Abstract
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.
Highlights
The cooling of the Southern Ocean (SO) beginning 35 million years ago (Ma) had a profound impact on the evolution of Antarctic fishes [1]
To better understand how species can adapt to major climate disturbance, we looked back into the past at a group of fishes that have encountered dramatic climate upheavals and thrived: Antarctic notothenioid fishes
To track patterns of genome evolution associated with environmental change, we integrated paleoclimate data with a time-calibrated phylogeny of notothenioids
Summary
The cooling of the Southern Ocean (SO) beginning 35 million years ago (Ma) had a profound impact on the evolution of Antarctic fishes [1]. The stable, freezing temperatures, strong currents, and frequent storms created an environment in which dissolved oxygen was abundant and well mixed throughout the water column. In this unique environment, a single clade of Antarctic fishes, the icefishes (Notothenioidei: Cryonotothenioidea: Channichthyidae), lost the capacity to produce erythrocytes and the oxygen-transport protein hemoglobin (Hb)–and yet they thrive in the SO. Whereas the loss of erythrocytes among vertebrates is unique to icefishes, many closely related, but red-blooded, cryonotothenioid species cohabit the SO. Erythrocytes and hemoglobin appear to be dispensable in red-blooded notothenioid lineages, which suggests an inherent resiliency within cryonotothenioids to accommodate extreme anemia
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