Historical contingency shapes adaptive radiation in Antarctic fishes

Daane, Jacob M.; Dornburg, Alex; Smits, Patrick; MacGuigan, Daniel J.; Hawkins, M. Brent; Near, Thomas J.; Detrich, H. William; Harris, Matthew P.

doi:10.1038/s41559-019-0914-2

Cited by 54 publications

(65 citation statements)

References 67 publications

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“…georgianus (Fig 3A, S7 Fig). Consistent with our prior work, globin genes (hba and hbb) were also absent from most icefish species, with the exception of Neopagetopsis ionah, whose genome retained a pseudogenized version of the globins of the LA cluster ( Fig 3A) [8,10].…”

Section: Plos Geneticssupporting

confidence: 89%

“…Prior to and during the MMCT, regional sea surface temperature (SST) estimates and other oceanic temperature proxies [23][24][25][26][27][28] exceeded the critical thermal maxima (CT max ) of two extant icefish species [Chaenocephalus aceratus (13.9˚± 0.4˚C); Chionodraco rastrospinosus (13.3˚± 0.2˚C)] (S3 Fig), which are considered to be determined by the oxygen-carrying capacity of blood [29]. Therefore, evolution of the erythrocyte-null phenotype of Antarctic icefishes is tightly coupled, via physiology, to environmental cooling after the MMCT, in striking contrast to the increase in genetic diversity and positive selection for reduced skeletal density that evolved prior to the cryonotothenioid radiation [8].…”

Section: Drift In Anemia-associated Genetic Regions Followed the Declmentioning

confidence: 99%

“…Recent studies of the erythroid system in notothenioids have focused on the evolution of specific candidate genes, most notably the alpha-and beta-globin genes of the teleost globin clusters. These genes are almost completely deleted from the genomes of most icefishes [8][9][10], and globin regulatory elements are progressively deleted in the ancestral lineages leading to the icefishes [11]. Myoglobin expression is also absent from the hearts of 6 out of 16 icefish species, although mutated myoglobin genes remain in their genomes [12][13][14][15].…”

Section: Introductionmentioning

confidence: 99%

“…Part of this limitation has been the lack of the genome-wide data across cryonotothenioids necessary to establish a timeline of genomic changes supporting and potentially driving phenotypic adaptations. Recently, we published a dataset of ~250,000 loci representing protein-coding exons and conserved non-coding elements (CNEs) from 44 notothenioid species, including 10 icefishes and 6 dragonfishes ( S1 Fig ) [ 8 ]. The power of this phylogeny-wide genomic dataset lies in the ability to reconstruct the genetic steps that preceded, initiated, and follow trait evolution.…”

Section: Introductionmentioning

confidence: 99%

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

et al. 2020

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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.

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Section: Plos Geneticssupporting

confidence: 89%

Section: Drift In Anemia-associated Genetic Regions Followed the Declmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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

et al. 2020

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“…While our study did detect strong signals of accelerated evolution across whole chaperone promoters as well as instances of relaxed purifying selection or exaptation at conserved promoter elements in Cryonotothenioidei, it is clear these instances were more pervasive in diverging Antarctic lineages. This finding is interesting in relation to genome-wide evidence of heightened genomic diversification at the ancestral subpolar node of Cryonotothenioidei and Eleginops maclovinus , the closest sister species to cryonotothens and a species included in this study [73], which suggests that the successful radiation of Notothenioidei within the Southern Ocean may have been shaped more by historical contingency than adaptive evolution [74]. In the case of chaperone genes, we found a greater degree of evidence that adaptive evolution has shaped lineage-specific variation in chaperone cis- regulatory homology within Cryonotothenioidei lineages as opposed to subpolar nodes ancestral to Cryonotothenioidei.…”

Section: Discussionmentioning

confidence: 98%

Accelerated evolution at chaperone promoters among Antarctic notothenioid fishes

Bogan

Place

2019

BMC Evol Biol

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BackgroundAntarctic fishes of the Notothenioidei suborder constitutively upregulate multiple inducible chaperones, a highly derived adaptation that preserves proteostasis in extreme cold, and represent a system for studying the evolution of gene frontloading. We screened for Hsf1-binding sites, as Hsf1 is a master transcription factor of the heat shock response, and highly-conserved non-coding elements within proximal promoters of chaperone genes across 10 Antarctic notothens, 2 subpolar notothens, and 17 perciform fishes. We employed phylogenetic models of molecular evolution to determine whether (i) changes in motifs associated with Hsf1-binding and/or (ii) relaxed purifying selection or exaptation at ancestral cis-regulatory elements coincided with the evolution of chaperone frontloading in Antarctic notothens.ResultsAntarctic notothens exhibited significantly fewer Hsf1-binding sites per bp at chaperone promoters than subpolar notothens and Serranoidei, the most closely-related suborder to Notothenioidei included in this study. 90% of chaperone promoters exhibited accelerated substitution rates among Antarctic notothens relative to other perciformes. The proportion of bases undergoing accelerated evolution (i) was significantly greater in Antarctic notothens than in subpolar notothens and Perciformes in 70% of chaperone genes and (ii) increased among bases that were more conserved among perciformes. Lastly, we detected evidence of relaxed purifying selection and exaptation acting on ancestrally conserved cis-regulatory elements in the Antarctic notothen lineage and its major branches.ConclusionA large degree of turnover has occurred in Notothenioidei at chaperone promoter regions that are conserved among perciform fishes following adaptation to the cooling of the Southern Ocean. Additionally, derived reductions in Hsf1-binding site frequency suggest cis-regulatory modifications to the classical heat shock response. Of note, turnover events within chaperone promoters were less frequent in the ancestral node of Antarctic notothens relative to younger Antarctic lineages. This suggests that cis-regulatory divergence at chaperone promoters may be greater between Antarctic notothen lineages than between subpolar and Antarctic clades. These findings demonstrate that strong selective forces have acted upon cis-regulatory elements of chaperone genes among Antarctic notothens.

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A material‐based panspermia hypothesis: The potential of polymer gels and membraneless droplets

et al. 2022

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The Panspermia hypothesis posits that either life's building blocks (molecular Panspermia) or life itself (organism‐based Panspermia) may have been interplanetarily transferred to facilitate the origins of life (OoL) on a given planet, complementing several current OoL frameworks. Although many spaceflight experiments were performed in the past to test for potential terrestrial organisms as Panspermia seeds, it is uncertain whether such organisms will likely “seed” a new planet even if they are able to survive spaceflight. Therefore, rather than using organisms, using abiotic chemicals as seeds has been proposed as part of the molecular Panspermia hypothesis. Here, as an extension of this hypothesis, we introduce and review the plausibility of a polymeric material‐based Panspermia seed (M‐BPS) as a theoretical concept, where the type of polymeric material that can function as a M‐BPS must be able to: (1) survive spaceflight and (2) “function”, i.e., contingently drive chemical evolution toward some form of abiogenesis once arriving on a foreign planet. We use polymeric gels as a model example of a potential M‐BPS. Polymeric gels that can be prebiotically synthesized on one planet (such as polyester gels) could be transferred to another planet via meteoritic transfer, where upon landing on a liquid bearing planet, can assemble into structures containing cellular‐like characteristics and functionalities. Such features presupposed that these gels can assemble into compartments through phase separation to accomplish relevant functions such as encapsulation of primitive metabolic, genetic and catalytic materials, exchange of these materials, motion, coalescence, and evolution. All of these functions can result in the gels' capability to alter local geochemical niches on other planets, thereby allowing chemical evolution to lead to OoL events.

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Historical contingency shapes adaptive radiation in Antarctic fishes

Cited by 54 publications

References 67 publications

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

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

Accelerated evolution at chaperone promoters among Antarctic notothenioid fishes

A material‐based panspermia hypothesis: The potential of polymer gels and membraneless droplets

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