Beneath the ice-covered waters of the Southern Ocean, a group of fish has pulled off one of the most remarkable evolutionary stories on Earth. Notothenioids, the dominant fish of the Antarctic shelf, survived dramatic cooling of the continent over tens of millions of years and diversified into more than a hundred species, many of them equipped with biological antifreeze. A new study published in Genome Biology has now taken one of the most detailed genomic looks yet at how this radiation unfolded, using a high-quality phased assembly of the Antarctic spiny plunderfish, Harpagifer antarcticus, as its reference point and comparing genomes across the entire clade.

The research team, led by Jacopo Martelossi of the Senckenberg Research Institute and Natural History Museum and Iliana Bista, with collaborators at the Wellcome Sanger Institute, the University of Cambridge, the University of Colorado School of Medicine and the British Antarctic Survey, built what is known as a phased assembly. This means the genome was reconstructed as two separate haplotypes, one inherited from each parent, rather than being collapsed into a single mixed sequence. The approach allowed the researchers to examine haplotypic variability across the genome of H. antarcticus and revealed surprisingly low levels of variation between the two chromosome sets, a finding that speaks to the genetic history of this cold-adapted species.

Yet low haplotype diversity did not mean a quiet genome. The assembly was riddled with insertions from multiple clades of LINE-L2 elements, a family of retrotransposons that copy and paste themselves through the genome via an RNA intermediate. The abundance of these elements from several distinct lineages suggests that transposition is ongoing in the plunderfish genome, and the authors argue that this relentless activity may have contributed to speciation within the group. Transposable elements are increasingly recognised as engines of genome evolution, capable of shuffling regulatory sequences, creating new genes and driving chromosomal rearrangements, and the notothenioid genome now appears to be a prime example of this dynamic at work.

One of the most celebrated adaptations in Antarctic fish is the antifreeze glycoprotein, or afgp, which binds to ice crystals and prevents them from growing inside blood and body fluids. The new phased assembly offered an unusually clear view of the afgp locus, and the results overturned expectations. The two haplotypes turned out to be highly similar at this locus, with the exception of large length variants in the afgp genes themselves. Based on the structural patterns observed, the researchers propose a model in which the afgp locus expanded in H. antarcticus through segmental tandem duplications, with two pairs of afgp genes duplicated at a time. This stepwise copy-and-paste mechanism provides a concrete picture of how one of the most iconic innovations in polar biology was amplified in the genome.

Beyond the plunderfish, the team carried out syntenic reconstructions, aligning genomes from species across the notothenioid clade to trace how chromosomes have been rearranged over evolutionary time. The analysis demonstrated conserved macrosyntenic relationships, meaning large blocks of genes have remained together on chromosomes across tens of millions of years, but it also revealed group-specific chromosomal fusions, structural events in which entire chromosomes merged. These fusions may have played a role in reproductive isolation and the diversification of the flock, since changes in chromosome structure can reduce the fertility of hybrids and push populations onto separate evolutionary paths.

Perhaps the most striking result concerns the tempo of genome change itself. By quantifying genome gain and transposition rates during cryonotothenioid diversification, the researchers identified two distinct phases. First, an ancestral period of slow genome expansion occurred concurrently with historic drops in ocean temperature, as Antarctica froze over and the Southern Ocean became one of the coldest marine environments on the planet. Then, as individual lineages branched off and adapted to their own niches, the record shows massive lineage-specific peaks of genomic gain and transposition activity. The pattern suggests that bursts of mobile element activity and DNA acquisition were not evenly spread through time but concentrated at key moments of evolutionary innovation.

The study also searched for signatures of selection and regulatory novelty. The team identified a set of genes that underwent diversifying selection in the ancestor of the cryonotothenioids and simultaneously acquired novel conserved non-coding elements, stretches of DNA that likely act as regulatory switches controlling when and where genes are expressed. Remarkably, these genes were related to antioxidant activity and proteostasis, the cellular machinery that maintains protein folding and clears damaged proteins. Both processes are critical under extreme cold, where low temperatures slow biochemical reactions, increase the production of reactive oxygen species and make protein misfolding a constant hazard.

Taken together, the findings paint a coherent picture of how the notothenioid radiation was fuelled. Diversifying selection acting on key physiological genes, combined with genomic gain driven by transposon activity, emerges as the primary contributor to the lineage-specific evolutionary dynamics that allowed these fish to colonise and diversify in the Antarctic. Rather than a single master mutation, cold adaptation appears to have been built from many layers: duplicated antifreeze genes, reshuffled chromosomes, waves of mobile elements and new regulatory elements tuning the expression of stress-response genes.

The work also demonstrates the power of modern phased genome assemblies for evolutionary biology. Because the two haplotypes are reconstructed separately, researchers can detect structural variants, measure allelic differences and trace the history of gene families with far greater precision than with collapsed assemblies. Applied to a species flock as ecologically significant as the notothenioids, this approach turns a single fish genome into a time machine, revealing not just what the animal is but how its lineage came to be.

As the Southern Ocean warms and Antarctic ecosystems face unprecedented change, understanding the genomic foundations of cold adaptation has taken on new urgency. The spiny plunderfish assembly, generated with support from the Wellcome Sanger Institute DNA pipelines and samples collected by the Rothera Marine Team under Antarctic Treaty permits, now provides a reference framework for future studies of how polar fish genomes respond to environmental extremes, and how they may cope as those extremes begin to shift.

Subject of Research: Genomic evolution and cold adaptation in Antarctic notothenioid fish

Article Title: A new phased assembly of the Antarctic spiny plunderfish provides novel insights into the evolution of the notothenioid radiation

Article References: A new phased assembly of the Antarctic spiny plunderfish provides novel insights into the evolution of the notothenioid radiation. (n.d.). https://doi.org/10.1186/s13059-026-04293-7

Image Credits: AI Generated

DOI: 10.1186/s13059-026-04293-7

Keywords: notothenioids, Antarctic fish, genome assembly, transposons, antifreeze glycoprotein, cold adaptation, LINE-L2, genome evolution, diversifying selection, proteostasis, haplotype, spiny plunderfish