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

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.

Novel regulators of growth identified in the evolution of fin proportion in flying fish

“…In parallel to advances in whole genome sequencing, targeted sequencing studies have effectively and efficiently probed both patterns of genome evolution and have identified developmental regulation underlying trait evolution [9,10,50]. The majority of comparative genomic studies asking questions over large evolutionary distances of many millions of years tend to focus on highly conserved protein coding sequences and non-coding elements due to the lack of clear homology and/or obvious functional roles for large swaths of the genome.…”

“…Many CNEs function as tissue specific enhancers and promoters. As in Daane et al [50], we used the Genomic Regions Enrichment of Annotations Tool ('GREAT') approach to assign CNEs to neighboring genes as putative regulatory targets [29]. This approach defines a basal regulatory window that is 5kb downstream and 1kb upstream of each gene's transcription start site (TSS).…”

Positive and relaxed selective pressures have both strongly influenced the evolution of cryonotothenioid fishes during their radiation in the freezing Southern Ocean

“…Studies by Daane and colleagues (2020; 2019) have since investigated the genetic mechanisms that enable or constrain evolutionary change in the cryonotothenioids during their radiation in the Southern Ocean. Using the evolution of buoyancy adaptation among several Antarctic lineages (Eastman, 2020) as a model to explore the origins of novel traits in the cryonotothenioids, this was found to result from bone demineralization associated with developmental alterations similar to human skeletal dysplasia (Beck et al, 2021).…”

Refining Convergent Rate Analysis with Topology in Mammalian Longevity and Marine Transitions

“…These accelerations and constraints of change on a locus can be powerfully informative as to the selective pressures acting on it (Echave et al, 2016; Pollard et al, 2006). Importantly, such rate analyses can scale in scope, from single positions, to genes, or even discontiguous loci comprising entire pathways (Daane et al, 2020). This contrasts with analyses that quantify a specific measure, like gene loss, expansion, or the detection of identical amino acid substitutions.…”