say it comes down to a critical gene in limb development called ‘Sonic hedgehog’, named for the videogame character by a research team at Harvard Medical School.

The intriguing paper in the journal Development is here, and a very lucid description by one of the authors, J. Andrew Gillis, is here.

Gillis and his co-author Brian K. Hall provide evidence showing that in the development of the gill or branchial arches (a paired series of skeletal elements that support the gills and run down either side of the pharynx in fishes) and of the branchial rays (cartilaginous rods that articulate at their base with the gill arches in sharks and rays and protrude laterally from the gill arches), the common toolbox gene sonic hedgehog (Shh) establishes the anterior-posterior axis and the proliferative expansion of branchial endoskeletal progenitor cells. Those are the cells that give rise to the internal support system in vertebrates, composed of bone (in bony fishes and tetrapods) or cartilage (in sharks and rays).

What is the significance of their report? It is that precisely the same gene establishes the anterior-posterior axis in the tetrapod limb (in the human hand this is the axis from the thumb to the little finger) and promotes proliferation of the endosketal progenitor cells. This, as mentioned, supports a notion first proposed more than a century ago by the great German morphologist Carl Gegenbaur. As Gillis and Hall point out in a recent PNAS paper:

Gegenbaur drew parallels between the organization of the gill arch skeleton with that of the paired appendage skeletons of gnathostomes [jawed fishes], homologizing the appendage girdle with the proximal branchial arch, and the endoskeleton of paired fins proper with the distal branchial rays.

On this theory, the fin and limb girdles of vertebrates would be homologous to and derived from gill or branchial arch skeletal elements. Meanwhile the lateral appendages, the fins and limbs themselves, would be homologous to and derived from branchial rays.

In light of Gillis and Hall’s research, Gegenbaur might turn out to have been right. However, as with so many other evolutionary transitions, one of the major problems in assessing his “arch to fin” scenario is, as Gillis and Hall confess, the absence of any known intermediates between branchial arches and fins. The gap between a branchial ray and a fish fin is certainly considerable (as is obvious in figure 1 in the Gillis and Hall paper). And the existence of developmental homologies throws no light on the question of how the evolutionary transformations might have come about.

Was it, as Darwin envisaged, via a long series of adaptive intermediates, i.e., imposed by external constraints? Or did it occur via a sudden, or series of relatively saltational events, driven by internal causal factors or constraints?

Intriguingly, there is a similar gap between fins and tetrapod limbs. And once more, although no one doubts that fins and limbs are homologous, how the fin-to-limb transition came about is not known. Again as with the considerable gap between branchial rays and fins, there is a considerable morphological gap between fins and limbs while no intermediate fossils are known that might throw light on the transition.

Thus the familiar question arises: Was the fin-to-limb transition gradual or sudden? And was the tetrapod limb imposed by the external pressure of natural selection or by internal causal factors? The same might be asked about the origin of many other novelties in nature even where, as would seem to be the case here, a novelty is clearly homologous to some preexisting structure.

Photo: Skate embryo, by Andrew Gillis via Science Daily.