Long-accepted theory of vertebrate origin upended by fossilized lamprey larvae

Lampreys are ancient, jawless, eel-like fishes that arose around half a billion years ago and they have long provided insights into vertebrate evolution. Now, scientists with the Canadian Museum of Nature, the University of Chicago and the Albany Museum in South Africa are reporting their analysis of dozens of tiny fossils that track the life stages and growth of ancient lampreys, from hatchlings to juveniles to adults.

Their results counter the established view that the blind, filter-feeding larvae of modern lampreys (called ammocoetes) are a holdover from the ancestors of all living vertebrates. The new fossil discoveries show that ancient lamprey hatchlings were completely unlike their modern larvae counterparts.

"We've basically removed lampreys from the position of the ancestral condition of vertebrates," explains lead author Tetsuto Miyashita, Ph.D, a palaeontologist with the Canadian Museum of Nature. "So now we need an alternative."

Miyashita explains that lampreys have a curious life cycle. "Once hatched, the larvae of modern lampreys bury themselves in a riverbed and filter feed before eventually metamorphosing into blood-sucking adults. The larvae are so different from adults that scientists originally thought they were different species. Even after finding out they are just an early phase in the lamprey life cycle, scientists saw the image of our distant ancestors in these seemingly primitive larvae."

The newly discovered lamprey fossils are now changing this story. The fossils, belonging to four extinct species, were discovered in South Africa and the United States (Illinois and Montana) and range in age from 310 to 360 million years old. The researchers found that the smallest individuals, barely 15mm in length (fingernail sized), still carried a yolk sac, signalling that these had only just hatched before dying. Further examination revealed that these youngsters already had large eyes and were armed with a toothed sucker, characteristics that in modern lamprey species only develop in the adults.

"Remarkably, we've got enough specimens to reconstruct a trajectory from hatchling to adult in several independent lineages of early lampreys," said Michael Coates, Ph.D, a biology professor at UChicago and co-author of the study along with Rob Gess, Ph.D at the Albany Museum and Kristen Tietjin at the University of Kansas. "They each show the same pattern: the larval form was like a miniature adult."

The researchers say that these results run counter to the 150-year-old evolutionary narrative that modern lamprey larvae, with their curious life cycle, offer a glimpse of deep ancestral vertebrate conditions. By demonstrating that ancient lampreys never went through the same blind, filter-feeding stage seen in modern species, the researchers have falsified the conventional ancestral model shared in textbooks.

After their examination of the fossil record, the researchers now believe that extinct armored fishes known as ostracoderms might instead represent better candidates for the root of the vertebrate family tree, whereas modern lamprey larvae are a more recent evolutionary innovation.

If so, then why do modern lamprey larvae appear so primordial? The team suggests that the evolution of filter-feeding larvae may have been an innovation that allowed lampreys to populate rivers and lakes. Fossil lampreys reported in the new study all came from marine sediments, but modern lampreys, with their filter-feeding, blind larvae, mostly live in freshwater.

For ancient blood-sucking lampreys, rivers and lakes would be tough environments in which to migrate because of the limited and unpredictable supply of prey. "Lampreys solved this problem by burrowing in sand and slurping up whatever food particles were available until they could mature enough to start looking for prey with blood," said Miyashita. "But you don't have to be too complicated for this kind of lifestyle. So even though lampreys invented this filter feeding larval phase anew, the larvae themselves looked simple and primordial. Until now we were misinterpreting this simplicity for primitiveness."

The researchers say that this is the sort of discovery that can rewrite textbooks. "Lampreys are not quite the swimming time capsules that we once thought they were," said Coates. "They remain important and essential for understanding the deep history of vertebrate diversity, but we also need to recognize that they, too, have evolved and specialized in their own right."