Pectoral fin muscle in a paddlefish (Polyodon spathula)
Credit: Peter Currie / PLoS Biology
CAMBRIDGE: A stepping stone in the evolution of all four-legged life has been revealed by new research into the pelvic fin muscle development of bony fish.
All tetrapods, or terrestrial four-legged vertebrates, are thought to have descended from an aquatic animal that adapted to terrestrial dwelling. A new study, published in PLoS Biology today, has used living fish to demonstrate changes in muscle development that were crucial to this adaptation.
"[Our study] shows that dramatic changes in the way the muscles of the pelvic fin were made precede the tetrapod transition, and provides mechanistic insights into how this occurred," said lead author Peter Currie of Monash University in Melbourne.
Ancestor of all tetrapods
Four hundred million years ago, the aquatic ancestor of all tetrapods stepped onto land for the first time. Its ability to walk using its pelvic (back) fins was essential for leaving the water, and developed into the rear limb-driven locomotion of today's tetrapods.
Fossil records demonstrate skeletal changes in early tetrapods as this evolution occurred, but since soft tissue rarely fossilises, little is known about how or when the muscles developed.
To investigate, Currie and his team examined pelvic fin muscle development in living fish that are sitting at important evolutionary positions. They compared the developmental mechanisms of pelvic fin muscle in two groups of fish: 'primitive' cartilaginous fish and more derived bony fish, including the Australian Lungfish, which are thought to share an ancestor with the tetrapods.
"The extant lungfish species are the closest living relatives to tetrapods," said Currie, "although debate rages as to how closely it resembles the common ancestor."
Mixture of mechanisms
Currie and his colleagues found that pelvic fin muscles in the cartilaginous fish developed by extension of the body wall muscle, a primitive mechanism also found in their pectoral (front) fins.
In the bony fish, a similar extension towards the fin was seen initially, but it did not progress as far. Instead, cells migrated from the extension into the fin, where they developed into muscle independently. The team were able to demonstrate this cell migration in zebra fish by transplanting body wall sections, or somites.
"Essentially [we] take a somite from a donor marker with a red fluorescent protein and transplant [it] into a host that is carrying a green fluorescent protein," said Currie, "All muscle tissue derived from the donor somite will be red."
The cell migration seen is similar to that in tetrapod limb formation, where stem cells migrate earlier to the limbs and develop into muscle. The bony fish hence show a mixture of the primitive extension mechanism seen in cartilaginous fish, and cell migratory mechanisms seen in tetrapods.
An evolutionary intermediate
The group believe that this mixed mechanism is an evolutionary intermediate and say that further evolution of this mechanism allowed the first tetrapod to make its way onto land and branch off from its common ancestor with bony fish.
"Our study produces a unifying hypothesis as to how the mechanisms that make fin and limb muscle evolved in the vertebrate lineage," said Currie.
Brian Hall, an evolutionary developmental biologist at Dalhousie University in Canada, commented that these findings will be important in further understanding the fish to tetrapod transition.
"This study places developmental and gene expression data in a functional context to provide a testable scenario for the transformation of pelvic fins to hind limbs," he said. "It will be important to place these findings into a phylogenetic framework to determine whether the pattern of development ... arose in derived bony fishes or is more basal, representing the conditions in the tetrapod ancestors."
