Adaptations and Diversity of Antarctic Fishes: A Genomic Perspective

Antarctic notothenioid fishes are the classic example of vertebrate adaptive radiation in a marine environment. Notothenioids diversified from a single common ancestor ∼25 Mya to more than 140 species today, and they represent ∼90% of fish biomass on the continental shelf of Antarctica. As they diversified in the cold Southern Ocean, notothenioids evolved numerous traits, including osteopenia, anemia, cardiomegaly, dyslipidemia, and aglomerular kidneys, that are beneficial or tolerated in their environment but are pathological in humans. Thus, notothenioids are models for understanding adaptive radiations, physiological and biochemical adaptations to extreme environments, and genetic mechanisms of human disease. Since 2014, 16 notothenioid genomes have been published, which enable a first-pass holistic analysis of the notothenioid radiation and the genetic underpinnings of novel notothenioid traits. Here, we review the notothenioid radiation from a genomic perspective and integrate our insights with recent observations from other fish radiations. Expected final online publication date for the Annual Review of Animal Biosciences, Volume 10 is February 2022. Please see http://www.annualreviews.org/page/journal/pubdates for revised estimates.

Warming, not CO2-acidified seawater, alters otolith development of juvenile Antarctic emerald rockcod (Trematomus bernacchii)

The combustion of fossil fuels is currently causing rapid rates of ocean warming and acidification worldwide. Projected changes in these parameters have been repeatedly observed to stress the physiological limits and plasticity of many marine species from the molecular to organismal levels. High latitude oceans are among the fastest changing ecosystems; therefore, polar species are projected to be some of the most vulnerable to climate change. Antarctic species are particularly sensitive to environmental change, having evolved for millions of years under stable ocean conditions. Otoliths, calcified structures found in a fish’s inner ear used to sense movement and direction, have been shown to be affected by both warming and CO2-acidified seawater in temperate and tropical fishes but there is no work to date on Antarctic fishes. In this study, juvenile emerald rockcod (Trematomus bernacchii) were exposed to projected seawater warming and CO2-acidification for the year 2100 over 28 days. Sagittal otoliths were analyzed for changes in area, perimeter, length, width and shape. We found ocean warming increased the growth rate of otoliths, while CO2-acidified seawater and the interaction of warming and acidification did not have an effect on otolith development. Elevated temperature also altered the shape of otoliths. If otolith development is altered under future warming scenarios, sensory functions such as hearing, orientation, and movement may potentially be impaired. Changes in these basic somatic abilities could have broad implications for the general capabilities and ecology of early life stages of Antarctic fishes.

Fitting Together the Evolutionary Puzzle pieces of the Immunoglobulin T Gene from Antarctic Fishes

Cryonotothenioidea is the main group of fishes that thrive in the extremely cold Antarctic environment, thanks to the acquisition of peculiar morphological, physiological and molecular adaptations. We have previously disclosed that IgM, the main immunoglobulin isotype in teleosts, display typical cold-adapted features. Recently, we have analyzed the gene encoding the heavy chain constant region (CH) of the IgT isotype from the Antarctic teleost Trematomus bernacchii (family Nototheniidae), characterized by the near-complete deletion of the CH2 domain. Here, we aimed to track the loss of the CH2 domain along notothenioid phylogeny and to identify its ancestral origins. To this end, we obtained the IgT gene sequences from several species belonging to the Antarctic families Nototheniidae, Bathydraconidae and Artedidraconidae. All species display a CH2 remnant of variable size, encoded by a short Cτ2 exon, which retains functional splicing sites and therefore is included in the mature transcript. We also considered representative species from the three non-Antarctic families: Eleginopsioidea (Eleginops maclovinus), Pseudaphritioidea (Pseudaphritis urvillii) and Bovichtidae (Bovichtus diacanthus and Cottoperca gobio). Even though only E. maclovinus, the sister taxa of Cryonotothenioidea, shared the partial loss of Cτ2, the other non-Antarctic notothenioid species displayed early molecular signatures of this event. These results shed light on the evolutionary path that underlies the origins of this remarkable gene structural modification.

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

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.

Understanding the Metabolic Capacity of Antarctic Fishes to Acclimate to Future Ocean Conditions

Synopsis Antarctic fishes have evolved under stable, extreme cold temperatures for millions of years. Adapted to thrive in the cold environment, their specialized phenotypes will likely render them particularly susceptible to future ocean warming and acidification as a result of climate change. Moving from a period of stability to one of environmental change, species persistence will depend on maintaining energetic equilibrium, or sustaining the increased energy demand without compromising important biological functions such as growth and reproduction. Metabolic capacity to acclimate, marked by a return to metabolic equilibrium through physiological compensation of routine metabolic rate (RMR), will likely determine which species will be better poised to cope with shifts in environmental conditions. Focusing on the suborder Notothenioidei, a dominant group of Antarctic fishes, and in particular four well-studied species, Trematomus bernacchii, Pagothenia borchgrevinki, Notothenia rossii, and N. coriiceps, we discuss metabolic acclimation potential to warming and CO2-acidification using an integrative and comparative framework. There are species-specific differences in the physiological compensation of RMR during warming and the duration of acclimation time required to achieve compensation; for some species, RMR fully recovered within 3.5 weeks of exposure, such as P. borchgrevinki, while for other species, such as N. coriiceps, RMR remained significantly elevated past 9 weeks of exposure. In all instances, added exposure to increased PCO2, further compromised the ability of species to return RMR to pre-exposure levels. The period of metabolic imbalance, marked by elevated RMR, was underlined by energetic disturbance and elevated energetic costs, which shifted energy away from fitness-related functions, such as growth. In T. bernacchii and N. coriiceps, long duration of elevated RMR impacted condition factor and/or growth rate. Low growth rate can affect development and ultimately the timing of reproduction, severely compromising the species’ survival potential and the biodiversity of the notothenioid lineage. Therefore, the ability to achieve full compensation of RMR, and in a short-time frame, in order to avoid long term consequences of metabolic imbalance, will likely be an important determinant in a species’ capacity to persist in a changing environment. Much work is still required to develop our understanding of the bioenergetics of Antarctic fishes in the face of environmental change, and a targeted approach of nesting a mechanistic focus in an ecological and comparative framework will better aid our predictions on the effect of global climate change on species persistence in the polar regions.