The origin of all living vertebrates just got more mysterious.

Since the 1970s, many evolutionary biologists have considered an eel-like, deep-sea-dwelling creature called the hagfish to be the closest extant relative of a last common ancestor for all backboned creatures.

That made the hagfish a stand-in for a transitional species between invertebrates and higher animals, spanning a leap as dramatic as any in evolutionary history. But a new family tree based on high-powered molecular analysis lumps hagfish together with lampreys, a jawless fish that's primitive, but very much a vertebrate.

"It removes hagfish from representing the intermediate step, and makes the jump from invertebrates to vertebrates all the more formidable," said paleobiologist Philip Donoghue of the University of Bristol. "All of a sudden, you realize that you haven't got the faintest idea to sketch a last common ancestor."

Donoghue's study, co-authored with Dartmouth College biologist Kevin Peterson and published October 19 in the Proceedings of the National Academy of Sciences, is the latest in a series of attempts to arrange hagfish and lampreys in the tree of life.

Prior to the 1970s, researchers extrapolated their trees from comparisons of physical characteristics. On this basis, hagfish resembled lampreys. But when scientists used genetic analysis to revisit those comparisons, they found major genetic differences between the two species. Since hagfish have a skull but no backbone and only a rudimentary nervous system, they were interpreted as resembling an earlier, pre-lamprey evolutionary stage.

The new study goes beyond genes to the level of microRNA – molecular snippets that help turn genes on and off and seem to play a crucial role in allowing basic genetic components to be configured and reconfigured in ever-more-complex ways. As a guide for determining relationships between species, they're more reliable than genes. And they suggest that hagfish really are close relatives of lampreys, and have only evolved to seem more primitive.

Without hagfish, evolutionary biologists are left with a gap between complex invertebrates like sea squirts and amphioxus, and simple vertebrates like lampreys. Whatever went between them, "we don't even know what sort of sensory organs they had, how they made their living feeding, and so on," said Donoghue. The invertebrates provide little guidance. "Sea squirts are glorified water pistols. They're bags of water that make their living sucking in water through one tube, then squirting it out the other."

On the positive side, the reclusive, elusive hagfish made for a poor model organism, said Donoghue. "In the whole of the 20th century, only three embryos were found," he said. Only three years ago did researchers develop techniques for hatching their eggs. Evolutionary biologists may be better served comparing lampreys to sea squirts and amphioxus, and seeing how their genetic architecture – especially their microRNA – changed.

Such comparisons have already shown the jump from invertebrate to vertebrate was attended by a duplication of every gene in the genome, and an explosion in new types of microRNA. "There are more microRNAs acquired at the origin of vertebrates than at any other time in animal evolutionary history," said Donoghue. "It was just bizarre."

Images: 1) Lamprey attached to the side of an aquarium./Enrique Dans, Flickr. 2) Hagfish./Joe Kunkel, University of Massachusetts. 3) Sea squirts./Wikimedia Commons. 4) Amphioxus./Wikimedia Commons.

See Also:

Citation: "microRNAs reveal the interrelationships of hagfish, lampreys, and gnathostomes and the nature of the ancestral vertebrate." By Alysha M. Heimberg, Richard Cowper-Sallari, Marie Sémon, Philip C. J. Donoghue, and Kevin J. Peterson. Proceedings of the National Academy of Sciences, Vol. 107 No. 42, October 19, 2010.

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