Julia M. York

Having evolved in the chronically cold and thermally stable waters of the Southern Ocean (SO) for millions of years, Antarctic fish possess a suite of physiological specializations that enable them to survive at temperatures near the freezing point of seawater. Adaptations include the evolution of antifreeze proteins, modifications of membrane composition, altered metabolic processes, unique mechanisms of oxygen transport and utilization, and distinctive cellular stress responses. This review synthesizes current knowledge of the physiological adaptations of Antarctic fish, focusing on the mechanisms that support survival in extreme cold environments. We examine adaptations related to cold tolerance, osmoregulation, metabolism, reproduction, sensory biology and oxygen transport and discuss the evolutionary processes that have shaped these traits. We further evaluate how ongoing climate‐driven changes, including ocean warming, acidification and biological invasions, may affect Antarctic fish populations and ecosystems. Understanding the physiological foundations underlying Antarctic fish adaptation provides important insights into evolutionary responses to environmental extremes and provides a framework for predicting potential vulnerabilities of polar marine organisms in a rapidly changing world.

Climate change is threatening global biodiversity as a result of increasing temperature and climate variability outpacing adaptation rates. Ectothermic animals, such as most fishes, are particularly vulnerable to environmental change because their physiology is intimately controlled by their surrounding environment. Importantly, the impact of temperature on animals depends not only on the degree of warming but also on their ability to accurately detect and evade that warming. The first step in this process is the recognition of changes in temperature by integral membrane proteins such as transient receptor potential (TRP) channels, some of which are temperature sensitive (thermoTRPs). Most of our understanding of thermoTRPs comes from studies in mammals, with a dearth of information in ectotherms on thermal sensitivities, and modulation of these thermal sensors. In this Commentary, we highlight what is known about the mechanism of temperature sensing in fishes. We also propose that changes in biological context (e.g. social interactions, lipids and immune state), leading to changes in physiology and behaviour, influence how fish sense temperature, potentially altering thermal susceptibility. Finally, we discuss redundancy in temperature-sensing systems, identify knowledge gaps, and suggest integrative approaches and questions for us to better understand temperature sensing and its modulation in fishes.

Antarctic notothenioid fish genomes contain evidence of an ancient evolutionary history including their remarkable adaptive radiation beginning ∼10 MYA amid extreme selective pressures of Southern Ocean glaciation. Several Antarctic lineages subsequently escaped and recolonized temperate waters, thus their genomes chronicle the re-adaptation to warmer climates. Here, we report two chromosome-scale genomes assembled from HiFi long reads and Hi-C data for the Antarctic cryonotothenioid Notothenia coriiceps and its secondarily temperate close relative Paranotothenia angustata . The N. coriiceps assembly comprises 11 pseudo-chromosomes, spans 1.12 Gbp with a N90 of 81.48 Mbp and 97.8% gene complete with 24,272 annotated genes. The P. angustata assembly comprises 13 pseudo-chromosomes, spans 1.00 Gbp with a N90 of 62.3 Mbp and 97.9% gene complete with 23,828 annotated genes. We report two new N. coriiceps mitochondrial genome structures, map the antifreeze glycoprotein loci, and corroborate the unusual notothenioid ribosomal RNA gene arrangement. The high-quality assemblies of this species pair provide valuable resources for investigating both the historical evolution of polar fish and their adaptive potential to climate change.

High-altitude life poses physiological challenges to all animals due to decreased environmental oxygen (O ₂ ) availability (hypoxia) and cold. Supporting high metabolic rates and body temperatures with limited O ₂ is challenging. Many birds, however, thrive at high altitudes. The O ₂ -transport cascade describes the pathway involved in moving O ₂ from the environment to the tissues encompassing: (i) ventilation, (ii) pulmonary O ₂ diffusion, (iii) circulation, (iv) tissue O ₂ diffusion, and (v) mitochondrial O ₂ use for ATP production. Shared avian traits such as rigid lungs with cross-current gas exchange and unidirectional airflow aid in O ₂ acquisition and transport in all birds. Many high-altitude birds, however, have evolved enhancements to some or all steps in the cascade. In this review, we summarize the current literature on gas exchange and O ₂ transport in high-altitude birds, providing an overview of the O ₂ -transport cascade that principally draws on the literature from high-altitude waterfowl, the most well-studied group of high-altitude birds. We close by discussing two important avenues for future research: distinguishing between the influences of plasticity and evolution and investigating whether the morphological and physiological differences discussed contribute to enhanced locomotor or thermogenic performance, a potential critical link to fitness. This article is part of the theme issue ‘The biology of the avian respiratory system’.

TRPV1, a member of the transient receptor potential (TRP) family, is a non-selective cation channel primarily known for its role in pain perception, inflammation, and thermosensation. In mammals, it responds to noxious heat (>43°C) and chemical stimuli such as capsaicin and protons. It is widely expressed in sensory neurons, notably in the dorsal root and trigeminal ganglia. However, it is also found in some non-neuronal tissues, like the skin and bladder. The human canonical variant of TRPV1 renders a protein with 839 residues. Different splice variants have been described, and some display a dominant negative effect, partially or totally inhibiting the activity of the canonical counterpart. Here, we characterize a splice variant that encodes for a channel of 850 amino acids (TRPV1 ₈₅₀ ). This variant is an evolutionary novelty of catarrhine (Old World monkeys and apes) primates, incorporating an exon of 33 bp long. Both imaging of membrane expression and electrophysiological recordings suggest that TRPV1 ₈₅₀ alone does not reach the plasma membrane. However, in cells co-expressing the canonical and TRPV1 ₈₅₀ variants, the latter would act as a dominant negative, preventing the canonical variant from reaching the plasma membrane and rendering smaller macroscopic currents in response to capsaicin. Thus, this new isoform of the TRPV1 ion channel represents a novel form of functional regulation only present in apes and Old World monkeys. Significance: We identified a novel isoform of the TRPV1 ion channel, a protein essential for detecting pain and heat stimuli unique to apes and Old World monkeys. This isoform contains an additional exonic sequence encoding eleven amino acids, which originated in the common ancestor of apes and Old World monkeys. This additional exonic sequence disrupts a specific domain in the N-terminal region of the protein, resulting in functional differences. Unlike the canonical TRPV1 isoform, this variant cannot reach the plasma membrane independently. Instead, it exerts a dominant-negative effect by interfering with the canonical TRPV1 protein, reducing its ability to localize to the cell surface and diminishing its responsiveness to capsaicin, a well-known TRPV1 activator.

Leaf cutting ants of the genus Atta cultivate fungal gardens, carefully modifying environmental conditions to maintain optimal temperature for fungal growth. Antennal nerves from Atta are highly temperature sensitive, but the underlying molecular sensor is unknown. Here, we utilize Atta texana (Texas leaf cutter ant) to investigate the molecular basis of ant temperature sensation and how it might have evolved as the range expanded northeast across Texas from ancestral populations in Mexico. We focus on transient receptor potential (TRP) channel genes, the best characterized temperature sensor proteins in animals. Atta texana antennae express 6 of 13 Hymenopteran TRP channel genes and sequences are under a mix of relaxed and intensified selection. In a behavioral assay, we find A. texana workers prefer 24 °C (range 21−26 °C) for fungal growth. There was no evidence of regulatory evolution across a temperature transect in Texas, but instead Hymenoptera‐specific TRPA (HsTRPA) expression highly correlated with ambient temperature. When expressed in vitro, HsTRPA from A. texana is temperature activated with Q10 values exceeding 100 on initial exposure to temperatures above 33 °C. Surprisingly, HsTRPA also appears to be activated by cooling, and therefore to our knowledge, the first non‐TRPA1 ortholog to be described with dual heat/cold activation and the first in any invertebrate.

Antarctic notothenioid fishes (cryonotothenioids) live in waters that range between −1.86°C and an extreme maximum +4°C. Evidence suggests these fish sense temperature peripherally, but the molecular mechanism of temperature sensation in unknown. Previous work identified transient receptor potential (TRP) channels TRPA1b, TRPM4 and TRPV1a as the top candidates for temperature sensors. Here, cryonotothenioid TRPA1b and TRPV1a are characterized using Xenopus oocyte electrophysiology. TRPA1b and TRPV1a showed heat-evoked currents with Q10s of 11.1 ± 2.2 and 20.5 ± 2.4, respectively. Unexpectedly, heat activation occurred at a threshold of 22.9 ± 1.3°C for TRPA1b and 32.1 ± 0.6°C for TRPV1a. These fish have not experienced such temperatures for at least 15 Myr. Either (1) another molecular mechanism underlies temperature sensation, (2) these fishes do not sense temperatures below these thresholds despite having lethal limits as low as 5°C, or (3) native cellular conditions modify the TRP channels to function at relevant temperatures. The effects of osmolytes, pH, oxidation, phosphorylation, lipids and accessory proteins were tested. No conditions shifted the activity range of TRPV1a. Oxidation in combination with reduced cholesterol significantly dropped activation threshold of TRPA1b to 11.3 ± 2.3°C, it is hypothesized the effect may be due to lipid raft disruption.

Background: Some poison arrow frogs sequester the toxin epibatidine as a defense against predators. We previously identified a single amino acid substitution (S108C) at a highly conserved site in a neuronal nicotinic acetylcholine receptor (nAChR) ß2 subunit that prevents epibatidine from binding to this receptor. When placed in a homologous mammalian nAChR this substitution minimized epibatidine binding but also perturbed acetylcholine binding, a clear cost. However, in the nAChRs of poison arrow frogs, this substitution appeared to have no detrimental effect on acetylcholine binding and, thus, appeared cost-free. Results: The introduction of S108C into the α4β2 nAChRs of non-dendrobatid frogs also does not affect ACh sensitivity, when these receptors are expressed in Xenopus laevis oocytes. However, α4β2 nAChRs with C108 had a decreased magnitude of neurotransmitter-induced currents in all species tested ( Epipedobates anthonyi , non-dendrobatid frogs, as well as human), compared with α4β2 nAChRs with the conserved S108. Immunolabeling of frog or human α4β2 nAChRs in the plasma membrane using radiolabeled antibody against the β2 nAChR subunit shows that C108 significantly decreased the number of cell-surface α4β2 nAChRs, compared with S108. Conclusions: While S108C protects these species against sequestered epibatidine, it incurs a potential physiological cost of disrupted α4β2 nAChR function. These results may explain the high conservation of a serine at this site in vertebrates, as well as provide an example of a tradeoff between beneficial and deleterious effects of an evolutionary change. They also provide important clues for future work on assembly and trafficking of this important neurotransmitter receptor.

Animals rely on their sensory systems to inform them of ecologically relevant environmental variation. In the Southern Ocean, the thermal environment has remained between −1.9 and 5 °C for 15 Myr, yet we have no knowledge of how an Antarctic marine organism might sense their thermal habitat as we have yet to discover a thermosensitive ion channel that gates (opens/closes) below 10 °C. Here, we investigate the evolutionary dynamics of transient receptor potential (TRP) channels, which are the primary thermosensors in animals, within cryonotothenioid fishes—the dominant fish fauna of the Southern Ocean. We found cryonotothenioids have a similar complement of TRP channels as other teleosts (∼28 genes). Previous work has shown that thermosensitive gating in a given channel is species specific, and multiple channels act together to sense the thermal environment. Therefore, we combined evidence of changes in selective pressure, gene gain/loss dynamics, and the first sensory ganglion transcriptome in this clade to identify the best candidate TRP channels that might have a functional dynamic range relevant for frigid Antarctic temperatures. We concluded that TRPV1a, TRPA1b, and TRPM4 are the likeliest putative thermosensors, and found evidence of diversifying selection at sites across these proteins. We also put forward hypotheses for molecular mechanisms of other cryonotothenioid adaptations, such as reduced skeletal calcium deposition, sensing oxidative stress, and unusual magnesium homeostasis. By completing a comprehensive and unbiased survey of these genes, we lay the groundwork for functional characterization and answering long-standing thermodynamic questions of thermosensitive gating and protein adaptation to low temperatures.