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Invertebrates
The New York Times, January 18, 2010

When Built-In Antifreeze Beats a Winter Coat
By Sean B. Carroll

In the bleak midwinter

Frosty wind made moan,

Earth stood hard as iron,

Water like a stone;

Snow had fallen, snow on snow,

Snow on snow,

In the bleak midwinter

Long ago.

— Christina Rossetti (1872)

As the mercury plunges to its annual lows, those of us at higher latitudes retreat to cozy shelters. We might sympathize with the birds and the squirrels that endure the subfreezing cold outside and fill some feeders, but we don’t give any thought to smaller, less appealing creatures — the insects and spiders, for instance, that inhabited the backyard or woods in the summer.

They will re-emerge in the spring, so somehow they must make it through the bitter cold. How do these animals survive the deep freeze without the benefit of fur or feathers?

The threat to life at low temperatures is not really cold, but ice. With cells and bodies composed mostly of water, ice is potentially lethal because its formation disrupts the balance between the fluids outside and inside of cells, which leads to their shrinkage and irreversible damage to tissues.

Insects have therefore evolved all sorts of ways to avoid freezing. One strategy is to escape winter altogether. Butterflies like the monarch migrate south. A great solution, but this is a relatively rare capability. Most insects remain in their local habitat and must find some other way to avoid freezing. They evade the ice by crawling into holes or burrows below the snow cover and frost line, or, as some insect larvae do, by overwintering on the bottoms of lakes and ponds that do not completely freeze.

But many insects, and other animals, defend themselves against direct exposure to subfreezing temperatures through biochemical ingenuity, by producing antifreeze. In a previous column, I explained how different animal species defend themselves against predators with the same molecule acquired from their environment. By contrast, the story of defense against the cold is one of widespread and diverse innovations.

The first animal antifreezes were identified several decades ago in the blood plasma of Antarctic fish by Arthur DeVries, now at the University of Illinois, and his colleagues. The ocean around Antarctica is very cold, about 29 degrees Fahrenheit. It is salty enough to stay liquid several degrees below the freezing temperature of fresh water. The abundant ice particles floating in these waters are a hazard to fish because, if ingested, they can initiate ice formation in the gut and then — bang, you have frozen fish sticks. Unless something prevents the ice crystals from growing.

That is what the fish antifreeze proteins do. The tissues and bloodstream of about 120 species of fish belonging to the Notothenioidei family are full of antifreeze. These proteins have an unusual repeating structure that allows them to bind to ice crystals and to lower the minimum temperature at which the crystals can grow to about 28 degrees. That is just a bit below the minimum temperature of the Southern Ocean and about two full degrees lower than the freezing point of fish plasma that does not have antifreeze. This small margin of protection has had profound consequences. Antifreeze-bearing fish now dominate Antarctic waters.

The ability to survive and thrive in frigid water is impressive, but insects must survive much colder temperatures on land.

Some, like the snow flea, are active even in winter and can be found hopping about on snow banks when the temperature is as low as 20 degrees. These bugs are not really fleas, but springtails, a primitive wingless insect that can leap long distances using its tail. Laurie Graham and Peter Davies at Queen’s University in Kingston, Ontario, isolated antifreeze proteins from snow fleas and discovered that they also had a simple repeating structure that bound to ice and prevented crystal growth.

The snow flea antifreeze proteins have an entirely different composition from those of antifreezes that have been isolated from other insects, like the fire colored beetle, which has antifreeze proteins that are in turn different from those of the spruce budworm caterpillar. And all of these insect antifreezes are distinct from the kind that keeps Antarctic fish alive. Each animal’s antifreeze is a separate evolutionary invention.

But insect innovation goes beyond antifreeze. Biologists have discovered another strategy for coping with extreme cold: some bugs just tolerate freezing.

In the most northern climates, like the interior of Alaska, midwinter temperatures fall as low as minus 60 degrees Fahrenheit, and snow cover and subzero temperatures can last until May. At these extreme temperatures, most insects are bugsicles. The Alaskan Upis beetle, for example, freezes at around minus 19 degrees. But, remarkably, it can survive exposure to temperatures as low as about minus 100 degrees.

To tolerate freezing, it is crucial that insects minimize the damage that freezing (and thawing) would normally cause.

Insects have evolved a variety of cryoprotective substances. As winter approaches, many freeze-tolerant insects produce high concentrations of glycerol and other kinds of alcohol molecules. These substances don’t prevent freezing, but they slow ice formation and allow the fluids surrounding cells to freeze in a more controlled manner while the contents of the cells remain unfrozen.

For maximum protection, some Arctic insects use a combination of such cryoprotectants and antifreezes to control ice formation, to protect cells and to prevent refreezing as they thaw. Indeed, a new kind of antifreeze was recently discovered in the Upis beetle by a team of researchers from the University of Notre Dame and the University of Alaska-Fairbanks. Unlike the protein antifreezes of other beetles, snow fleas and moths, the Upis antifreeze is a complex sugar called xylomannan that is as effective at suppressing ice growth as the most active insect protein antifreezes.

The necessity of avoiding freezing has truly been the mother of a great number of evolutionary inventions. This new finding raises the likelihood that there are more chemical tricks to discover about how insects cope with extreme cold.

This is not merely a matter of esoteric Arctic entomology.

A long-standing challenge in human organ preservation has been precisely the problem that these insects have solved — how tissues can be frozen for a long time and then thawed out successfully. Research teams are now exploring how to apply insights from the animal world to the operating room.

Sean B. Carroll, a molecular biologist and geneticist, is the author of “Remarkable Creatures: Epic Adventures in the Search for the Origin of Species.”

Photo © Paul S. Hamilton