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1. Cold-Driven Hemoglobin Evolution in Antarctic Notothenioid Fishes Prior to Hemoglobin Gene Loss in White-Blooded Icefishes

   https://doi.org/10.1093/molbev/msad236  

   Desvignes, Thomas; Bista, Iliana; Herrera, Karina; Landes, Audrey; Postlethwait, John H (November 2023, Molecular Biology and Evolution)

   Yang, Guang (Ed.)

   Abstract Expression of multiple hemoglobin isoforms with differing physiochemical properties likely helps species adapt to different environmental and physiological conditions. Antarctic notothenioid fishes inhabit the icy Southern Ocean and display fewer hemoglobin isoforms, each with less affinity for oxygen than temperate relatives. Reduced hemoglobin multiplicity was proposed to result from relaxed selective pressure in the cold, thermally stable, and highly oxygenated Antarctic waters. These conditions also permitted the survival and diversification of white-blooded icefishes, the only vertebrates living without hemoglobin. To understand hemoglobin evolution during adaptation to freezing water, we analyzed hemoglobin genes from 36 notothenioid genome assemblies. Results showed that adaptation to frigid conditions shaped hemoglobin gene evolution by episodic diversifying selection concomitant with cold adaptation and by pervasive evolution in Antarctic notothenioids compared to temperate relatives, likely a continuing adaptation to Antarctic conditions. Analysis of hemoglobin gene expression in adult hematopoietic organs in various temperate and Antarctic species further revealed a switch in hemoglobin gene expression underlying hemoglobin multiplicity reduction in Antarctic fish, leading to a single hemoglobin isoform in adult plunderfishes and dragonfishes, the sister groups to icefishes. The predicted high hemoglobin multiplicity in Antarctic fish embryos based on transcriptomic data, however, raises questions about the molecular bases and physiological implications of diverse hemoglobin isoforms in embryos compared to adults. This analysis supports the hypothesis that the last common icefish ancestor was vulnerable to detrimental mutations affecting the single ancestral expressed alpha- and beta-globin gene pair, potentially predisposing their subsequent loss. 

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2. Museomic analyses clarify species diversity in the icefish genus Channichthys

   https://doi.org/10.1007/s00300-025-03349-x  

   Garmann-Aarhus, Benedicte; Nikolaeva, Ekaterina; Desvignes, Thomas; Straube, Nicolas; Matschiner, Michael (January 2025, Polar Biology)

   Abstract The rapid diversification of notothenioid fishes in Antarctic waters is a prime example of the process of adaptive radiation. Within around 10 million years, Antarctic notothenioids have diversified into over 100 species with a broad range of lifestyles and ecological adaptations. However, the exact number of species within this radiation has long been unclear. Particularly challenging is the taxonomy of the genusChannichthys, for which between one and nine species have been recognized by different authors. The putative species of this genus are known from a limited number of specimens, of which most were sampled decades ago. Here, we investigated the mitochondrial genomes of museum specimens representing the four species Unicorn Icefish (C. rhinoceratus), Red Icefish (C. rugosus), Sailfish Pike (C. velifer), and Charcoal Icefish (C. panticapaei), complemented by morphological analyses. All analyzed specimens were collected in the 1960s and 1970s and fixed in formaldehyde, and their DNA has been heavily degraded. Applying ancient-DNA protocols for DNA extraction and single-stranded library preparation, we were able to obtain sufficient endogenous DNA to reconstruct the mitochondrial genomes of one specimen per species. These mitochondrial genome sequences were nearly identical for the three specimens assigned to Unicorn Icefish, Red Icefish, and Sailfish Pike, while greater divergence was observed for the Charcoal Icefish specimens. We discuss possible explanations of the contrast between these molecular results and the recognizable morphological variation found among the four species, and recommend that at least the Charcoal Icefish be included in the list of valid notothenioid species. 

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3. Bone microstructure and bone mineral density are not systemically different in Antarctic icefishes and related Antarctic notothenioids

   https://doi.org/10.1111/joa.13537  

   Ashique, Amir M.; Atake, Oghenevwogaga J.; Ovens, Katie; Guo, Ruiyi; Pratt, Isaac V.; Detrich, III, H. William; Cooper, David M. L.; Desvignes, Thomas; Postlethwait, John H.; Eames, B. Frank (August 2021, Journal of Anatomy)

   Abstract Ancestors of the Antarctic icefishes (family Channichthyidae) were benthic and had no swim bladder, making it energetically expensive to rise from the ocean floor. To exploit the water column, benthopelagic icefishes were hypothesized to have evolved a skeleton with “reduced bone,” which gross anatomical data supported. Here, we tested the hypothesis that changes to icefish bones also occurred below the level of gross anatomy. Histology and micro‐CT imaging of representative craniofacial bones (i.e., ceratohyal, frontal, dentary, and articular) of extant Antarctic fish species specifically evaluated two features that might cause the appearance of “reduced bone”: bone microstructure (e.g., bone volume fraction and structure linear density) and bone mineral density (BMD, or mass of mineral per volume of bone). Measures of bone microstructure were not consistently different in bones from the icefishesChaenocephalus aceratusandChampsocephalus gunnari, compared to the related benthic notothenioidsNotothenia coriicepsandGobionotothen gibberifrons. Some quantitative measures, such as bone volume fraction and structure linear density, were significantly increased in some icefish bones compared to homologous bones of non‐icefish. However, such differences were rare, and no microstructural measures were consistently different in icefishes across all bones and species analyzed. Furthermore, BMD was similar among homologous bones of icefish and non‐icefish Antarctic notothenioids. In summary, “reduced bone” in icefishes was not due to systemic changes in bone microstructure or BMD, raising the prospect that “reduced bone” in icefish occurs only at the gross anatomic level (i.e., smaller or fewer bones). Given that icefishes exhibit delayed skeletal development compared to non‐icefish Antarctic fishes, combining these phenotypic data with genomic data might clarify genetic changes driving skeletal heterochrony. 

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4. Novel mitochondrial genome rearrangements including duplications and extensive heteroplasmy could underlie temperature adaptations in Antarctic notothenioid fishes

   https://doi.org/10.1038/s41598-023-34237-1  

   Minhas, Bushra Fazal; Beck, Emily A.; Cheng, C.-H. Christina; Catchen, Julian (December 2023, Scientific Reports)

   Abstract Mitochondrial genomes are known for their compact size and conserved gene order, however, recent studies employing long-read sequencing technologies have revealed the presence of atypical mitogenomes in some species. In this study, we assembled and annotated the mitogenomes of five Antarctic notothenioids, including four icefishes (Champsocephalus gunnari,C. esox,Chaenocephalus aceratus, andPseudochaenichthys georgianus) and the cold-specializedTrematomus borchgrevinki. Antarctic notothenioids are known to harbor some rearrangements in their mt genomes, however the extensive duplications in icefishes observed in our study have never been reported before. In the icefishes, we observed duplications of the protein coding geneND6, two transfer RNAs,and the control region with different copy number variants present within the same individuals and with someND6duplications appearing to follow the canonical Duplication-Degeneration-Complementation (DDC) model inC. esoxandC. gunnari. In addition, using long-read sequencing and k-mer analysis, we were able to detect extensive heteroplasmy inC. aceratusandC. esox. We also observed a large inversion in the mitogenome ofT. borchgrevinki, along with the presence of tandem repeats in its control region. This study is the first in using long-read sequencing to assemble and identify structural variants and heteroplasmy in notothenioid mitogenomes and signifies the importance of long-reads in resolving complex mitochondrial architectures. Identification of such wide-ranging structural variants in the mitogenomes of these fishes could provide insight into the genetic basis of the atypical icefish mitochondrial physiology and more generally may provide insights about their potential role in cold adaptation. 

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5. Developmental constraint shaped genome evolution and erythrocyte loss in Antarctic fishes following paleoclimate change

   https://doi.org/10.1371/journal.pgen.1009173  

   Daane, Jacob M.; Auvinet, Juliette; Stoebenau, Alicia; Yergeau, Donald; Harris, Matthew P.; Detrich, H. William (October 2020, PLOS Genetics)

   Mullins, Mary C. (Ed.)

   In the frigid, oxygen-rich Southern Ocean (SO), Antarctic icefishes (Channichthyidae; Notothenioidei) evolved the ability to survive without producing erythrocytes and hemoglobin, the oxygen-transport system of virtually all vertebrates. Here, we integrate paleoclimate records with an extensive phylogenomic dataset of notothenioid fishes to understand the evolution of trait loss associated with climate change. In contrast to buoyancy adaptations in this clade, we find relaxed selection on the genetic regions controlling erythropoiesis evolved only after sustained cooling in the SO. This pattern is seen not only within icefishes but also occurred independently in other high-latitude notothenioids. We show that one species of the red-blooded dragonfish clade evolved a spherocytic anemia that phenocopies human patients with this disease via orthologous mutations. The genomic imprint of SO climate change is biased toward erythrocyte-associated conserved noncoding elements (CNEs) rather than to coding regions, which are largely preserved through pleiotropy. The drift in CNEs is specifically enriched near genes that are preferentially expressed late in erythropoiesis. Furthermore, we find that the hematopoietic marrow of icefish species retained proerythroblasts, which indicates that early erythroid development remains intact. Our results provide a framework for understanding the interactions between development and the genome in shaping the response of species to climate change. 

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