Big heart, acute senses key to explosive radiation of early fishes

An international team led by scientists from the Canadian Museum of Nature and the University of Chicago reconstructed the brain, heart, and fins of an extinct fish called Norselaspis glacialis from a tiny fossil the size of a fingernail. They found evidence of change toward a fast-swimming, sensorily attuned lifestyle well before jaws and teeth were invented to better capture food. 

“These are the opening acts for a key episode in our own deep evolutionary history,” said Tetsuto Miyashita, research scientist at the Canadian Museum of Nature and lead author of the new study published in the journal Nature.

Jaws changed everything – but maybe not first

Fish have been around for half a billion years. The earliest species lived close to the seafloor, but when they evolved jaws and teeth, everything changed; by 400 million years ago, jawed fishes dominated the water column. Ultimately, limbed animals – including humans – also originated from this radiation of vertebrates.

It has long been a mystery, however, how this pivotal event occurred. The standard theory holds that jaws evolved first, and other body parts underwent changes to sustain a new predatory lifestyle. “But there is a large data gap beneath this transformation,” said Michael Coates, Professor and Chair of Organismal Biology and Anatomy at the University of Chicago and a senior author of the study. “We’ve been missing snapshots from the fossil record that would help us order the key events; to reconstruct the pattern and direction of change.”

The new study flips the “jaws-first” idea on its head. “We found features in a jawless fish, Norselaspis, that we thought were unique to jawed forms,” said Miyashita, who was formerly a postdoctoral fellow in Coates’ lab in Chicago. “This fossil from the Devonian Period more than 400 million years ago shows that acute senses and a powerful heart evolved well before jaws and teeth.”

But the team also needed a chance encounter and a special tool to gain these insights into the inner workings of Norselaspis.

Synchrotron X-rays reveal ghosts of organs never seen before

The fossil of Norselaspis the team studied is so exquisitely preserved in a fragment of rock that they were able to scan it and see impressions of its heart, blood vessels, brain, nerves, inner ears, and even the tiny muscles that moved the eyeball. The fossil was hidden in one of thousands of sandstone blocks collected during a French paleontological expedition to Spitsbergen, Norway’s Arctic Archipelago, in 1969. 

Sorting through these rocks 40 years later, the study’s co-authors Philippe Janvier and Pierre Gueriau split one open, revealing a perfectly preserved cranium of Norselaspis barely half an inch long. The team took the fossil to Switzerland to scan it with high-energy X-ray beams at the TOMCAT beamline of the Swiss Light Source SLS.

“We used a technique known as X-ray tomographic microscopy,” said Federica Marone, TOMCAT beamline scientist at the SLS. “This allowed us to non-destructively study the 3D details of the fossil at very high resolution, and gain insights that have never been seen before,” 

The result was jaw-dropping. Slice by slice, the X-ray images revealed with astonishing detail delicate bone membranes that enclosed the fish’s organs. These tissue-thin bones capture the ghosts of organs formerly held by the skeleton. 

"Making use of the tiny refraction of the X-ray beam going through the sample, in addition to its commonly used absorption, we have been able to boost the contrast between similar tissues,” explains Marone. “This enabled us to image these tiny bones, only a hundredth of a millimetre wide, which show the imprints of now lost organs.”

 

X-ray tomographic microscopy of tiny, 400-million-year-old fish shows how anatomy geared toward evading predators equipped it to become the hunter once jaws evolved. © Michael Coates, University of Chicago

 

Avocado ears and a melon heart 

Over thousands of screen hours, this X-ray data was digitally dissected and stitched together to make a map of the fish’s anatomy.

“With this exquisite digital atlas, we now know Norselaspis in greater anatomical detail than many living fishes,” Miyashita said. For example, the fish had seven tiny muscles to move its eyeballs, whereas humans have six. It had outsized inner ears, an enormous heart, and vessels arranged like highway bypasses to carry more blood. “If Norselaspis was to our scale, its inner ears would be each the size of an avocado, and its heart would be as large as a cantaloupe melon,” he said.

Fish use their inner ears in much the same way that we humans use ours, to sense vibration, orientation, and acceleration. The capacious heart and greater blood flow provide more horsepower for the animal. “One might even say Norselaspis had the heart of a shark under the skin of a lamprey,” Miyashita said.

The fish also sported a pair of tilted, paddle-like fins behind the gills, which Coates explained would have been useful for making sudden stops, bursts and turns. These anatomical innovations made Norselaspis something of a sportscar among the generally sluggish jawless fishes of its time.

From escape artist to predator

Such “action-packed” anatomy likely evolved for evading predators rather than for chasing prey. But what triggers rapid escape responses in jawless fish would in turn give jawed fish an advantage to do the opposite, detecting and capturing food efficiently. 

“When jaws evolved against this background, it brought about a pivotal combination of sensory, swimming, and feeding systems, eventually leading to the extraordinary variety and abundance of Devonian fishes,” Coates said.

The earliest jaws were probably better adapted for sucking up food along with water and mud than for snapping at passing prey, however. “It wasn’t as simple as marching straight from a bottom feeder to an apex predator,” Miyashita said.

Clues to how vertebrates took shape

The new study also challenges the idea that shoulders and arms in modern tetrapods (four-limbed vertebrate animals) evolved from modified gill structures. The team traced the nerve going to the shoulder in Norselaspis and saw that it was separate from the nerves going to the gills – clear evidence that one did not come from the other. Instead, the team argues that the shoulder evolved as a new structure with a new domain, the neck, separating the head from the torso.

“A lot of these evolutionary changes have to do with how the head is attached to the trunk,” Miyashita said. In primitive jawless fishes, the head is continuous from the torso, while jawed vertebrates have a neck and throat to separate the two regions. Norselaspis is in the middle – its head is directly attached to the shoulder without a neck, almost as if arms in humans were sticking out behind the cheeks. But the organs at this interface, like inner ears, shoulders and a heart, are enhanced or reorganized for greater abilities to navigate its environment. 

Paleontologists are still investigating what ignited this transformation. Some, like Christian Klug of the University of Zurich, Switzerland, who was not involved in the study, believe the lineage of Norselaspis arose in the time of the so-called Nekton Revolution, when marine organisms were beginning to move up in the water column. The game then was about getting faster, smarter, and more manoeuvrable.

“For a historical event, we often emphasize one or two symbolic moments to the point of becoming a cliché. In this sense, the evolution of jaws is like a gunshot in Sarajevo that started World War One in 1914,” Miyashita said. “But it is imperative we understand the context. With Norselaspis, we can really find it in its heart.”

Since the X-ray tomographic measurements that revealed Norselapsis’ anatomy, the SLS and its beamlines have undergone a comprehensive upgrade. In addition to the original and now refurbished beamline (now called S-TOMCAT), the upgraded TOMCAT portfolio now includes a second, brand-new beamline (I-TOMCAT) –  built explicitly for high resolution and high throughput experiments. 

“With the new capabilities, we will be able to uncover details in fossils that were previously hidden,” says Marone. “Having access to such a new level of detail could transform our understanding of how life on Earth evolved.”