Few fish would survive a swim in Antartica's ice-covered waters. Temperatures can drop to -1.9 ℃, whereas a typical fish starts to freeze at -0.8 ℃. If the water is colder, microscopic ice crystals will soon infiltrate the fish through gills and skin and start growing from within. Nerves are severed, tissues damaged, and the fish dies within minutes.
But crystals don't bother Antarctic icefish. These cold-adapted creatures carry antifreeze proteins in their blood and body fluids. The antifreeze proteins bind ice crystals and smother them by dividing the long and growing crystal fronts into many small and curved fronts. This inhibits crystal growth just enough to prevent the icefish from freezing.
The Antarctic Icefish rule the seas that lie over Antarctica's continental shelf. Here, more than 90% of all fish are icefish. There are over 132 different species of Antarctic icefish known to science. Some are native to the coastal waters of Australia and South-America, but the majority of them dwell near Antarctica.
Many biologists assume that the antifreeze proteins were the key to the icefish's evolutionary success. Antarctica went through a major period of cooling around 24 million years ago. Ice sheets formed and glaciers scoured over the continent. In a study that was published last year, German biologists found that the onset of this cooling event coincided with the origin icefish and the evolution of antifreeze proteins. Their conclusion was simple: the antifreeze proteins were the evolutionary innovation that triggered the diversification of icefish. With their newly acquired cold resistance, the ancestral icefish and their descendants invaded the frigid waters of the Antarctic and multiplied.
These ancestors were bottom dwellers. When they first spread out over the Antarctic shelf, a world of plenty awaited above their heads, full of tasty krill and opportunities. But this world was out of reach: icefish don't have a swim bladder. To rise up from the sea floor, ice fish evolved other tricks. Some replaced bone with cartilage, others store fatty molecules in sacs between their muscles and under their skin, as a kind of visceral floating devices.
But now a team of ecologists and biologists suggests there's more to this simple two-stage model. Their DNA analyses confirm that the last common ancestor of all Antarctic Icefish lived 22.4 million years ago, but also reveal that the majority of icefish diversity evolved 10 million years after these first origins. The Trematomus family originated 9 million years ago, the crocodile icefish 6 million years ago, and the Artedidraconidae 3 million years ago. These additional pulses of speciation occurred long after the first antifreeze proteins evolved.
The evolutionary path towards buoyancy was not straightforward either. In general, closely related species share similar ways of life. For example, one icefish family could have dominated the sea floor, whereas another lineage inhabits the upper waters. But when the biologists compared the buoyancy measurements of different icefish, they found a different pattern. Within each icefish family there were many species that had adapted to life at different depths. For icefish, there exists no link between niche and lineage.
Antarctica's harsh and erratic climate might explain this lack of direction in icefish evolution. While Antarctica has been a cool place for millions of years, the degree to which the continent and its surrounding waters have been covered by ice has varied. Sometimes the ice expanded as far as the edges of the continental shelf, wiping out the animal communities that lived there, only to suddenly retreat again, leaving a few isolated ice caps behind.
In 2008, polar researchers describe how Antarctic life might have 'hung by a thread' during such glacial periods. Fish and other creatures might have persisted in so-called 'polynyas', areas of open water surrounded by sea ice. Or in this case, oases in a desert of ice. Once the ice retreated again, the survivors had an empty sea floor all for themselves. The cycle of creation and destruction of ice would have brought in new waves of colonists every time, explaining why the different lineages of Icefish repeatedly colonized the different layers of the Antarctic Ocean.
This goes to show that nothing in evolution is as simple as it might first seem. 'Antifreeze proteins triggered icefish diversification' makes for a simple story, but it does not hold up once we take a closer, deeper look. Even with antifreeze, Antarctic life has treated icefish harshly.
For creatures so familiar with extreme cold, it remains to be seen how they will cope with a warming world. The authors conclude: "In a tragic twist of fate, the development of polar climatic conditions that shaped the radiation of Antarctic icefish is now reversing, and the increasing temperature of the Southern Ocean, with the associated potential for the arrival of invasive species and disruption of foodwebs, is the greatest threat to the survival of this unparalleled radiation of fish."
Climate change could be more than the icefish can take. There might be no icy oases this time.
Near, T., Dornburg, A., Kuhn, K., Eastman, J., Pennington, J., Patarnello, T., Zane, L., Fernandez, D., & Jones, C. (2012). Ancient climate change, antifreeze, and the evolutionary diversification of Antarctic fishes Proceedings of the National Academy of Sciences DOI: 10.1073/pnas.1115169109
Thatje S, Hillenbrand CD, Mackensen A, & Larter R (2008). Life hung by a thread: endurance of Antarctic fauna in glacial periods. Ecology, 89 (3), 682-92 PMID: 18459332
Matschiner M, Hanel R, & Salzburger W (2011). On the origin and trigger of the notothenioid adaptive radiation. PloS one, 6 (4) PMID: 21533117
Eastman, J. (2004). The nature of the diversity of Antarctic fishes Polar Biology, 28 (2), 93-107 DOI: 10.1007/s00300-004-0667-4
DEVRIES, A., & EASTMAN, J. (1978). Lipid sacs as a buoyancy adaptation in an Antarctic fish Nature, 271 (5643), 352-353 DOI: 10.1038/271352a0
Cheng, C. (2003). Functional Antifreeze Glycoprotein Genes in Temperate-Water New Zealand Nototheniid Fish Infer an Antarctic Evolutionary Origin Molecular Biology and Evolution, 20 (11), 1897-1908 DOI: 10.1093/molbev/msg208
Diagram from reference.