Dragon fish experiment could shed light on shift from fish to four legs

Dragon fish have lungs and can scooch themselves across dry land. The experiment appeared to trigger changes in the fish that parallel changes that scientists see in the fossil record.

Antoine Morin/Nature

Dragon fish can wreak havoc in the family fish tank. They eat smaller fish and aren't afraid to snack on the fins of larger ones or each other.

But what the fish, formally known as Polypterus senegalus, lack in civility, they more than make up for in scientific interest. They have two fully formed lungs. They can survive out of water. And they can scooch themselves across dry land in search of the next pond.

Now, after an eight-month experiment, researchers have shown that dragon fish raised outside an aquarium are more adept at moving across surfaces than their water-raised counterparts. As the fish matured in a non-aquatic environment, the fish's behavior in that environment imposed measurable changes on bones and muscles involved in locomotion, the scientists report.

In effect, P. senegalus – a freshwater fish from Africa and a living fossil along with lungfish and furtive coelacanths – appears to have opened a unique window on behavioral and biological processes that drove the evolution of fish to four-limbed vertebrates some 400 million years ago, the researchers say.

In the process, dragon fish may become the latest poster child for a feature of biology known as developmental plasticity, adds Hans Larsson, who holds the Canada Research Chair in Vertebrate Paleontology at McGill University's Redpath Museum in Montreal.

In essence, this plasticity is expressed when environmental changes or stresses alter an organism's physique. The changes at first are subtle, Dr. Larsson explains. But the expectation is that if these changes confer an advantage to an organism, over time the changes will work their way into the organism's genome, to be passed to succeeding generations. Some researchers see this as a powerful force driving evolution.

Critics of this marriage of plasticity and evolution, championed by Mary Jane West-Eberhard, staff scientist emerita with the Smithsonian's Tropical Research Institute in Panama, have argued that there is little convincing evidence for changes in body structure driven by environmental stresses, never mind those changes leading to inheritable genetic changes.

The dragon fish in this new experiment may provide at least a partial answer to the first objection. The team picked the species because it belongs to the genus that represents the most primitive form of spiny-finned fish – fish whose fins are supported by a row of spines or bones. These constitute some 99 percent of all the fish species on earth.

Dragon fish can grow up to 14 inches long. The researchers recorded the changes as the young fish grew from just under half an inch long to an average of four inches long.

"We wanted to push them in this new environment to see if we could reveal this cryptic variation, and if it works, what does it look like?" says Larsson, the senior author on a formal description of the results appearing in Thursday's issue of the journal Nature.

The hope was that the changes between the water-raised dragon fish and their terrestrial counterparts would look vaguely like the changes seen in the fossil record for fish during the piscine-to-tetrapod transition, he adds.

Trends in anatomical changes to the dragon fish raised outside an aquarium "were shockingly similar" to those that appear in the fossil record, he says. Indeed, the evidence for anatomical changes in these fish was stronger and more widespread than the team anticipated.

The "terrestrialized" fish were raised outside water-filled tanks, but they still needed water. Their environment was kept in a kind of wetland condition, with perhaps a millimeter or so of water on the surface. In addition, the team used vegetable misters to keep the terrestrialized fish moist.

The team used detailed 3-D video of the fish and used a micro version of the CT scan technology that hospitals use to image the interior of the human body.

Among their findings at the end of eight months:

• Walking behavior among the terrestrials was less haphazard than the fish raised in water.

• The terrestrial fish planted their pectoral fins-cum-legs closer to their bodies' center lines, and the fins exhibited less slipping and sliding than did the fins of waterborne fish as they moved outside their aquariums. The terrestrial fish took shorter steps. Their heads were lifted higher off the surface, and they used their tails less than did the aquarium-raised fish to help propel themselves across a surface.

• The portion of their skeleton that would correspond to a chest became elongated with stronger attachments, a change that would not only affect walking, but also begin to separate this portion of the skeleton from the skull, leading to more flexible head – and perhaps eventually neck – motions.

• For all the changes they were undergoing, the terrestrials were no worse at swimming than their water-raised control group.

The experiment was conceived, designed, and executed by Emily Standen, who specializes in evolutionary biomechanics at the University of Ottawa and is the lead author on the Nature paper reporting the results. McGill graduate student Trina Du did the heavy lifting in analyzing the micro CT scans and videos that the experiment produced.

The project was a bold one, according to John Hutchinson, a professor of evolutionary biomechanics at the Royal Veterinary College in Britain, who was not part of Dr. Standen's team.

"It was a hard experiment – lots of animals and lots of data," he says. It isn't one that can be casually redone.

"Luckily, the results look pretty good," and the authors have made it easy to check them, he says.

Dr. Hutchinson and Larsson have an ambitious list of follow-up experiments they'd like to perform. For his part, Hutchinson says he would like to see these fish traverse special plates that record the forces that the fish's fins exert as they walk. And he says he'd like to see a more detailed comparison between the dragon fish and the fossil record – a laborious task, but one well within reach given the wealth of fossils available, he adds.

Larsson also is interested in the mechanics – making detailed measurements of every part of the fish's step cycles. From a biological standpoint, he says, another frontier to explore is differences in metabolism – from eating to elimination – between the terrestrial-raised and aquatic-raised fish. These processes also should be experiencing developmental plasticity.

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