Iceburg with penguins, Antarctica

Historical contingency shapes adaptive radiation in Antarctic fishes


We recently concluded a study illuminating the genomic substrate for adaptive radiation in the group and linking the genetics of boneloss in notothenioids to the genetics of human bone disease.

Background

The cooling of the Southern Ocean surrounding Antarctica, which began approximately 35 million years ago and gave rise to its present icy state, has for decades been considered a classic example of climate change triggering rapid adaptation.

Using tens of thousands of genes mapped from across the genomes of Antarctic notothenioids, and working with a team from Yale, Harvard, and Northeastern Universities, we challenged this paradigm.

We found that the massive amount of genetic change required for life in the Antarctic occurred long before the Antarctic cooled.

These genetic changes not only have major implications for understanding the evolution of Antarctica’s unusual animals, but also highlight that some key adaptations used by fishes mirror the genetics of human disease.

Some of the over 100 species of Notothenioids that have taken over the Antarctic. Photos from T. Near

Specifically, we saw changes in key genes linked to human bones diseases also changing the level of skeletal bone density in these fish. These genes have been long been linked to human birth defects and skeletal disorders.

Notothenioids as models of human disease

Many species have evolved traits that are adaptive in their environment but are similar to disease states in humans and we can use this natural variation to better understand genetic mechanisms of disease.

In our case, we found that an increase in mutation rate prior to the onset of polar conditions in the Southern Ocean corresponds to a severe reduction of bone mineral density.

The ecological relevance for this is that Antarctic notothenioids don’t have swim bladders to adjust their buoyancy in water. Instead they use reductions in bone density to help them ‘float’ in the water column at low energetic cost.

Depiction of the loss of bone based on CT-scans

Basically, what is a genetic disease state in us is a means of survival in these fishes.

The genetic changes we found in these fishes are severely pathological in humans. They include genes in which mutations have been considered not compatible with life.

Finding that notothenioids use the same genetic pathways to achieve buoyancy in water represents a tremendous opportunity for human health research.

To test the function of the genetic changes identified, we used advances in gene editing to engineer genetically modified zebrafish embryos with the same mutations as Antarctic notothenioids. As these zebrafish grew, they displayed the same loss of bone as observed in the Antarctic species.

Genetically engineered zebrafish mirroring the loss of bone in notothenioids along the same genetic pathways as human bone disease.

Our research is revealing Antarctic notothenioids to be important models for human disease. In addition to low bone density, Antarctic fishes also have evolved other apparently pathological conditions, including the loss of kidney glomeruli and red blood cells.

These biomedically-relevant processes can be studied to reveal the genetic mechanisms behind these ‘disease’ states and their accommodation in these fishes. The results should lead to deeper understanding of how we might treat comparable disorders in humans.

The chronicle of notothenioid adaptive radiation


Rather than evolving these unusual adaptations in the face of major environmental upheaval, we found that much of this genetic variation was already in place before the Antarctic cooled. This finding challenges how we consider adaptation versus standing genetic diversity to predict the response of modern populations to contemporary climate change.

Chronicle of the Notothenioid adaptive radiation. Summary graphic from Longo 2019.

Antarctic notothenioids were basically in the right place at the right time to capitalize on the transition to an icy Antarctic millions of years ago. However, their future is uncertain.

As our team has stated before, notothenioids are of high ecological, economic and medical importance, however, many species can’t tolerate warming of more than a few degrees.

In an ironic twist of fate, forecasts of climate change now warn that this unique radiation of fishes could become decimated over the next century. It is up to us to prevent such a tragic loss.

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