An international team of scientists has uncovered information about the nerve networks required for walking on land, suggesting the last common ancestor of sharks and mammals walked underwater about 400 million years ago (Devonian period). The study appears in the journal Cell.
Little skates (Leucoraja erinacea). Image credit: Monash University.
Past research had revealed that the little skate (Leucoraja erinacea), a cartilaginous fish considered to be one of the most primitive vertebrates, displays alternating, left-right, two-limbed motion with its pelvic fins similar to that used by land animals.
The new study shows that this fish uses paired muscle groups, genetic regulatory proteins, and spinal cord nerve circuits similar to those used by humans to coordinate ‘bipedal locomotion.’
“Our research challenges previous ideas, pushing the estimated time of land-walking back 50 million years,” said study co-author Dr. Catherine Boisvert, from the School of Molecular and Life Sciences at Curtin University and the Australian Regenerative Medicine Institute at Monash University.
For the study, Dr. Boisvert and colleagues studied skate embryos because the circuits that control walking in skates and humans are formed during gestation.
They found that walking in both species is enabled by ‘central pattern generators’ (CPGs).
Embedded in the spinal cord, such neural networks connect to nerve cells, called neurons, targeting limbs to enable rhythmic muscle movements like the flapping of insect wings or the running motion of human legs.
The researchers found that skate and humans employ similar CPGs to control flexor and extensor muscles that cooperate to bend and straighten appendages.
Along with anatomical features and nerve circuitry, experiments showed that skate and mammals both use HOX and FOXP, protein groups that act ‘genetic switches,’ turning genes on or off as they control the formation of networks of neurons that enable motion, called motor neurons.
The circuits involved in limb control were established in the common ancestor to all vertebrates with pair appendages millions of years before the first tetrapod walked on land. Image credit: Jung et al, doi: 10.1016/j.cell.2018.01.013.
“The common ancestor of fish and land animals started using these proteins to control genes related to body pattern and motion. Since then, evolution has adjusted this same set of regulatory tools as fins changed to legs and wings, and even as snakes lost their limbs, reverting to a more ancient slithering program along their head-to-toe body axis,” the authors said.
“We found that skates are primitive enough to have both axial and bipedal motor programs, slithering along their tails early in life, and walking later on with their pelvic fins.”
In addition, humans and skate use similar mechanisms to guide nerve cells as they wire from the spinal cord into limb muscle cells.
Based on genetic maps of innervation, both species for instance use dorsal neurons in the spinal CPG to control dorsal limb muscles.
They also use same proteins, such as ephrins, on the tips of spinal nerve cell extensions called axons to ‘find’ and connect to the right limb nerves.
“The nerve networks needed for walking were thought to be unique to land animals that transitioned from fishes, but our research has uncovered that the little skate and some basal sharks already had those neural networks in place,” Dr. Boisvert said.
“Our study suggests that the neural circuits that control walking were established, not as our ancestors first crawled onto land as once thought, but instead long before in primitive fish,” said lead author Dr. Jeremy Dasen, from the Department of Neuroscience and Physiology at NYU Langone Health.
“Given that that skates use many of the same neural circuits that we do to walk, but with six muscles instead of the hundreds we use, the fish provide a simple model to study how the circuits that enable walking are assembled.”
“Until we understand how spine-limb nerve connections are wired, we can’t expect to reverse spinal cord damage.”
“This research is very significant as the little skate could become a very good model for understanding the development of nerve networks controlling our limbs and also reveal further information about the diseases associated with them,” Dr. Boisvert said.
_____
Heekyung Jung et al. 2018. The Ancient Origins of Neural Substrates for Land Walking. Cell 172 (4): 667-682; doi: 10.1016/j.cell.2018.01.013
