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Abstract Numerous 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, here we generate and analyse new genome assemblies for 24 species covering all major subgroups of the radiation, including five long-read assemblies. 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 the long-read 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. Both the haemoglobin and antifreeze genomic loci are characterised by multiple transposon expansions that may have driven the evolutionary history of these genes. 

Circulating miRNAs (c-miRNAs) are found in most, if not all, biological fluids and are becoming well-established non-invasive biomarkers of many human pathologies. However, their features in non-pathological contexts and whether their expression profiles reflect normal life history events have received little attention, especially in non-mammalian species. The aim of the present study was to investigate the potential of c-miRNAs to serve as biomarkers of reproductive and metabolic states in fish.

The blood plasma was sampled throughout the reproductive cycle of female rainbow trout subjected to two different feeding regimes that triggered contrasting metabolic states. In addition, ovarian fluid was sampled at ovulation, and all samples were subjected to small RNA-seq analysis, leading to the establishment of a comprehensive miRNA repertoire (i.e., miRNAome) and enabling subsequent comparative analyses to a panel of RNA-seq libraries from a wide variety of tissues and organs. We showed that biological fluid miRNAomes are complex and encompass a high proportion of the overall rainbow trout miRNAome. While sharing a high proportion of common miRNAs, the blood plasma and ovarian fluid miRNAomes exhibited strong fluid-specific signatures. We further revealed that the blood plasma miRNAome significantly changed depending on metabolic and reproductive states. We subsequently identified three evolutionarily conserved muscle-specific miRNAs or myomiRs (miR-1-1/2-3p, miR-133a-1/2-3p, and miR-206-3p) that accumulated in the blood plasma in response to high feeding rates, making these myomiRs strong candidate biomarkers of active myogenesis. We also identified miR-202-5p as a candidate biomarker for reproductive success that could be used to predict ovulation and/or egg quality.

Together, these promising results reveal the high potential of c-miRNAs, including evolutionarily conserved myomiRs, as physiologically relevant biomarker candidates and pave the way for the use of c-miRNAs for non-invasive phenotyping in various fish species.

 

Long‐read sequencing is driving a new reality for genome science in which highly contiguous assemblies can be produced efficiently with modest resources. Genome assemblies from long‐read sequences are particularly exciting for understanding the evolution of complex genomic regions that are often difficult to assemble. In this study, we utilized long‐read sequencing data to generate a high‐quality genome assembly for an Antarctic eelpout,Ophthalmolycus amberensis, the first for the globally distributed family Zoarcidae. We used this assembly to understand howO. amberensishas adapted to the harsh Southern Ocean and compared it to another group of Antarctic fishes: the notothenioids. We showed that selection has largely acted on different targets in eelpouts relative to notothenioids. However, we did find some overlap; in both groups, genes involved in membrane structure, thermal tolerance and vision have evidence of positive selection. We found evidence for historical shifts of transposable element activity inO. amberensisand other polar fishes, perhaps reflecting a response to environmental change. We were specifically interested in the evolution of two complex genomic loci known to underlie key adaptations to polar seas: haemoglobin and antifreeze proteins (AFPs). We observed unique evolution of the haemoglobin MN cluster in eelpouts and related fishes in the suborder Zoarcoidei relative to other Perciformes. For AFPs, we identified the first species in the suborder with no evidence ofafpIIIsequences (Cebidichthys violaceus) in the genomic region where they are found in all other Zoarcoidei, potentially reflecting a lineage‐specific loss of this cluster. Beyond polar fishes, our results highlight the power of long‐read sequencing to understand genome evolution.

 

Southern Ocean ecosystems are globally important and vulnerable to global drivers of change, yet they remain challenging to study. Fish and squid make up a significant portion of the biomass within the Southern Ocean, filling key roles in food webs from forage to mid-trophic species and top predators. They comprise a diverse array of species uniquely adapted to the extreme habitats of the region. Adaptations such as antifreeze glycoproteins, lipid-retention, extended larval phases, delayed senescence, and energy-conserving life strategies equip Antarctic fish and squid to withstand the dark winters and yearlong subzero temperatures experienced in much of the Southern Ocean. In addition to krill exploitation, the comparatively high commercial value of Antarctic fish, particularly the lucrative toothfish, drives fisheries interests, which has included illegal fishing. Uncertainty about the population dynamics of target species and ecosystem structure and function more broadly has necessitated a precautionary, ecosystem approach to managing these stocks and enabling the recovery of depleted species. Fisheries currently remain the major local driver of change in Southern Ocean fish productivity, but global climate change presents an even greater challenge to assessing future changes. Parts of the Southern Ocean are experiencing ocean-warming, such as the West Antarctic Peninsula, while other areas, such as the Ross Sea shelf, have undergone cooling in recent years. These trends are expected to result in a redistribution of species based on their tolerances to different temperature regimes. Climate variability may impair the migratory response of these species to environmental change, while imposing increased pressures on recruitment. Fisheries and climate change, coupled with related local and global drivers such as pollution and sea ice change, have the potential to produce synergistic impacts that compound the risks to Antarctic fish and squid species. The uncertainty surrounding how different species will respond to these challenges, given their varying life histories, environmental dependencies, and resiliencies, necessitates regular assessment to inform conservation and management decisions. Urgent attention is needed to determine whether the current management strategies are suitably precautionary to achieve conservation objectives in light of the impending changes to the ecosystem.