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

Abstract

White-blooded Antarctic icefishes 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 of C. esox, 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. Our study presents the first whole genome characterization of a secondarily temperate notothenioid to date, providing a key resource and platform for understanding the adaptive potential of the highly vulnerable icefishes, and of cryonotothenioids in general, in face of a warming Antarctic environment.

Novel mitochondrial genome rearrangements including duplications and extensive heteroplasmy could underlie temperature adaptations in Antarctic Notothenioid Fishes

“…For C. esox , a single male specimen obtained from the Patagonia water near Puerto Natales, Chile was sequenced using HMW DNA derived from isolated hepatocytes. Methods of DNA preparation, Pacific Biosciences continuous long read (PacBio CLR) library construction, and sequencing on PacBio Sequel II instruments (2 SMRT cells each) are detailed in Rivera-Colón, et al, (2022). Briefly, sequencing yielded 10.7 million raw reads for C. gunnari with a mean and N50 read length of 29.7 kbp and 29.8 respectively.…”

“…C. esox displays both higher mitochondrial densities (Johnston et al, 1998) and inner membrane morphology different from that of other icefishes (Johnston et al, 1998; O’Brien & Mueller, 2010). Positive selection has also been observed to act on several nuclear genes related to mitochondrial function and morphology when compared to its Antarctic sister species, Champsocephalus gunnari (Rivera-Colón et al, 2022). These patterns of selection, combined with the observed mitochondrial phenotypes, suggest that the organelle plays a fundamental role in the adaptation to warmer, temperate environments.…”

Transcriptomic analysis of the Brazilian blind characid, Stygichthys typhlops, reveals convergent selection with Astyanax mexicanus and other cavefishes

“…Another differentially expressed gene is cox5b, which encodes for a hypoxia-inducible isoform of COX subunit recently identified in the pike icefish Champsocephalus esox (Rivera-Colón et al, 2022). The absence of primary productivity decreases the oxygen content in caves and cave streams creating hypoxic conditions (Malard and Hervant, 1999;Boggs and Gross, 2021).…”

The law of the critical illness and its far-reaching implications

“…The phenomena that research is to model towards modifying the underlying pathology on the path to be forged by means of our results towards solving the problems that the far-reaching consequences of illness have hitherto constituted must therefore be those that underlie the absence, in white-blooded icefish (Channichthyidae), which possess neither hemoglobin nor RBC, of the worsening of clinical outcomes that are attributed to anemias, hemoglobinopathies or thalassemias. 28,29 While these white-blooded vertebrates have been assumed to have survived only because they inhabit highly oxygenated icy waters, 30 the existence of species that successfully inhabit temperate waters 31 demands a justifiable account on the path to the understanding required to model the phenomena underlying their recovery from illness despite the absence of hemoglobin or RBC. To achieve this understanding, we shall deduce the following consequence from the law of the critical illness.…”