These bizarre blood-sucking fish have a “surprising” evolutionary origin

These aggressive, blood-sucking fish “may hold the key to understanding where we came from.”

one of only two jawless animals SpineSea lampreys, which are causing significant damage to Midwestern fisheries, are also helping scientists understand the origins of two important stem cells that played a crucial role in the evolution of vertebrates.

Northwestern University Biologists have determined when the gene networks that control these stem cells evolved, and have also found insights into what may cause the lamprey to lose its jaws.

The two types of cells — pluripotent blastula cells (or embryonic stem cells) and neural crest cells — are both “pluripotent,” meaning they can become all other cell types in the body.

In a new paper, the researchers compared lamprey genes to those of Xenopus, a jawed aquatic frog. Using comparative transcriptomics, the study revealed a surprisingly similar pluripotency gene network in jawless and jawed vertebrates, even at the level of transcript abundance for key regulatory factors.

Differences in gene expression

But the researchers also found a significant difference. species‘Blastula cells express the pou5 gene, a key stem cell regulator, a gene that is not expressed in neural crest stem cells in lampreys. Losing this factor may limit the ability of neural crest cells to form the cell types found in jawed vertebrates (animals with backbones) that form the skeleton of the head and jaw.

This study has been published recently in the journal Nature Ecology and Evolution.

By comparing the biology of jawless and jawed vertebrates, researchers can gain insight into the evolutionary origins of features that define vertebrate animals, including humans, how differences in gene expression contribute to major differences in body structure, and what the common ancestor of all vertebrates looked like.

“Lampreys may be the key to understanding where we came from,” said Northwestern’s Carole LeBon, who led the study. “In evolutionary biology, if you want to understand where a feature came from, you can’t expect to look to more complex vertebrates that have been evolving independently for 500 million years. You need to look at the most primitive version of the type of animal you’re studying, which takes us back to hagfish and lampreys — the last surviving examples of jawless vertebrates.”

An expert in developmental biology, LaBonne is a professor of molecular biosciences in the Weinberg College of Arts and Sciences. She holds the Erastus Otis Haven Chair and is part of the leadership of the National Science Foundation’s (NSF) new Simons National Institute for Theory and Mathematics in Biology.

LaBonne and his colleagues previously demonstrated that the developmental origin of neural crest cells was linked to maintaining the gene regulatory network that controls pluripotency in blastula stem cells. In the new study, they explored the developmental origins of the relationship between these two stem cell populations.

Importance of Neural Crest Cells

“Neural crest stem cells are like an evolutionary Lego set,” LaBonne said. “They become very different cell types, including neurons and muscle, and what all of those cell types have in common is a shared developmental origin within the neural crest.”

Whereas blastula-stage embryonic stem cells lose their pluripotency and become restricted to distinct cell types fairly rapidly as the embryo develops, neural crest cells retain the molecular toolkit that regulates pluripotency later in development.

Labonne’s team found a fully intact pluripotency network within lamprey blastula cells, stem cells whose role within jawless vertebrates had been an open question. This implies that the blastula and neural crest stem cell populations of jawed and jawless vertebrates co-evolved at the base of vertebrates.

Joshua York, a postdoctoral fellow at Northwestern and first author, saw “more similarities than differences” between lampreys and Xenopus.

“While most of the genes that control pluripotency are expressed in the lamprey neural crest, expression of one of these key genes — pou5 — was lost from these cells,” York said. “Surprisingly, even though pou5 is not expressed in the neural crest of lampreys, when we expressed it in frogs it could promote neural crest formation, suggesting that this gene is part of an ancient pluripotency network that existed in our early vertebrate ancestors.”

The experiment also led them to speculate that the gene was lost specifically in certain primates, rather than evolving later in jawed vertebrates.

“Another remarkable finding of the study is that even though these animals have evolved over 500 million years, there are rigid constraints on the expression levels of the genes needed to promote pluripotency,” Labonne said. “The big unanswered question is why?”

Reference: “Shared features of blastula and neural crest stem cells evolved across vertebrates” by Joshua R. York, Anjali Rao, Paul B. Huber, Elizabeth N. Shock, Andrew Montequin, Sarah Rigney, and Carole LaBonne, July 26, 2024, Nature Ecology and Evolution,
DOI: 10.1038/s41559-024-02476-8

This paper was funded by National Institutes of Health (grants R01GM116538 and F32DE029113), NSF (grant 1764421), Simons Foundation (grant SFARI 597491-RWC) and the Walder Foundation through the Life Sciences Research Foundation. This study is dedicated to the memory of Dr. Joseph Walder.