Lampreys are one of the only existing jawless vertebrates. The development of jaws originates from a crucial group of stem cells known as the neural crest. Recent studies shed light on the genetic regulatory changes that might clarify the physical differences between jawed and jawless vertebrates.
Sea lampreys, one of the two jawless vertebrate species causing significant disruption in Midwestern fisheries, simultaneously offer crucial insights into the origins of critical stem cells that influenced vertebrate evolution.
Researchers from Northwestern University have identified the timeline for the evolution of the gene network responsible for regulating these stem cells and have discovered potential reasons behind the absence of jaws in lampreys.
There are two primary cell types involved: pluripotent blastula cells (embryonic stem cells) and neural crest cells. Pluripotent means these cells have the capacity to evolve into any other cell type within the body.
In their latest study, scientists compared the genes of lampreys to those of the jawed aquatic frog, Xenopus. Through comparative transcriptomics, they found that the gene network associated with pluripotency is notably similar in both jawless and jawed vertebrates, even in terms of the quantity of key regulatory factors.
However, the team also made a significant finding. While the pou5 gene, essential for stem cell regulation, is expressed in the blastula cells of both species, it is absent in the neural crest cells of lampreys. The loss of this gene may have hindered neural crest cells’ ability to develop into specific cell types that are present in jawed vertebrates, contributing to the differences in jaw and head structures.
The study is set to publish on July 26 in the journal Nature Ecology & Evolution.
By examining both jawless and jawed vertebrates, scientists can better understand the evolutionary roots of features that characterize vertebrate animals, including humans, how variations in gene expression impact the structural differences among species, and what the ancestors of all vertebrates resembled.
“Lampreys may provide crucial insights into our evolutionary history,” stated Carole LaBonne from Northwestern, who led the research. “To comprehend the origin of a specific feature, it is essential to look back at the most primitive forms of the animal in question instead of more complex vertebrates that have diverged for 500 million years. This leads us to hagfish and lampreys, the last remaining jawless vertebrates.”
LaBonne, a specialist in developmental biology, is a professor of molecular biosciences in the Weinberg College of Arts and Sciences. She also holds the Erastus Otis Haven Chair and is involved in the leadership of the National Science Foundation’s new Simons National Institute for Theory and Mathematics in Biology.
Previously, LaBonne and her team showed that the origin of neural crest cells is closely tied to the retention of the gene regulatory network that manages pluripotency in blastula stem cells. In this new study, they investigated the evolutionary evolution of the relationship between these two stem cell types.
“Neural crest stem cells function like an evolutionary Lego set,” LaBonne explained. “They have the potential to morph into various cell types, such as neurons and muscle cells, while sharing a common developmental origin within the neural crest.”
Unlike blastula embryonic stem cells that quickly lose their pluripotency and specialize into distinct cell types during early development, neural crest cells maintain their pluripotency-related molecular tools for a longer duration during development.
The research team discovered that lamprey blastula cells possess an entirely intact pluripotency network, addressing long-standing questions regarding the role of these stem cells in jawless vertebrates. This suggests that the populations of blastula and neural crest stem cells in both jawed and jawless vertebrates evolved concurrently at the dawn of vertebrate evolution.
Joshua York, a postdoctoral fellow at Northwestern and the primary author, noted that their findings revealed “more similarities than differences” between lampreys and Xenopus.
“Although many genes managing pluripotency are present in the lamprey neural crest, the absence of one crucial gene, pou5, stood out,” York mentioned. “Remarkably, the introduction of pou5 into frog neural crest cells could encourage neural crest formation, suggesting this gene is part of an ancient pluripotency network found in our earliest vertebrate ancestors.”
The study also led them to theorize that the loss of this gene occurred specifically in certain lineages, rather than it being a later development in jawed vertebrates.
“A standout revelation from the research is that, despite being separated by 500 million years of evolutionary history, there is a strong constraint on the expression levels of genes necessary to maintain pluripotency.” LaBonne noted. “The major unresolved question remains: why?”
This research received funding from the National Institutes of Health (grants R01GM116538 and F32DE029113), the NSF (grant 1764421), the Simons Foundation (grant SFARI 597491-RWC), and the Walder Foundation through the Life Sciences Research Foundation, and is dedicated to the memory of Dr. Joseph Walder.
