Genomics of Secondarily Temperate Adaptation in the Only Non-Antarctic Icefish

Abstract

White-blooded Antarctic icefishes, a family within the adaptive radiation of Antarctic notothenioid fishes, are an example of extreme biological specialization to both the chronic cold of the Southern Ocean and life without hemoglobin. As a result, icefishes display derived physiology that limits them to the cold and highly oxygenated Antarctic waters. Against these constraints, remarkably one species, the pike icefish Champsocephalus esox, successfully colonized temperate South American waters. To study the genetic mechanisms underlying secondarily temperate adaptation in icefishes, we generated chromosome-level genome assemblies of both C. esox and its Antarctic sister species, Champsocephalus gunnari. The C. esox genome is similar in structure and organization to that of its Antarctic congener; however, we observe evidence of chromosomal rearrangements coinciding with regions of elevated genetic divergence in pike icefish populations. We also find several key biological pathways under selection, including genes related to mitochondria and vision, highlighting candidates behind temperate adaptation in C. esox. Substantial antifreeze glycoprotein (AFGP) pseudogenization has occurred in the pike icefish, likely due to relaxed selection following ancestral escape from Antarctica. The canonical AFGP locus organization is conserved in C. esox and C. gunnari, but both show a translocation of two AFGP copies to a separate locus, previously unobserved in cryonotothenioids. Altogether, the study of this secondarily temperate species provides an insight into the mechanisms underlying adaptation to ecologically disparate environments in this otherwise highly specialized group.

Chromosome-Level Genome Assembly and Circadian Gene Repertoire of the Patagonia blennieEleginops maclovinus- the closest ancestral proxy of Antarctic cryonotothenioids

“…A total of 25 thousand protein-coding genes were annotated using a combined proteome-and transcriptome-based annotation. This number is comparable with the 20-30 thousand protein-coding genes described in other notothenioid assemblies [21,22,49], and the 23 thousand genes annotated for the Illumina short-read assembly [20]. With regard to repeat content, this assembly is composed of 33.2% repetitive sequences, characterized from a de novo repeat library.…”

“…Additional manual inspection and curation of this scaffolding process was done using a conserved synteny analysis (methods described below), e.g., verifying that structural variants were not limited to the boundaries of a contig/scaffold, or that the large-scale organization of the chromosomes was supported by patterns of within-species synteny. Any manual changes made to the assembly were propagated to the corresponding structure (AGP), annotation (GTF), and sequence files (FASTA) using a custom Python program, as described in [22].…”

“…Champsocephalus esox and Champsocephalus gunnari [22], Chaenocephalus aceratus (NCBI GCA_023974075.1), and Pseudochaenichthys georgianus [21]). To run SYNOLOG, we first reciprocally matched the annotated gene models for all species using the blastp algorithm in BLAST+ v2.4.0 [44].…”

“…Thus added to the historical interest of how cryonotothenioids evolved cold adaptation and specialization to dominate the SO fish fauna, are pressing questions regarding whether their derived polar character harbors sufficient plasticity and adaptive potential to survive the changing contemporary SO environment. To this end, the fast trajectory of generating high quality genome assemblies of species across Notothenioidei promises to be an accelerator in our ability to address a wide range of important questions, including variations in genetic diversity, mutation rates, transposable element mobilization [12,20,21], genome structures [22], protein genes experiencing positive or relaxed selective pressures [23], and historical and extant demography (by whole genome resequencing of populations) shaped by Antarctic glacial cycles [24], among others, that would inform on the degree of resilience of the cryonotothenioids under climate change scenarios. Seventeen draft genomes of notothenioids with various degree of completeness have been published since 2014.…”

“…The Patagonia blennie (locally known as róbalo), E. maclovinus, the monotypic species of the family Eleginopidae, long recognized as the taxonomic and phylogenetic direct sister species of the Antarctic clade would serve as the most fitting closest ancestral state for evaluating trait changes and reconfigurations shaped by Southern Ocean selective pressures during cryonotothenioid evolution. A few studies have utilized E. maclovinus as the ancestral reference, namely the nature of the native chaperome [26], loss of the classical heat shock response [15], proliferation of transposable elements and a number of developmental traits during cold adaptation [20], and the state of the AFGP orthologous genomic region prior to the emergence of the AFGP genotype [22]. Apart from these more visible traits, there are expectedly myriad subtler trait changes across the genetic blueprint, requiring a well assembled and gene-complete genome to decode.…”