How did fish develop their bony, scaly armor?

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Reconstruction of a sturgeon sturgeon, close-up. Bone-forming cells are highlighted in purple. Credit: J. Stundl

About 350 million years ago, your evolutionary ancestors—and the ancestors of all modern vertebrates—were just soft-bodied ocean-dwelling animals. In order to survive and evolve into what we are today, these animals needed to have some protection and advantages over ocean predators, which were then dominated by crustaceans.

The evolution of leathery armor, such as the sharp spines found on armored catfish or the diamond-shaped, bony scales called scales that cover sturgeons, was a successful strategy. Thousands of species of fish use different styles of dermal shields, consisting of bone and/or a material called dentin, an important component of modern human teeth. The protective coatings helped such vertebrates survive and evolve into new animals and eventually into humans.

But where did this shield come from? How did our ancient underwater ancestors evolve to grow this protective coat?

Now, using sturgeon, a new study has found that a specific group of stem cells, called stump neural crest cells, are responsible for the development of the osteosarcoma in the fish. The work was conducted by Jan Standell, now a Marie Sklodowska-Curie postdoctoral researcher in the lab of Marianne Brunner, the Edward B. Lewis Professor of Biology and director of the Beckman Institute at Caltech. A paper describing the research appears in the journal Proceedings of the National Academy of Sciences On July 17th.

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Brunner’s lab has long been interested in studying neural crest cells. These cells are found in all vertebrates including fish, chicken, and ourselves, and they specialize based on whether they arise from areas of the head (the skull) or the spinal cord (the trunk). Both cranial and trunk neural crest cells migrate from their starting points throughout the developing animal’s body, giving rise to the cells that make up the jaws, heart, and other important structures.

After a 2017 study from the University of Cambridge showed that neural stem cells give rise to an ivory-based skin shield in a species of fish called tiny skates, Stundell and his colleagues hypothesized that the same set of cells might also give rise to bone. – Armor based on large scale vertebrates.

To study this, Stundl and the team turned to sturgeon, specifically the sterlet sturgeon (Acipenser ruthenus). Modern sturgeon, known for producing the world’s most expensive caviar, still have many of the same characteristics as their ancestors millions of years ago. This makes them prime candidates for evolutionary studies.

Jan Standell holds a sturgeon in the laboratory. Credit: J. Stundl

Using sturgeon embryos cultured at the Research Institute of Fish Breeding and Aquatic Biology in the Czech Republic, Stundl and his team used a fluorescent dye to track how the neural crest cells of the fish’s trunk migrate throughout its developing body. Sturgeons begin developing their ossicles after two weeks, so the researchers kept the developing fish in a dark lab so they wouldn’t disturb the fluorescent dye with light.

The team found fluorescently labeled stem neural crest cells at the exact sites where the sturgeon’s ossicles were forming. Then they used a different technique to highlight the osteoblasts, a type of cell that forms bone. Gene signatures associated with osteoblast differentiation were found in fluorescent cells in developing fish scales, providing strong evidence that the neural crest cells of the stem in fact give rise to osteogenic cells.

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Combined with 2017 findings on the role of neural crest cells in the formation of an dentin-based shield, the work shows that dendritic neural crest cells are indeed responsible for the emergence of the ectodermal-osseous shield that enabled the evolutionary success of vertebrate fish.

“Working with non-model organisms is challenging; tools on standard laboratory organisms such as the mouse or zebrafish either don’t work or need to be highly adapted,” says Stündl. “Despite these challenges, information from non-model organisms such as sturgeon allows us to answer fundamental evolutionary biology questions in a rigorous manner.”

“By studying the many animals on the tree of life, we can infer the evolutionary events that took place,” Bruner says. “This is especially powerful if we can approach evolutionary questions from the perspective of evolutionary biology, because many of the changes that lead to different types of cells occurred through small modifications in embryonic development.”

The paper is titled “Ancient Vertebrate Skin Shield Evolution from the Trunk Neural Crest”.

more information:
Jan Standell et al., Ancient vertebrate skin shield evolved from trunk neural crest, Proceedings of the National Academy of Sciences (2023). DOI: 10.1073/pnas.2221120120

Journal information:
Proceedings of the National Academy of Sciences

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