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

Autor: Daane, Jacob M., Auvinet, Juliette, Stoebenau, Alicia, Yergeau, Donald, Harris, Matthew P., Detrich III, H. William
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Zdroj: PLoS Genetics; 10/27/2020, Vol. 16 Issue 10, p1-22, 22p
Abstrakt: 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. Author summary: Our climate is rapidly changing. 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. In particular, we focus on the icefishes, which lost the ability to produce red blood cells in the frigid environment of the Southern Ocean. By integrating past climate records with a large genetic dataset of Antarctic fishes, we show that the loss of red blood cells occurred only after sustained cooling of the Southern Ocean. As cooling continued into the modern era, we discover that even some of the "red-blooded" relatives of the icefishes show early genetic and morphological signs of erythrocyte loss. This cooling event left a non-random imprint on the genome of icefishes. With few exceptions, the genetic toolkit underlying red cell development has remained intact in icefishes because many "erythroid" genes perform important functions in other tissues. Rather, mutations have accumulated in gene regulatory regions near genes that control terminal erythroid maturation, such that icefishes continue to produce red cell progenitors but not mature erythrocytes. These results show that the genetic constraints regulating embryonic development shaped the evolutionary response of this fish group to climate change. [ABSTRACT FROM AUTHOR]
Databáze: Complementary Index
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