De NovoGene Evolution of Antifreeze Glycoproteins in Codfishes Revealed by Whole Genome Sequence Data

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New genes can arise through duplication of a pre-existing gene orde novofrom non-coding DNA, providing raw material for evolution of new functions in response to a changing environment. A prime example is the independent evolution of antifreeze glycoprotein genes (afgps) in the Arctic codfishes and Antarctic notothenioids to prevent freezing. However, the highly repetitive nature of these genes complicates studies of their organization. In notothenioids,afgps evolved from an extant gene, yet the evolutionary origin ofafgps in codfishes is unknown. Here, we demonstrate thatafgps in codfishes have evolvedde novofrom non-coding DNA 13–18 Ma, coinciding with the cooling of the Northern Hemisphere. Using whole-genome sequence data from several codfishes and notothenioids, we find higher copy number ofafgpin species exposed to more severe freezing suggesting a gene dosage effect. Notably, antifreeze function is lost in one lineage of codfishes analogous to theafgplosses in non-Antarctic notothenioids. This indicates that selection can eliminate the antifreeze function when freezing is no longer imminent. In addition, we show that evolution ofafgp-assisting antifreeze potentiating protein genes (afpps) in notothenioids coincides with origin and lineage-specific losses ofafgp. The origin ofafgps in codfishes is one of the first examples of an essential gene born from non-coding DNA in a non-model species. Our study underlines the power of comparative genomics to uncover past molecular signatures of genome evolution, and further highlights the impact ofde novogene origin in response to a changing selection regime.

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