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Abstract Rising ocean temperatures pose significant threats to marine ectotherms. Sensitivity to temperature change varies across life stages, with embryos often being less tolerant to thermal perturbation than adults. Antarctic notothenioid fishes evolved to occupy a narrow, cold thermal regime (−2 to +2°C) as the high-latitude Southern Ocean (SO) cooled to its present icy temperatures, and they are particularly vulnerable to small temperature changes, which makes them ideal sentinel species for assessing climate change impacts. Here, we detail how predicted warming of the SO may affect embryonic development in the Antarctic bullhead notothen,Notothenia coriiceps. Experimental embryos were incubated at +4°C, a temperature projected for the high-latitude SO within the next 100–200 years under high emission climate models, whereas control embryos were incubated at present-day ambient temperature, ∼0°C. Elevated temperature caused a high incidence of embryonic morphological abnormalities, including body axis kinking/curvature and reduced body size. Experimental embryos also developed more rapidly, such that they hatched 68 days earlier than controls (87 vs. 155 days post-fertilization). Accelerated development disrupted the evolved timing of seasonal hatching, shifting larval emergence into the polar winter when food availability is scarce. Transcriptomic analyses revealed molecular signatures of hypoxia and disrupted protein-folding in near-hatching embryos, indicative of severe cellular stress. Predictive modeling suggested that temperature-induced developmental disruptions would narrow seasonal reproductive windows, thereby threatening population viability under future climate scenarios. Together, our findings underscore the vulnerability of Antarctic fish embryos to higher water temperature and highlight the urgent need to understand the consequences of disruption of this important trophic component on ecosystem stability in the SO. Significance StatementAntarctic fishes evolved cold-adapted phenotypes suited to the stable thermal conditions of the Southern Ocean, yet are threatened by rising temperatures. The impact of rising temperatures on early life stages in Antarctic fishes is not well understood; our findings show that projected warming may induce premature hatching, developmental abnormalities, and molecular stress responses in embryos, potentially reducing recruitment and leading to population instability and trophic-level ecosystem disruptions. These results underscore the urgency of assessing climate-driven vulnerabilities across life stages of Antarctic marine organisms to refine population projections and enhance conservation strategies amid ongoing environmental change. 

Abstract Antifreeze proteins (AFPs) have enabled teleost fishes to repeatedly colonize polar seas. Four AFP types have convergently evolved in several fish lineages. AFPs inhibit ice crystal growth and lower tissue freezing point. In lineages with AFPs, species inhabiting colder environments may possess more AFP copies. Elucidating how differences in AFP copy number evolve is challenging due to the genes’ tandem array structure and consequently poor resolution of these repetitive regions. Here, we explore the evolution of type III AFPs (AFP III) in the globally distributed suborder Zoarcoidei, leveraging six new long-read genome assemblies. Zoarcoidei has fewer genomic resources relative to other polar fish clades while it is one of the few groups of fishes adapted to both the Arctic and Southern Oceans. Combining these new assemblies with additional long-read genomes available for Zoarcoidei, we conducted a comprehensive phylogenetic test of AFP III evolution and modeled the effects of thermal habitat and depth on AFP III gene family evolution. We confirm a single origin of AFP III via neofunctionalization of the enzyme sialic acid synthase B. We also show that AFP copy number increased under low temperature but decreased with depth, potentially because pressure lowers freezing point. Associations between the environment and AFP III copy number were driven by duplications of paralogs that were translocated out of the ancestral locus at which AFP III arose. Our results reveal novel environmental effects on AFP evolution and demonstrate the value of high-quality genomic resources for studying how structural genomic variation shapes convergent adaptation.