More Like this

1. Genetic variation in haemoglobin is associated with evolved changes in breathing in high-altitude deer mice

   https://doi.org/10.1242/jeb.243595  

   Ivy, Catherine M.; Wearing, Oliver H.; Natarajan, Chandrasekhar; Schweizer, Rena M.; Gutiérrez-Pinto, Natalia; Velotta, Jonathan P.; Campbell-Staton, Shane C.; Petersen, Elin E.; Fago, Angela; Cheviron, Zachary A.; et al (January 2022, Journal of Experimental Biology)

   ABSTRACT Physiological systems often have emergent properties but the effects of genetic variation on physiology are often unknown, which presents a major challenge to understanding the mechanisms of phenotypic evolution. We investigated whether genetic variants in haemoglobin (Hb) that contribute to high-altitude adaptation in deer mice (Peromyscus maniculatus) are associated with evolved changes in the control of breathing. We created F2 inter-population hybrids of highland and lowland deer mice to test for phenotypic associations of α- and β-globin variants on a mixed genetic background. Hb genotype had expected effects on Hb–O2 affinity that were associated with differences in arterial O2 saturation in hypoxia. However, high-altitude genotypes were also associated with breathing phenotypes that should contribute to enhancing O2 uptake in hypoxia. Mice with highland α-globin exhibited a more effective breathing pattern, with highland homozygotes breathing deeper but less frequently across a range of inspired O2, and this difference was comparable to the evolved changes in breathing pattern in deer mouse populations native to high altitude. The ventilatory response to hypoxia was augmented in mice that were homozygous for highland β-globin. The association of globin variants with variation in breathing phenotypes could not be recapitulated by acute manipulation of Hb–O2 affinity, because treatment with efaproxiral (a synthetic drug that acutely reduces Hb–O2 affinity) had no effect on breathing in normoxia or hypoxia. Therefore, adaptive variation in Hb may have unexpected effects on physiology in addition to the canonical function of this protein in circulatory O2 transport. 

   more » « less
2. Is hypoxia vulnerability in fishes a by-product of maximum metabolic rate?

   https://doi.org/10.1242/jeb.232520  

   Esbaugh, Andrew J.; Ackerly, Kerri L.; Dichiera, Angelina M.; Negrete, Benjamin (July 2021, Journal of Experimental Biology)

   null (Ed.)

   ABSTRACT The metabolic index concept combines metabolic data and known thermal sensitivities to estimate the factorial aerobic scope of animals in different habitats, which is valuable for understanding the metabolic demands that constrain species' geographical distributions. An important assumption of this concept is that the O2 supply capacity (which is equivalent to the rate of oxygen consumption divided by the environmental partial pressure of oxygen: ) is constant at O2 tensions above the critical O2 threshold (i.e. the where O2 uptake can no longer meet metabolic demand). This has led to the notion that hypoxia vulnerability is not a selected trait, but a by-product of selection on maximum metabolic rate. In this Commentary, we explore whether this fundamental assumption is supported among fishes. We provide evidence that O2 supply capacity is not constant in all fishes, with some species exhibiting an elevated O2 supply capacity in hypoxic environments. We further discuss the divergent selective pressures on hypoxia- and exercise-based cardiorespiratory adaptations in fishes, while also considering the implications of a hypoxia-optimized O2 supply capacity for the metabolic index concept. 

   more » « less
3. New insights into the allosteric effects of CO2 and bicarbonate on crocodilian hemoglobin

   https://doi.org/10.1242/jeb.242615  

   Bautista, Naim M.; Malte, Hans; Natarajan, Chandrasekhar; Wang, Tobias; Storz, Jay F.; Fago, Angela (August 2021, Journal of Experimental Biology)

   ABSTRACT Crocodilians are unique among vertebrates in that their hemoglobin (Hb) O2 binding is allosterically regulated by bicarbonate, which forms in red blood cells upon hydration of CO2. Although known for decades, this remarkable mode of allosteric control has not yet been experimentally verified with direct evidence of bicarbonate binding to crocodilian Hb, probably because of confounding CO2-mediated effects. Here, we provide the first quantitative analysis of the separate allosteric effects of CO2 and bicarbonate on purified Hb of the spectacled caiman (Caiman crocodilus). Using thin-layer gas diffusion chamber and Tucker chamber techniques, we demonstrate that both CO2 and bicarbonate bind to Hb with high affinity and strongly decrease O2 saturation of Hb. We propose that both effectors bind to an unidentified positively charged site containing a reactive amino group in the low-O2 affinity T conformation of Hb. These results provide the first experimental evidence that bicarbonate binds directly to crocodilian Hb and promotes O2 delivery independently of CO2. Using the gas diffusion chamber, we observed similar effects in Hbs of a phylogenetically diverse set of other caiman, alligator and crocodile species, suggesting that the unique mode of allosteric regulation by CO2 and bicarbonate evolved >80–100 million years ago in the common ancestor of crocodilians. Our results show a tight and unusual linkage between O2 and CO2 transport in the blood of crocodilians, where the build-up of erytrocytic CO2 and bicarbonate ions during breath-hold diving or digestion facilitates O2 delivery, while Hb desaturation facilitates CO2 transport as protein-bound CO2 and bicarbonate. 

   more » « less
4. Gills, growth and activity across fishes

   https://doi.org/10.1111/faf.12757  

   Bigman, Jennifer S.; Wegner, Nicholas C.; Dulvy, Nicholas K. (May 2023, Fish and Fisheries)

   Abstract Life history theory suggests that maximum size and growth evolve to maximize fitness. In contrast, the Gill Oxygen Limitation Theory (GOLT) suggests that growth and maximum size in fishes and other aquatic, water‐breathing organisms is constrained by the body mass‐scaling of gill surface area. Here, we use new data and a novel phylogenetic Bayesian multilevel modelling framework to test this idea by asking the three questions posed by the GOLT regarding maximum size, growth and gills. Across fishes, we ask whether the body mass‐scaling of gill surface area explains (1) variation in the von Bertalanffy growth coefficient (k) above and beyond that explained by asymptomatic size (W_∞), (2) variation in growth performance (a trait that integrates the tradeoff betweenkandW_∞) and (3) more variation in growth performance compared to activity (as approximated by caudal fin aspect ratio). Overall, we find that there is only a weak relationship among maximum size, growth and gill surface area across species. Indeed, the body mass‐scaling of gill surface area does not explain much variation ink(especially for those species that reach the sameW_∞) or growth performance. Activity explained three to five times more variation in growth performance compared to gill surface area. Our results suggest that in fishes, gill surface area is not the only factor that explains variation in maximum size and growth, and that other covariates (e.g. activity) are likely important in understanding how growth, maximum size and other life history traits vary across species. 

   more » « less
5. Thermal optima in the hypoxia tolerance of marine ectotherms: Physiological causes and biogeographic consequences

   https://doi.org/10.1371/journal.pbio.3002443  

   Endress, Martin-Georg A; Penn, Justin L; Boag, Thomas H; Burford, Benjamin P; Sperling, Erik A; Deutsch, Curtis A (January 2024, PLOS Biology)

   Pawar, Samraat (Ed.)

   The minimum O2 needed to fuel the demand of aquatic animals is commonly observed to increase with temperature, driven by accelerating metabolism. However, recent measurements of critical O2 thresholds (“Pcrit”) reveal more complex patterns, including those with a minimum at an intermediate thermal “optimum”. To discern the prevalence, physiological drivers, and biogeographic manifestations of such curves, we analyze new experimental and biogeographic data using a general dynamic model of aquatic water breathers. The model simulates the transfer of oxygen from ambient water through a boundary layer and into animal tissues driven by temperature-dependent rates of metabolism, diffusive gas exchange, and ventilatory and circulatory systems with O2-protein binding. We find that a thermal optimum in Pcrit can arise even when all physiological rates increase steadily with temperature. This occurs when O2 supply at low temperatures is limited by a process that is more temperature sensitive than metabolism, but becomes limited by a less sensitive process at warmer temperatures. Analysis of published species respiratory traits suggests that this scenario is not uncommon in marine biota, with ventilation and circulation limiting supply under cold conditions and diffusion limiting supply at high temperatures. Using occurrence data, we show that species with these physiological traits inhabit lowest O2 waters near the optimal temperature for hypoxia tolerance and are restricted to higher O2 at temperatures above and below this optimum. Our results imply that hypoxia tolerance can decline under both cold and warm conditions and thus may influence both poleward and equatorward species range limits. 

   more » « less