Genomics of cold adaptations in the Antarctic notothenioid fish radiation

• DOI: 10.1101/2022.06.08.494096
• Publication Date: 2022-06-10T03:55:10Z
• Authors: Iliana Bista; Jonathan M. D. Wood; Thomas Desvignes; Shane A. McCarthy; Michael Matschiner; Zemin Ning; Alan Tracey; James Torrance; Ying Sims; William Chow; Michelle Smith; Karen Oliver; Leanne Haggerty; Walter Salzburger; John H. Postlethwait; Kerstin Howe; Melody S. Clark; William H. Detrich; C.-H. Christina C...; Eric A. Miska; Richard Durbin
• Keywords: 0303 health sciences; Science; Q; Fishes; Antarctic Regions; Genomics; genome evolution; Article; Perciformes; Hemoglobins; 03 medical and health sciences; cold adaptation; Vertebrates; genomics; Animals; 14. Life underwater; transposable elements; notothenioids; Phylogeny

AbstractNumerous novel adaptations characterise the radiation of notothenioids, the dominant fish group in the freezing seas of the Southern Ocean. To improve understanding of the evolution of this iconic fish group, we generated and analysed new genome assemblies for 24 species covering all major subgroups of the radiation. We present a new estimate for the onset of the radiation at 10.7 million years ago, based on a time-calibrated phylogeny derived from genome-wide sequence data. We identify a two-fold variation in genome size, driven by expansion of multiple transposable element families, and use long-read sequencing data to reconstruct two evolutionarily important, highly repetitive gene family loci. First, we present the most complete reconstruction to date of the antifreeze glycoprotein gene family, whose emergence enabled survival in sub-zero temperatures, showing the expansion of the antifreeze gene locus from the ancestral to the derived state. Second, we trace the loss of haemoglobin genes in icefishes, the only vertebrates lacking functional haemoglobins, through complete reconstruction of the two haemoglobin gene clusters across notothenioid families. Finally, we show that both the haemoglobin and antifreeze genomic loci are characterised by multiple transposon expansions that may have driven the evolutionary history of these genes.