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Fish raised on land give clues to how early animals left the seas

When raised on land, a primitive, air-breathing fish walks much better than its water-raised comrades, according to a new study. The landlubbers even undergo skeletal changes that improve their locomotion. The work may provide clues to how the first swimmers adapted to terrestrial life.   

The study suggests that the ability of a developing organism to adjust to new conditions—its so-called developmental plasticity—may have played a role in the transition from sea to land. “It was a very adventurous study, and it paid off,” says Richard Blob, an evolutionary biomechanist at Clemson University in South Carolina who was not involved in the work. “They are bringing in a novel perspective and got some very thought-provoking results.”

While a postdoctoral fellow at McGill University in Montreal, Canada, Emily Standen decided to raise fish out of water because her graduate school study of fish fins had led her to appreciate how versatile these appendages can be. She teamed up with Hans Larsson, a McGill paleontologist, to determine if a life on land led to the changes necessary to thrive there. They picked a bichir to study because this fish looks like an ancestor to land animals: It’s long, has lungs and big bony scales, and uses the large pectoral fins behind its head to haul itself around on land to go to new watering holes. Also, bichirs sit at the base of the vertebrate family tree, close to the split between the so-called ray-finned fish (which include most kinds of fish) and the group that includes lobe-finned fish (such as lungfish and coelacanths) and the land animals—the tetrapods.

Standen bought 149 2-month-old bichirs from a pet supplier and kept 111 of them in a terrarium for 8 months and the rest in an aquarium. She compared the skeletons and the swimming and walking abilities of the water-reared and land-reared adults.

The bichirs raised on land were better walkers, with changes in their bones that likely help improve terrestrial locomotion, she and her colleagues report online today in Nature. In the land-raised fish, the front fins, instead of being splayed out to the sides, extended almost straight down, lifting the animals’ heads higher off the ground so they could put more weight on the fins. Thus, when these bichirs push off with a fin to take a step, their fins don’t slip and they can take quicker steps (see video).

The bones that support the fins and attach them to the back of the head took on new shapes. Those bones make up the pectoral girdle. One bone, the equivalent of our collarbone that extends under the chest, grew longer so that it could better support the body. The connection between it and another bone that goes up the side of the fish got stronger, but that bone itself thinned to allow more room for the head to swing from side to side. Contact between another pectoral girdle bone and the skull was also reduced, allowing the head to move up and down. Most fish don’t need such flexibility in the head, because in water they can easily move the body to look or eat in a different direction. “All the changes [we saw] are changes that you see in the fossil record,” says Standen, who is now an evolutionary and comparative biomechanist at the University of Ottawa.

“The results cast light on a factor that may have had a part in the origin of tetrapods,” says Per Ahlberg, a paleontologist at Uppsala University in Sweden. But because researchers don’t have a way to go back in time to see whether the tetrapod ancestors exhibited developmental plasticity, “how big a role it had in their evolution is really difficult to say.” And some biologists now think that limbs evolved in aquatic fish and are not derived from fins of primitive fish that took to the land, so plasticity on land would be moot.

Yet Armin Moczek, an evolutionary developmental biologist at Indiana University, Bloomington, who was not involved with the work, thinks the study is important. It’s very difficult to see how organisms get started on a new evolutionary trajectory, he says. “Developmental plasticity can facilitate the first couple of stages that can ultimately lead to an massive evolutionary transition.”

In Standen’s experiments, the fish showed a flexible response during development that caused them to look and act different from their parents and other bichirs. Such plasticity can influence evolution indirectly, Standen explains. If the new behavioral and skeletal traits brought about by the stress of living on land provide a survival advantage, then fish with their heads up the highest, more effective stride, and so on will be more likely to survive and pass on the genes that confer developmental plasticity. Subsequent generations will still have plastic responses, but “eventually those plastic responses can become [permanent] over many generations and over time,” she proposes. How this happens, she cautions, remains “a mystery.”

Michael Coates, a paleontologist at the University of Chicago in Illinois, thinks that scenario is feasible. However, the tricky part is figuring out where plasticity came into play, as there are many fossils of different fish and fishlike animals that may have been involved in the water-to-land transition. Nonetheless, “it seems to me that one of the points the paper is making is that this ought to be studied,” says Coates, who was not involved with the work. And Standen plans to see what happens to the next generation of land-reared fish.

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