Coping with the cold: energy storage strategies for surviving winter in freshwater fish

For many ectothermic animals, the acquisition, storage and depletion of lipids is integral to successfully coping with reduced metabolic rates and activity levels associated with cold, winter periods. In fish, lipids are crucial for overwinter survival and successful reproduction. The timing and magnitude of seasonal lipid storage should therefore vary predictably among fish with different thermal preferences and spawn times. Small‐ and large‐bodied fish should also face different constraints associated with season that influence lipid cycling. However, much work to date has been species‐ and location‐specific and a general conceptual model for the seasonal energy budgets of freshwater fish is lacking. Here, we conducted a comprehensive literature review of seasonal lipid levels in freshwater fishes. We predicted that warm and cool water species would be more likely to demonstrate peak lipid levels during warm months than cold water species, and expected a larger magnitude of annual lipid cycling in warm and cool water compared to cold water fish. We also expected dampened lipid cycling in larger fish due to their lower mass‐specific metabolic rates. Observed patterns in the timing and magnitude of lipid storage contradicted our prediction because lipid cycling was widespread across species, despite thermal guild, with peak lipid levels commonly occurring during warmer months, even in cold water fish. For body size effects, larger bodied fish species had dampened seasonal lipid cycling, as predicted. We developed a conceptual framework describing how the ‘scope’ for variation in annual lipid cycling changes with body size both among and within species in order to guide future work. Together, our findings suggest that energy acquired during warm months is broadly important for overwinter survival and reproduction in fishes, and provide a new perspective on the differential constraints and physiological responses to seasonality among freshwater fish. Improving our understanding of these dynamics is especially pressing given that a changing global climate is anticipated to alter existing seasonal signals.     

Seasonal variations in hematocrit, red cell hemoglobin and nucleoside triphosphate concentrations, in the European eel Anguilla anguilla

Eels acclimatized in nature show a significant annual variation in erythrocytic guanosine triphosphate (GTP) concentration, temperature range 0.5-17 degrees C. A similar but smaller annual variation is also present in eels acclimated in the laboratory at constant temperature, 17 degrees C. Hematocrit and blood oxygen capacity showed no seasonal variation. Natural minimal and maximal red cell GTP concentrations were found at the end of the dormancy period (March) and in the late summer, respectively. Furthermore, a chronological connection of the erythrocytic GTP values versus ambient temperature, in the natural environment, demonstrates a hysteresis. This allows for a prediction of a slowly progressing enhancement of the temperature effect on Hb-O2 binding throughout autumn, whereas a relatively fast and pronounced enhancement predictably takes place in spring (April-May) coincident with the "awakening" of the eels.     

Seasonal acclimation of preferred body temperatures improves the opportunity for thermoregulation in newts

Seasonal acclimation and thermoregulation represent major components of complex thermal strategies by which ectotherms cope with the heterogeneity of their thermal environment. Some ectotherms possess the acclimatory capacity to shift seasonally their thermoregulatory behavior, but the frequent use of constant acclimation temperatures during experiments and the lack of information about thermal heterogeneity in the field obscures the ecological relevance of this plastic response. We examined the experimentally induced seasonal acclimation of preferred body temperatures (T(p)) in alpine newts Ichthyosaura (formerly Triturus) alpestris subjected to a gradual increase in acclimation temperature from 5°C during the winter to a constant 15°C or diel fluctuations between 10° and 20°C during the spring/summer. Both the mean and range of T(p) followed the increase in mean acclimation temperature without the influence of diel temperature fluctuations. The direction and magnitude of this acclimatory capacity has the potential to increase the time window available for thermoregulation. Although thermoregulation and thermal acclimation are often considered as separate but coadapted adjustments to thermal heterogeneity, their combined response is employed by newts to tackle seasonal variation in a thermoregulatory-challenging aquatic environment.     

Seasonal differences in egg size in three species of crabs from a tropical upwelling zone

Egg size and offspring size are fundamentally important aspects of the life histories of all animals. However the impact of environmental conditions on intraspecific variation in egg size of marine invertebrates is poorly documented. Here we followed three species of intertidal crabs Xanthodius sternberghii, Petrolisthes armatus and Clibanarius albidigitus to understand how seasonal environmental variation in temperature and salinity associated with seasonal upwelling impacts egg size. Ovigerous females of both P. armatus and C. albidigitus were found year round, while X. sternberghii has a limited reproductive season, with ovigerous females found only between November and February. In all three species more than half of the variation in egg size was attributable to variation among broods from different females. Eggs collected during the dry, upwelling season were significantly larger than those collected during the wet, non-upwelling season. Multiple regression analysis showed that average egg size from each brood was significantly negatively correlated with temperature for all three species. Egg size was also negatively correlated with salinity in P. armatus when we controlled for temperature. Overall these results support the idea that changes in environmental temperature caused by seasonal upwelling play a significant role in generating seasonal differences in egg size.     

Fall field crickets did not acclimate to simulated seasonal changes in temperature

In nature, many organisms alter their developmental trajectory in response to environmental variation. However, studies of thermal acclimation have historically involved stable, unrealistic thermal treatments. In our study, we incorporated ecologically relevant treatments to examine the effects of environmental stochasticity on the thermal acclimation of the fall field cricket (Gryllus pennsylvanicus). We raised crickets for 5 weeks at either a constant temperature (25°C) or at one of three thermal regimes mimicking a seasonal decline in temperature (from 25 to 12°C). The latter three treatments differed in their level of thermal stochasticity: crickets experienced either no diel cycle, a predictable diel cycle, or an unpredictable diel cycle. Following these treatments, we measured several traits considered relevant to survival or reproduction, including growth rate, jumping velocity, feeding rate, metabolic rate, and cold tolerance. Contrary to our predictions, the acclimatory responses of crickets were unrelated to the magnitude or type of thermal variation. Furthermore, acclimation of performance was not ubiquitous among traits. We recommend additional studies of acclimation in fluctuating environments to assess the generality of these findings.     

A biogeographic reversal in sexual size dimorphism along a continental temperature gradient

The magnitude and direction of sexual size dimorphism (SSD) varies greatly across the animal kingdom, reflecting differential selection pressures on the reproductive and/or ecological roles of males and females. If the selection pressures and constraints imposed on body size change along environmental gradients, then SSD will vary geographically in a predictable way. Here, we uncover a biogeographical reversal in SSD of lizards from Central and North America: in warm, low latitude environments, males are larger than females, but at colder, high latitudes, females are larger than males. Comparisons to expectations under a Brownian motion model of SSD evolution indicate that this pattern reflects differences in the evolutionary rates and/or trajectories of sex‐specific body sizes. The SSD gradient we found is strongly related to mean annual temperature, but is independent of species richness and body size differences among species within grid cells, suggesting that the biogeography of SSD reflects gradients in sexual and/or fecundity selection, rather than intersexual niche divergence to minimize intraspecific competition. We demonstrate that the SSD gradient is driven by stronger variation in male size than in female size and is independent of clutch mass. This suggests that gradients in sexual selection and male–male competition, rather than fecundity selection to maximize reproductive output by females in seasonal environments, are predominantly responsible for the gradient.     

Seasonal metabolic changes in a year-round reproductively active subtropical tree-frog (Hypsiboas prasinus)

Although seasonal metabolic variation in ectothermic tetrapods has been investigated primarily in the context of species showing some level of metabolic depression during winter, but several species of anurans maintain their activity patterns throughout the year in tropical and subtropical areas. The tree-frog Hypsiboas prasinus occurs in the subtropical Atlantic Forest and remains reproductively active during winter, at temperatures below 10 degrees C. We compared males calling in summer and winter, and found that males of H. prasinus exhibit seasonal adjustments in metabolic and morphometric variables. Individuals calling during winter were larger and showed higher resting metabolic rates than those calling during summer. Calling rates were not affected by season. Winter animals showed lower liver and heart activity level of citrate synthase (CS), partially compensated by larger liver mass. Winter individuals also showed higher activity of pyruvate kinase (PK) and lower activity of CS in trunk muscles, and higher activity of CS in leg muscles. Winter metabolic adjustments seem to be achieved by both compensatory mechanisms to the lower environmental temperature and a seasonally oriented aerobic depression of several organs. The impact of seasonal metabolic changes on calling performance and the capacity of subtropical anurans for metabolic thermal acclimatization are also discussed.     

Seasonal variation in haematological parameters in male and female Tinca tinca

This study was designed to investigate any seasonal (spring, summer, autumn and winter) changes in haematological parameters in the blood of Tinca tinca measuring the number of red blood cells (RBC), haematocrit, white blood cells, and total plasma proteins.The results show significant changes in RBC and haematocrit in males comparing spring and summer with autumn and winter, whereas in females the RBC remained constant for all 4 seasons but the haematocrit decreased in autumn and winter compared to spring and summer. The white blood cells of male and female animals were significantly lower in spring and winter compared to summer and autumn. In male fish total protein contents significantly decreased in autumn and winter compared to spring and summer, whereas in females protein output significantly decreased in winter compared to the other seasons. The results indicate marked seasonal variation in the blood of male and female Tinca tinca. This variation may play a important protective role for the survival of the animals.     

Phenotypic variation in smooth softshell turtles (<Emphasis Type="Italic">Apalone mutica</Emphasis>) from eggs incubated in constant versus fluctuating temperatures

Temperatures experienced during embryonic development elicit well-documented phenotypic variation in embryonic and neonatal animals. Most research, however, has only considered the effects of constant temperatures, even though developmental temperatures in natural settings fluctuate considerably on a daily and seasonal basis. A laboratory study of 15 clutches of smooth softshell turtles (Apalone mutica) was conducted to explicitly examine the influence of thermal variance on phenotypic variation. Holding mean temperature constant and eliminating substrate moisture effects permitted a clear assessment of the impact of thermal variance on hatching success, incubation length, hatchling body size, swimming speed, and righting time. Incubation length and swimming speed varied significantly among temperature treatments. Both traits tended to increase with increasing thermal variance during embryonic development. Clutch significantly affected all traits examined, except righting time, even after accounting for the effects of initial egg mass. These results highlight the importance of accounting for the impact of both thermal mean and variance on phenotypic variation. The findings also strengthen the increasing recognition of maternal clutch effects as critical factors influencing phenotypic variation in neonatal animals.     

Climate and mammalian life histories

Mammals display considerable geographical variation in life history traits. To understand how climatic factors might influence this variation, we analysed the relationship between life history traits – adult body size, litter size, number of litters per year, gestation length, neonate body mass, weaning age and age at sexual maturity – and several environmental variables quantifying the seasonality and predictability of temperature and precipitation across the distribution range of five terrestrial mammal groups. Environmental factors correlated strongly with each other; therefore, we used principal components analysis to obtain orthogonal climatic predictors that could be used in multivariate models. We found that in bats, primates and even‐toed ungulates adult body size tends to be larger in species inhabiting cold, dry, seasonal environments, whereas in carnivores and rodents a smaller body size is characteristic of warm, dry environments, suggesting that low food availability might limit adult size. Species inhabiting cold, dry, seasonal habitats have fewer, larger litters and shorter gestation periods; however, annual fecundity in these species is not higher, implying that the large litter size of mammals living at high latitudes is probably a consequence of time constraints imposed by strong seasonality. On the other hand, the number of litters per year and annual fecundity were greater in species inhabiting environments with higher seasonality in precipitation. Lastly, we found little evidence for specific effects of environmental variability. Our results highlight the complex effects of environmental factors in the evolution of life history traits in mammals. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 111 , 719–736.     

Shorebirds' seasonal adjustments in thermogenic capacity are reflected by changes in body mass: how preprogrammed and instantaneous acclimation work together

Phenotypic flexibility in shorebirds has been studied mainly in the context of adjustments to migration and to quality of food; little is known on how birds adjust their phenotype to harsh winter conditions. We showed earlier that red knot (Calidris canutus islandica) can acclimate to cold by elevating body mass. This goes together with larger pectoral muscles, i.e., greater shivering machinery, and thus, better thermogenic capacity. Here, we present results of a yearlong experiment with indoor captive knots to determine whether this strategy is part of their natural seasonal phenotypic cycle. We maintained birds under three thermal regimes: constant cold (5 °C), constant thermoneutrality (25 °C) and natural seasonal variation between these extremes (9-22 °C). Each month we measured variables related to the birds' endurance to cold and physiological maintenance [body mass, thickness of pectoral muscles, summit metabolic rate (M(sum)), food intake, gizzard size, basal metabolic rate (BMR)]. Birds from all treatments expressed synchronized and comparable variation in body mass in spite of thermal treatments, with a 17-18% increase between the warmest and coldest months of the year; which appeared regulated by an endogenous driver. In addition, birds living in the cold exhibited a 10% higher average body mass than did those maintained at thermoneutrality. Thickness of the pectoral muscle tracked changes in body mass in all treatments and likely contributed to greater capacity for shivering in heavier birds. Consequently, M(sum) was 13% higher in cold-acclimated birds compared to those experiencing no thermoregulation costs. However, our data also suggest that part of maximal heat production comes from nonshivering processes. Birds facing cold conditions ate up to 25% more food than did birds under thermoneutral conditions, yet did not develop larger gizzards. Seasonal variation in BMR followed changes in body mass, probably reflecting changes in mass of metabolically active tissues. Just as cold-exposed birds, red knots in the variable treatment increased body mass in winter, thereby improving cold endurance. During summer, however, they maintained a lower body mass and thermogenic capacity compared to cold-exposed birds, similar to individuals kept at thermoneutrality. We conclude that red knots acclimate to seasonal variations in ambient temperature by modulating body mass, combining a preprogrammed increase in mass during winter with a capacity for fine-tuning body mass and thermogenic capacity to temperature variations.     

Female investment in offspring size and number shifts seasonally in a lizard with single-egg clutches

The timing of reproduction strongly influences reproductive success in many organisms. For species with extended reproductive seasons, the quality of the environment may change throughout the season in ways that impact offspring survival, and, accordingly, aspects of reproductive strategies may shift to maximize fitness. Life-history theory predicts that if offspring environments deteriorate through the season, females should shift from producing more, smaller offspring early in the season to fewer, higher quality offspring later in the season. We leverage multiple iterations of anole breeding colonies, which control for temperature, moisture, and food availability, to identify seasonal changes in reproduction. These breeding colonies varied only by the capture date of the adult animals from the field. We show that seasonal cohorts exhibit variation in key reproductive traits such as inter-clutch interval, egg size and hatchling size consistent with seasonal shifts in reproductive effort. Overall, reproductive effort was highest early in the season due to a relatively high rate of egg production. Later season cohorts produced fewer, but larger offspring. We infer that these results indicate a strategy for differential allocation of resources through the season. Females maximize offspring quantity when environments are favorable, and maximize offspring quality when environments are poor for those offspring. Our study also highlights that subtle differences in methodology (such as capture date of study animals) may influence the interpretation of results. Researchers interested in reproduction must be conscious of how their organism’s reproductive patterns may shift through the season when designing experiments or comparing results across studies.     

Calling behaviour under climate change: geographical and seasonal variation of calling temperatures in ectotherms

Calling behaviour is strongly temperature‐dependent and critical for sexual selection and reproduction in a variety of ectothermic taxa, including anuran amphibians, which are the most globally threatened vertebrates. However, few studies have explored how species respond to distinct thermal environments at time of displaying calling behaviour, and thus it is still unknown whether ongoing climate change might compromise the performance of calling activity in ectotherms. Here, we used new audio‐trapping techniques (automated sound recording and detection systems) between 2006 and 2009 to examine annual calling temperatures of five temperate anurans and their patterns of geographical and seasonal variation at the thermal extremes of species ranges, providing insights into the thermal breadths of calling activity of species, and the mechanisms that enable ectotherms to adjust to changing thermal environments. All species showed wide thermal breadths during calling behaviour (above 15 °C) and increases in calling temperatures in extremely warm populations and seasons. Thereby, calling temperatures differed both geographically and seasonally, both in terrestrial and aquatic species, and were 8–22 °C below the specific upper critical thermal limits (CT_max) and strongly associated with the potential temperatures of each thermal environment (operative temperatures during the potential period of breeding). This suggests that calling behaviour in ectotherms may take place at population‐specific thermal ranges, diverging when species are subjected to distinct thermal environments, and might imply plasticity of thermal adjustment mechanisms (seasonal and developmental acclimation) that supply species with means of coping with climate change. Furthermore, the thermal thresholds of calling at the onset of the breeding season were dissimilar between conspecific populations, suggesting that other factors besides temperature are needed to trigger the onset of reproduction. Our findings imply that global warming would not directly inhibit calling behaviour in the study species, although might affect other temperature‐dependent features of their acoustic communication system.     

Ecological biogeography of North American mammals: species density and ecological structure in relation to environmental gradients

Aim To evaluate the relationship of climate and physiography to species density and ecological diversity of North American mammals. Location North America, including Mexico and Central America. Methods Species density, size structure and trophic structure of mammalian faunas and nine environmental variables were documented for quadrats covering the entire continent. Spatial autocorrelation of species density and the environmental variables illustrated differences in their spatial structure at the continental scale. We used principal component analysis to reduce the dimensionality of the climatic variables, linear multiple regression to determine which environmental variables best predict species density for the continent and several regions of the continent, and canonical ordination to evaluate how well the environmental variables predict ecological structure of mammalian faunas over North America. Results In the best regression model, five environmental variables, representing seasonal extremes of temperature, annual energy and moisture, and elevation, predicted 88% of the variation in species density for the whole continent. Among different regions of North America, the environmental variables that predicted species density vary. Changes in the size and trophic structure of mammalian faunas accompany changes in species density. Redundancy analysis demonstrated that environmental variables representing winter temperature, frostfree period, potential and actual evapotranspiration, and elevation account for 77% of the variation in ecological structure. Main conclusions The latitudinal gradient in mammalian species density is strong, but most of it is explained by variation in the environmental variables. Each ecological category peaks in species richness under particular environmental conditions. The changes of greatest magnitude involve the smallest size categories (< 10 g, 11–100 g), aerial insectivores and frugivores. Species in these categories, mostly bats, increase along a gradient of decreasing winter temperature and increasing annual moisture and frostfree period, trends correlated with latitude. At the opposite end of this gradient, species in the largest size category (101–1000 kg) increase in frequency. Species in size categories 3 (101–1000 g), 5 (11–100 kg) and 6 (101–1000 kg), herbivores, and granivores increase along a longitudinal gradient of increasing annual potential evapotranspiration and elevation. Much of the spatial pattern is consistent with ecological sorting of species ranges along environmental gradients, but differential rates of speciation and extinction also may have shaped the ecological diversity of extant North American mammals.     

Climatic predictors of temperature performance curve parameters in ectotherms imply complex responses to climate change

Determining organismal responses to climate change is one of biology's greatest challenges. Recent forecasts for future climates emphasize altered temperature variation and precipitation, but most studies of animals have largely focused on forecasting the outcome of changes in mean temperature. Theory suggests that extreme thermal variation and precipitation will influence species performance and hence affect their response to changes in climate. Using an information-theoretic approach, we show that in squamate ectotherms (mostly lizards and snakes), two fitness-influencing components of performance, the critical thermal maximum and the thermal optimum, are more closely related to temperature variation and to precipitation, respectively, than they are to mean thermal conditions. By contrast, critical thermal minimum is related to mean annual temperature. Our results suggest that temperature variation and precipitation regimes have had a strong influence on the evolution of ectotherm performance, so that forecasts for animal responses to climate change will have to incorporate these factors and not only changes in average temperature.     

Physiological flexibility in the Andean lizard <Emphasis Type="Italic">Liolaemus bellii</Emphasis>: seasonal changes in energy acquisition,storage and expenditure

According to the “barrel model”, an organism may be represented by a container, with input energy constraints (foraging, digestion, and absorption) symbolized by funnels connected in tandem, and energy outputs (maintenance, growth, and reproduction) symbolized by a series of spouts arranged in parallel. Animals can respond to changes in environmental conditions, through adjustments in the size of the funnels, the fluid stored inside the barrel, or the output flow through the spouts. In the present study, we investigate the interplay among these processes through the analysis of seasonal changes in organ size and metabolic rate in a lizard species (Liolaemus bellii) that inhabits extremely seasonal environments in the Andes range. We found that digestive organ size showed the greatest values during spring and summer, that is, during the foraging seasons. Energy reserves were larger during summer and autumn, and then decreased through winter and spring, which was correlated with overwintering maintenance and reproductive costs. Standard metabolic rate was greater during the high-activity seasons (spring and summer), but this increase was only noticeable at higher environmental temperatures. The ability of many lizard species to reduce their maintenance cost during the cold months of the year, beyond what is expected from temperature decrease, is probably related to their success in coping with highly fluctuating environments. Here, we demonstrate that this ability is correlated with high physiological flexibility, which allows animals to adjust energy acquisition, storing and expenditure processes according to current environmental conditions.     

Acclimation of thermal physiology in natural populations of Drosophila melanogaster : a test of an optimality model

Many organisms modify their physiological functions by acclimating to changes in their environment. Recent studies of thermal physiology have been influenced by verbal models that fail to consider the selective advantage of acclimation and thus make no predictions about variation in acclimation capacity. We used a quantitative model of optimal plasticity to generate predictions about the capacity of Drosophila melanogaster to acclimate to developmental temperature. This model predicts that the ability to acclimate thermal sensitivity should evolve when temperature varies greatly among generations. Based on the model, we expected that flies from the highly seasonal environment of New Jersey would acclimate thermal sensitivity more than would flies from the less seasonal environment of Florida. When raised at constant and fluctuating temperatures, flies from these populations failed to adjust their thermal optima in the way predicted by the model, suggesting that current assumptions about functional and genetic constraints should be reconsidered.     

The adaptation of biological membranes to temperature and pressure: Fish from the deep and cold

The homoeostatic regulation of bilayer order is a property of functional importance. Arguably, it is best studied in those organisms which experience and must overcome disturbances in bilayer order which may be imposed by variations in temperature of hydrostatic pressure. This article reviews our recent work on the adaptations of order in brain membranes of those fish which acclimate to seasonal changes in temperature or which have evolved in extreme thermal or abyssal habitats. The effects of temperature and pressure upon hydrocarbon order and phase state are reviewed to indicate the magnitude of the disturbances experienced by animals in their environments over the seasonal or evolutionary timescale. Acclimation of fish to altered temperature leads to a partial correction of order, while comparison of fish from extreme cold environments with those from temperate or tropical waters reveals a more complete adaptation. Fish from the deep sea also display adaptations of bilayer order which largely overcome the ordering effects of pressure.     

The Sensitivity of Evapotranspiration to Inter-Specific Plant Neighbor Interactions: Implications for Models

Evapotranspiration (ET) is an important water loss flux in ecosystem water cycles, and quantifying the spatial and temporal variation of ET can improve ecohydrological models in arid ecosystems. Plant neighbor interactions may be a source of spatial and temporal variation in ET due to their effects on the above- and belowground microclimate and increased water demand for transpiration. Over longer timescales (annual to multiple years), adjustments in plant physiological traits may occur in response to neighbor environments, potentially affecting the transpiration (T) component of ET. We used a dynamic soil water model to assess the sensitivity of ET and T estimates to neighbor effects on soil moisture via competition for water, aboveground microclimate effects via canopy shading, and physiological adjustments (specifically, root distribution, stomatal behavior, and canopy leaf area). We focus on a common desert shrub (Larrea tridentata) under different inter-specific neighbor environments and precipitation regimes. Neighbors impacted T of Larrea by as much as 75% at the patch scale (plant and surrounding soil) and 30% at the stand scale. Annual T estimates were highly sensitive to changes in soil moisture associated with competition for water, and the inclusion of physiological adjustments to neighbor environments significantly impacted seasonal T. Plant neighbor interactions can significantly influence ET and soil moisture, and their inclusion in models can help explain spatial and temporal variation in water fluxes in arid ecosystems. Furthermore, physiological adjustments to neighbor environments may be an important source of variation to include in models that operate over seasonal timescales or in studies focused on plant responses to precipitation under climate change.     

Hummingbird blood traits track oxygen availability across space and time

Predictable trait variation across environments suggests shared adaptive responses via repeated genetic evolution, phenotypic plasticity or both. Matching of trait–environment associations at phylogenetic and individual scales implies consistency between these processes. Alternatively, mismatch implies that evolutionary divergence has changed the rules of trait–environment covariation. Here we tested whether species adaptation alters elevational variation in blood traits. We measured blood for 1217 Andean hummingbirds of 77 species across a 4600-m elevational gradient. Unexpectedly, elevational variation in haemoglobin concentration ([Hb]) was scale independent, suggesting that physics of gas exchange, rather than species differences, determines responses to changing oxygen pressure. However, mechanisms of [Hb] adjustment did show signals of species adaptation: Species at either low or high elevations adjusted cell size, whereas species at mid-elevations adjusted cell number. This elevational variation in red blood cell number versus size suggests that genetic adaptation to high altitude has changed how these traits respond to shifts in oxygen availability.