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Evolution Of Fish Antifreeze Gene Sheds Light On Climate History

National Science Foundation

New research shows that fish in the Antarctic and Arctic oceans, at opposite ends of the earth, independently evolved nearly identical antifreeze glycoproteins.

Studies by biologists have pinpointed the parent of the Antarctic antifreeze gene: a digestive enzyme called trypsinogen. The researchers also suggest that the gene arose five to 14 million years ago, providing a new line of evidence to confirm when the Southern Ocean froze.

Two papers in the April 15, 1997 issue of the National Academy of Sciences' Proceedings describe a rare, direct link between the evolution of a protein, the diversification of an animal and environmental change. The authors, supported by National Science Foundation (NSF) grants, are Liangbiao Chen, Arthur DeVries, and Chi-Hing C. Cheng, all from the University of Illinois.

Millions of years ago, fish in both northern and southern polar waters adapted to a cooling climate by evolving antifreeze proteins that kept them from freezing in frigid oceans, and let them exploit new ecological niches. The new research traces for the first time the genetic process by which a novel protein evolved to enable this adaptation.

The researchers show that the gene for antifreeze glycoprotein (AFGP), found in the Antarctic family of notothenioid fishes, evolved in a unique way: arising "whole cloth" from trypsinogen, an enzyme produced by the pancreas. New genes are usually created through recycling of existing protein genes.

"This is the first clear example of how an old protein gene spawned a gene for an entirely new protein with a new function," said Cheng. It is also one of very few newly-minted genes whose evolution can be so clearly traced.

"Demonstrations of this sort at the molecular level are rare and noteworthy," write John Logsdon and W. Ford Doolittle in a commentary on the paper.

The AFGP gene differs very little from its parent -- only 4 percent to 7 percent in the inherited gene segments -- so in evolutionary terms, its molecular clock began ticking quite recently. Segments at both ends of the gene are nearly identical to the parent trypsinogen gene. Applying the known rate at which DNA evolves in salmon mitochondria to the amount the AFGP gene has diverged from trypsinogen, the authors have pegged the gene's origin at five to 14 million years ago, close in time to the estimated freezing of the Antarctic Ocean. The freezing date was deduced independently, through studies of changing temperature as recorded in plankton in ocean sediments.

Some biologists had argued that Arctic cod, which produce very similar AFGPs, evolved from the same stock as the Antarctic fish. But DeVries, who discovered the first antifreeze gene in Antarctic fish thirty years ago, says the new molecular evidence shows that the two polar fishes, the Arctic cod and the Antarctic notothenioid, developed their antifreeze genes separately. By sequencing and analyzing -- essentially working out the architecture -- of the Arctic AFGP gene, the authors show that it does not resemble the gene for trypsinogen, and differs from its southern counterpart in gene structure and coding sequences as well.

The similar AFGPs in two unrelated fishes exemplify convergent evolution -- the development of a similar protein from different parents under similar environmental pressure.

The notothenioid family now dominates Antarctica's continental shelf, comprising more than half of the species and 95% of the biomass, or weight, of fish there. The fish arose in the deep ocean, but underwent a burst of evolutionary radiation into different ecological niches as the Southern Ocean cooled. In an evolutionary pattern akin to Darwin's finches, they are the only example of an oceanic fish to show this adaptive radiation. The antifreeze protein was evidently a key mechanism that let them colonize different depths of water.


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