Often, as I’ve looked at my embryonic zebrafish, I’ve noticed their prominent median fins. You can see them in this image, although it really doesn’t do them justice—they’re thin, membranous folds that make the tail paddle-shaped.
These midline fins are everywhere in fish—lampreys have them, sharks have them, teleosts have them, and we’ve got traces of them in the fossil record. Midline fins are more common and more primitive, yet usually its the paired fins, the pelvic and pectoral fins, that get all the attention, because they are cousins to our paired limbs…and of course, we completely lack any midline fins. A story is beginning to emerge, though, that shows that midline fin development and evolution is a wonderful example of a general principle: modularity and the reuse of hierarchies of genes.
First, I have to explain a little bit about the organization of embryonic mesoderm. Recall that there are three germ layers: ectoderm, which forms skin and nervous tissue; endoderm, which contributes to the gut; and mesoderm, which forms connective tissue and muscle. Mesoderm is also organized from medial to lateral in very specific ways, diagrammed below (taken from this more detailed overview of mesoderm development; I’ll also recommend these animations for those still struggling to sort the bits out.)
In the center is the neural tube, which isn’t mesodermal at all—it’s ectodermal. There is also another important ectodermal derivative, the neural crest, which separates away from the neural tube and is going to migrate into various places in the embryo, and is going to make essential contributions to lots of tissues.
At the midline is a special mesodermal tissue, the axial mesoderm, which forms the notochord. Next that is paraxial or somitic mesoderm, which forms the segmented blocks of muscle running the length of the animal. Next out is a band of intermediate mesoderm, which contributes to the urogenital system. Finally, and lateralmost is the lateral plate mesoderm, which is split into a somatic and splanchnic component. This sheet of tissues is going to fold over to form a tube (those animations will help!), and the splanchnic layer will line the endoderm of the gut, while the somatic is going to form various connective tissues and muscle of the body—in particular, somatic lateral plate mesoderm is going to form the connective tissue of the limbs. The paraxial/somitic mesoderm is going to form the body wall musculature, and also some cells are going to peel off and migrate into the limbs to build limb musculature. Complicated, I know…so here’s a another level of complication: the somites are also broken up into subunits.
This diagram (click on it for a larger image) shows how the paraxial mesoderm has a subdivision into a dermomyotome component in orange that will form the dermis of the skin and various muscles, and a sclerotome component in blue that will form, for instance, the vertebrae. Basically, the message here is that the embryo partitions the mesoderm into zones from the midline to further lateral positions, and these subsets of the mesoderm have specific roles to play.
There is also a regionalization of the mesoderm from anterior to posterior. The Hox genes are important players in this process, specifying positional identity along the long axis. Another class of transcription factors, the Tbx genes, are also crucial in defining boundaries and identities—expression of the Tbx5 gene, for instance, determines that a forelimb will form, while Tbx4 determines the formation of a hindlimb.
One way to think of this is that developmental processes take this sheet of mesodermal tissue and mark it off with a grid: there’s an organization from axial to lateral plate mesoderm, and there’s a demarcation from anterior to posterior defined by Hox and Tbx genes. Then, at specific coordinates in this grid, other genetic cascades are activated to start limb formation. I’ve described them before. An apical ectodermal ridge (AER) forms laterally for each of the fore and hind limbs, a zone of polarizing activity (ZPA) develops along the posterior edge and confers polarity on the limb, and a series of Hox genes define position within the limb. So, at a particular coordinate, a whole cascade of genes are turned on the generate a thickening, and a bump, and lead to a well-organized limb forming.
Now, how does a medial fin form? If you review this article on the formation of the genitals, you’ll have a clue. That article describes a series of genes activated to form the ‘bump’ of the embryonic penis/clitoris, and shows that it is a reactivation of the same genes used in forming the ‘bump’ of the limb. As you might guess, Freitas et al. find the same genes playing a role in making fins along the midline in sharks and lampreys as the ones that set up paired limbs.
This is a typical developmental paper, as I mentioned the other day, that means it is full of in situ stains for expression patterns of RNA. It’s a lot of data—there are matrices of the region of expression for various Hox genes in a series of midline fins, there are markers for sclerotome and neural crest, there are genes, genes, genes turned on all over the place. I’m not going to show any of the data for a change, since it’s either show the whole pattern or show a fragment out of context, which is unhelpful, so instead I’ll just summarize and you’ll have to trust me. Or look it up in Nature yourself.
The story is straightforward. At the midline, an apical ectodermal fold (AEF) forms that leads to the growth of the dorsal and ventral fins. Where the limbs are going to develop out in the lateral plate mesoderm, the median fins are going to draw on the cells of the paraxial mesoderm to form their substance—in particular, cells of the sclerotome are going to migrate dorsally to form the tissue, with some contribution from the dermamyotome. In addition, neural crest cells will migrate into the fin fold. Within the fin itself, anterior-posterior regionalization is defined by the same genes that do likewise in the developing limb, Hoxd9, Hoxd10, Hoxd12, and Hoxd13. A Tbx gene, Tbx18, is also expressed at the anterior border of each midline fin. Here’s a simple diagram of the mesodermal sources for the dorsal fin.
A dorsal fin looks an awful lot like a grossly simplified pectoral fin, which is a simpler version of a tetrapod limb (with differences, of course!) A dorsal fin, though, is an older structure, and those paired lateral fins are later evolutionary innovations. Both sharks and lampreys use homologous genes to develop these midline fins, which implies that we’re looking at a primitive, conserved mechanism. What all this suggests is that Cambrian fishes evolved patterning mechanisms to form a simple midline structure, the dorsal and ventral fins, with a small suite of genes to impose spatial organization on it, and sculpting paraxial mesoderm to build that thin flap. With that module in place, the easy way to build a lateral fin was to simply reactivate that very same cascade of genes in the lateral plate mesoderm, and presto…a flap forms in a novel location. Later elaborations on that basic genetic cascade led to the details of the teleost paired limbs, and other elaborations would have led to the tetrapod limb, but the core of the developmental process involved seems to reside right there, in a simple midline fin.
The authors propose that the next step is to look at the midline fins of cephalochordates, predicting that the same genes will be used there. I expect that they’ll be right. I would predict that we’d also find the same genes used in another novel structure, the re-evolved dorsal fins of whales. The redeployment of previously refined genetic modules is going to turn out to be a universal property of evolved systems, I expect.
Freitas R, Zhang G-J, Cohn MJ (2006) Evidence that mechanisms of fin development evolved in the midline of early vertebrates. Nature advance online publication, (doi:10.1038/nature04984).