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Biology subjects

Nord, A.

Publications and source records attributed to Nord, A..

At least 19 recordsLinked to original sources

Repeatable individual variation in body temperature is associated with cold tolerance and exercise-induced hyperthermia in zebra finches

In endotherms, body temperature is regulated by balancing the rates of metabolic heat production and dissipation. Birds and mammals maintain high and relatively constant body temperatures, but there is growing evidence that body temperature and heterothermy vary considerably between individuals of a population. Based on the interdependence of metabolic rate and body temperature, variation in body temperature could be expected to be related to metabolic performance. In this study, we aimed to determine if body temperature is a variable and repeatable trait in captive zebra finches (Taeniopygia guttata) and if body temperature could be related to different metrics of performance. We measured body temperature for 14 days in in caged male zebra finches to assess within- and among-individual variation and repeatability, as well as during measurements of three metabolic traits; basal (BMR), summit cold-induced (Msum) and maximum exercise-induced (MMR) metabolic rate. Median Tb (R = 0.48), and peak Tb (R = 0.53) body temperature were repeatable and positively correlated, suggesting that the birds show consistent differences in body temperature. We found that birds with higher daytime body temperatures showed higher thermoregulatory performance in a cold challenge and had higher body temperature during forced exercise. However, daytime body temperature was not related to MMR or BMR. Our study is one of few that have measured the repeatability of body temperature in birds. Our results show that individuals may have distinct body temperature phenotypes which could be related to metabolic and thermoregulatory performance. However, additional research is needed to disentangle the interrelated effects of metabolic capacity, body temperature, and heat dissipation on performance and how this might change with thermal conditions and activity levels.

physiology↗

Air temperature limits aerobic capacity and scope in active birds

Thermal tolerance limits are an important determinant of species vulnerability to climate change. However, most of our knowledge of thermal tolerance pertains to resting animals, which could yield unrealistic predictions about how air temperature will affect animals when they are active. To gain a better understanding of thermoregulatory contstraints in active birds, we induced zebra finches in captivity to exercise continuously in air temperatures ranging from cool to warm (12- 36 C) while we simultaneously measured their metabolic rate, body temperature, and evaporative water loss. During activity, birds overheated in air temperatures well below their resting thermal tolerance limit, and aerobic scope was reduced by 22% at the warmest temperature. Although zebra finches showed a 8-fold increase in evaporative water loss during exercise in the warmest temperature, this was not sufficiently high to compensate for the substantial increase in heat produced during activity. This could explain why birds became hyperthermic and showed reductions in metabolic rate in the higher air temperatures. Thus, our results provide a mechanistic explanation for how heat could limit aerobic capacity and scope in active birds. These findings support growing evidence that increased air temperature can lead to sub-lethal fitness costs in free-living birds.

ecology↗

Allometric correlates of heat tolerance in birds: A test using quail breeds with extreme size variation

Birds and mammals are shrinking and shapeshifting as global temperatures rise. Ecogeographic rules predict that such changes should ease heat stress by increasing surface-area-to-volume ratios, and thus, the capacity for heat exchange. This has led to the hypothesis that body size reductions are driven by thermoregulatory selection or adaptive plasticity, although recent syntheses point to more complex, multifactorial causes. Crucially, recent theoretical models predict that thermoregulatory benefits of smaller body size only emerge at extreme deviations from average phenotypes. Here, we exploit agricultural selection in Japanese quail to directly test this hypothesis, using three breeds spanning extreme differences in body mass, surface area, and relative appendage lengths. Evaporative cooling capacity and the scope for evaporative water loss broadly followed allometric predictions when contrasting small and larger breeds. As expected, this allowed the smallest breed to tolerate higher air temperatures. However, differences in heat tolerance limits between breeds were consistently much smaller than predicted. Additionally, the breadth of thermoneutral zones overlapped in full, and upper critical temperatures were remarkably similar, between breeds. Together, these results show that heat tolerance is only weakly linked to surface-area-to-volume relationships and cannot be explained by size alone. Thus, although smaller bodies may modestly enhance heat dissipation when size variation in a population is substantial, our findings suggest that recent body size reductions and morphological shifts are unlikely to be driven primarily by thermoregulatory benefits.

evolutionary biology↗

Spatiotemporal and demographic effects on avian malaria prevalence in blue tits

While the ubiquity of parasites is well understood, the extent to which host demographic factors shape parasite prevalence patterns merits further investigation. Using 15 years of breeding data from blue tits (Cyanistes caeruleus) in southern Sweden, spanning a 26-year timeframe, we assessed the roles of host age, sex, and field site on the odds of infection with three avian malaria parasite genera: Haemoproteus, Plasmodium, and Leucocytozoon. Further, we also evaluated the effects of these demographics on the odds of triple-genus coinfections. We found first-year breeders have fewer infections with Haemoproteus and Plasmodium, and fewer triple infections compared to older age classes, suggesting that birds are accumulating infections over time. Leucocytozoon infections are more prevalent in males than in females, and this may be due to sex-specific differences in physiology. The prevalence of malaria parasites and their coinfections also vary between the three sampling sites, indicative of an effect of host breeding habitat, even at a relatively small spatial scale (neighboring sites were separated by <5km). Across all three field sites, prevalence is overall significantly increasing over time. For Haemoproteus, this increase is more pronounced in older birds compared to younger birds. Such temporal changes in age-related infection patterns would not have been apparent without long-term data thus highlighting the importance of long-term studies for informing our understanding of host demographic effects on parasite prevalence.

molecular biology↗

Rising role of phenotypic plasticity explains changes in avian body size distributions

Natural selection widely favours the largest within animal species. Why body sizes are declining in the worlds temperate birds is therefore mechanistically confusing and ecologically worrying. We argue that understanding the causes of these declines requires knowledge of how complete, body mass probability distributions - not just averages - are moving. Using data from 159 North American bird species - spanning 26 families, 53{degrees} of latitude, and 25 years - we show that body mass distributions are not only downgrading, but also narrowing, and losing their upper tails (the heaviest individuals), with the largest changes occurring at southern range limits. Combining fitness models with a novel, distributional Price equation revealed that these changes are increasingly driven by phenotypic plasticity, not selection or genetic drift, and may yet be reversible.

evolutionary biology↗

Postnatal developmental temperature affects the ontogeny of heat- and cold tolerance

Thermoregulatory precision is key to maintaining fitness in thermally unstable environments. Previous research found that development in the warmth renders birds better able to handle mild heat stress, while cold postnatal development gives no apparent benefit upon mild cold exposure. It is still not known how developmental temperature affects maximal heat tolerance limits, or if there is a physiological trade-off between heat and cold tolerance. We investigated how postnatal developmental under simulated cold snap- or heatwave-like conditions from hatching until reproductive maturity impacted the ontogeny of maximal heat- and cold tolerance in Japanese quail (Coturnix japonica). To study if any such effects were reversible or permanently programmed, we transferred half of each treatment group to intermediate common garden conditions once reproductive maturity was reached and repeated the measurements several weeks later. Development in heatwave-like conditions increased evaporative water loss rate and moved heat tolerance limits upwards, whereas cold snap-like development rendered more thermogenic birds with improved cold tolerance limits. However, we found no evidence for a trade-off between thermogenic performance and evaporative cooling capacity. The common garden birds converged in nearly all thermoregulatory traits at the end of the study, suggesting that the prior emergence of temperature-dependent phenotypes reflected reversible plasticity. We suggest that improved temperature tolerance limits improve performance in matched thermal conditions, reducing the rate at which thermal injury accrues. Yet, in the short term, we found markedly lower capacity to acclimate heat tolerance compared to cold tolerance, with possible implications for life in a warming world.

ecology↗

Climate-driven increase in transmission of wildlife malaria parasite over the last quarter century

Climate warming is expected to influence the prevalence of vector-transmitted parasites. Understanding the extent to which this is ongoing, or has already occurred, requires empirical data from populations monitored over long periods of time, but these studies are sparse. Further, vector-disease research involving human health is often influenced by disease control efforts that supersede natural trends. By screening for malaria parasite infections in a wildlife population of blue tits (Cyanistes caeruleus) in Northern Europe, over a 26-year period, we tested whether observed prevalence and transmission changes were climate-driven and show that all three malaria parasite genera have increased significantly in their prevalence and transmission over time. The most common parasite in the study, Haemoproteus majoris, increased in prevalence from 47% (1996) to 92% (2021), and this is a direct consequence of warmer temperatures elevating transmission. Climate window analyses reveal that elevated temperatures between May 9th and June 24th, a time period that overlaps with the host nestling period, are strongly positively correlated with H. majoris transmission in one-year-old birds. Warmer climate during this narrow timeframe has a demonstrable impact on parasite transmission, and this permeates into the overall prevalence in the host population. We now have empirical support that climate warming can drive a rapid rise in vector-transmitted parasites, and this has implications for other host-parasite systems. Given that we now know the exact time of year when climate warming is most influential on a common vector-transmitted parasite in this system, it is possible to investigate the evolutionary and environmental mechanisms that underly how these infections ultimately manifest. While more challenging to measure, similar implications of climate warming on human vector-disease systems might be occurring.

ecology↗

Single-molecule observation of multi-scale dynamic heterogeneity in the molecular bearing of the bacterial flagellum

The bacterial flagellar motor (BFM) is a protein-based rotary machine that drives bacterial motility. It comprises a stator anchored to the cell wall and a rotor in the cytoplasmic membrane, linked via the flagellar rod to the extracellular hook and filament. We describe high-speed polarization microscopy of gold nanorods attached to the hook, allowing unprecedented continuous recording of single BFMs with [~]0.5{degrees} resolution at 250 kHz for tens of minutes. The angular distribution of actively rotating motors exhibited multiple periodicities that are consistent with structure of the bearing between the rod and LP-ring. We observed passive diffusional rotation of this bearing, revealing complex dynamics at odds with the expected classical Ornstein-Uhlenbeck process in a smooth potential. Resolved transitions between the main 26-fold bearing states exhibited highly non-Poissonian kinetics spanning four orders of magnitude in timescale. Using the average transition times, we estimated the interaction barrier in the bearing to be close to 13 kBT, suggesting that the previously estimated torque generated by a single stator unit is just sufficient to overcome this barrier. At sub-millisecond timescales we observed anomalous ultra-slow diffusion typically associated with multi-scale disordered systems, despite the ordered crystalline atomic structure of the bearing revealed by cryo-Electron Microscopy. Over longer periods, we observed dynamic shifts in the preferred angular positions, indicating that the motors potential energy landscape evolves over time. We speculate that these newly discovered rich dynamics may be a universal feature of protein machines.

biophysics↗

Insertion of fluorescent proteins near the plug domain of MotB generates functional stator complex.

Many bacteria swim by the rotation of the bacterial flagellar motor (BFM). The BFM is powered by proton translocation across the inner membrane through the hetero-heptameric MotA5MotB2 protein complex. Two periplasmic domains of MotB are critical in activating BFM rotation: (1) the peptidoglycan binding (PGB) domain that anchors MotB in the peptidoglycan layer and (2) the plug domain that modulates the proton flow. Existing cytoplasmic fluorescent probes have been shown to negatively affect motor rotation and switching. Here we inserted a fluorescent probe in the periplasm near the plug of MotB in an attempt to circumvent issues with cytoplasmic probes and for possible use in observing the mechanism of plug-based regulation of proton flow. We inserted green fluorescent protein (GFP) and iLOV, a fluorescent version of the light-oxygen-voltage (LOV) domain, in four periplasmic locations in MotB. Insertions near the plug retained motility but showed limited fluorescence for both fluorophores. Additional short, flexible glycine-serine (GS) linkers improved motility but did not improve brightness. Further optimization is necessary to improve the fluorescence of these periplasmic probes.

microbiology↗

Development in the cold renders bird mitochondria more susceptible to heat stress

Research on birds suggests that extreme weather events during development may have long-lasting consequences on form and function. The underlying cellular mechanisms mediating such phenotypic effects are poorly studied. We raised Japanese quail in warm (30{degrees}C) or cold (10{degrees}C) temperatures from hatching until adulthood, and then measured mitochondrial metabolism in intact blood cells at representative normothermic body temperature (41{degrees}C) and a hyperthermic temperature (45{degrees}C) that quail commonly attain when heat stressed. To investigate whether any developmental effects were reversible, half of the cold- and warm-acclimated birds were assigned to a common garden (20{degrees}C) 3 weeks before the measurements. Across groups, hyperthermia was associated with increased proton leak, but decreases in both phosphorylating respiration (where ATP is produced) and working capacity of the mitochondria. Cold-acclimated birds were more strongly affected by heat stress: the increase in proton leak was 1.6-fold higher, and the decrease in phosphorylating capacity during endogenous respiration was 1.7-fold greater, compared to warm-acclimated birds. These differences did not remain in the common-garden birds. Our study suggests that developmental cold acclimation is traded off against heat tolerance at the level of cellular metabolism, with implications for our understanding of avian responses to climate change.

physiology↗

No evidence that shrinking and shapeshifting meaningfully affect how birds respond to warming and cooling

Across the globe, birds and mammals are becoming smaller and longer-limbed. Although the cause of these changes is unclear, many argue that each provide thermoregulatory benefits in a warmer world by easing heat dissipation. Here, we show that neither body size nor limb length in a model species (the Japanese quail) influenced metabolic costs of warming during a cold challenge. In the heat, larger body sizes increased metabolic costs of thermoregulation, however, this effect was moderate and almost always negated by cooling from the limbs (>97% of cases). Rearing in the warmth (30{degrees}C) relative to the cold (10{degrees}C) reduced body sizes and increased limb lengths at adulthood but thermoregulatory benefits of these changes in later heat exposures were absent. Our findings demonstrate that shrinking and shape-shifting are unlikely to ease thermoregulation in contemporary birds or reflect selection for such. Alternative contributors, including neutral or non-adaptive plasticity, should be further investigated. TeaserUsing experimental data, we show for the first time that shrinking and shape-shifting - which has been described as the third general response to climate change in animals - does not inherently provide thermoregulatory benefits to birds in a warming world. Further research evaluating the drivers of shape-shifts (including neutral plasticity and temporal reductions in resource abundance) is needed before we can determine why animals shrink under climate change.

physiology↗

Seasonal and environmental factors contribute to the variation in the gut microbiome: a large-scale study of a small bird

Environmental variation can shape the gut microbiome, but majority of studies use captive-bred species, while data on large-scale variation in the gut microbiome and the associated environmental factors is lacking. Furthermore, previous studies have limited taxonomical coverage, and for example knowledge about avian gut microbiomes is still scarce. We investigated large-scale environmental variation in the gut microbiome of wild adult great tits across the species European distribution range. Our results show that gut microbiome diversity is higher during winter and that there are compositional differences between winter and summer gut microbiomes. During winter, individuals inhabiting mixed forest habitat show higher gut microbiome diversity, whereas there was no similar association during summer. Also, temperature was found to be a small contributor to compositional differences in the gut microbiome. We did not find significant differences in the gut microbiome among populations, nor any association between latitude, rainfall, and the gut microbiome. The results suggest that there is a seasonal change in wild avian gut microbiomes, but that there are still many unknown factors that shape the gut microbiome of wild bird populations.

ecology↗

Using metabolic data to uncover the ontogeny of endothermy in an altricial bird

Altricial songbirds transform themselves from naked poikilotherms to fully-feathered endothermic homeotherms over a matter of weeks from hatching to fledging. The timing of development of endothermy has been studied in altricial birds for over half a century. However, the potential determinants, constraints, and flexibility of the onset of endothermy are not yet fully understood. We experimentally investigated whether brood size influences the ontogeny of endothermic heat production in 4-8 day-old nestling blue tits (Cyanistes caeruleus) in southern Sweden. We found that both nestlings capacity to produce heat and the proportion of nestlings exhibiting a metabolic response to a cooling challenge (15 {degrees}C for 15 min) increased with age. However, we did not find an effect of brood size on the ontogeny of endothermy and this may be explained by the lack of differences in body mass of nestlings in enlarged and reduced broods in our study. The metabolic response in all age groups was brief and not sufficient to sustain a stable body temperature. Our study shows that the development and use of endothermy is present at an early age in nestling blue tits, but further study is needed to disentangle the factors contributing to individual variation in the timing of these developments. This will serve to improve our understanding of a developmental milestone of cold tolerance in birds in the temperate zone that not only face warmer average temperatures, but also increasingly frequent cold snaps and extreme weather. Summary StatementThis study serves to improve our understanding of the ontogeny of endothermy in altricial birds while examining the potential role of brood size in the timing thereof.

ecology↗

Combinatorial transcription factor binding encodes cis-regulatory wiring of forebrain GABAergic neurogenesis

Transcription factors (TFs) bind combinatorially to genomic cis-regulatory elements (cREs), orchestrating transcription programs. While studies of chromatin state and chromosomal interactions have revealed dynamic neurodevelopmental cRE landscapes, parallel understanding of the underlying TF binding lags. To elucidate the combinatorial TF-cRE interactions driving mouse basal ganglia development, we integrated ChIP-seq for twelve TFs, H3K4me3-associated enhancer-promoter interactions, chromatin and transcriptional state, and transgenic enhancer assays. We identified TF-cREs modules with distinct chromatin features and enhancer activity that have complementary roles driving GABAergic neurogenesis and suppressing other developmental fates. While the majority of distal cREs were bound by one or two TFs, a small proportion were extensively bound, and these enhancers also exhibited exceptional evolutionary conservation, motif density, and complex chromosomal interactions. Our results provide new insights into how modules of combinatorial TF-cRE interactions activate and repress developmental expression programs and demonstrate the value of TF binding data in modeling gene regulatory wiring.

developmental biology↗

Permeabilization status affects the relationship between basal metabolic rate and mitochondrial respiration in great tit blood cells

Although mitochondrial respiration is believed to explain a substantial part of the variation in whole-animal basal (BMR) or resting metabolic rate (RMR), few studies have addressed the relationship between organismal and cellular metabolism and how this may vary in environments where individual demands for energy differ. We investigated the relationship between whole-individual metabolic rate, measured in temperatures ranging thermoneutrality to far below thermoneutrality, and mitochondrial respiration of intact or permeabilized blood cells in two separate studies on wild great tits (Parus major L.). Our results show that, in permeabilized cells, there are significant positive relationships between BMR or RMR and several mitochondrial traits, including phosphorylating respiration rate through both complexes I and II (i.e., OXPHOS respiration). However, surprisingly, the LEAK respiration (i.e., basal respiration that mainly counteract for proton leakage) was not related to BMR or RMR. When measurements were performed using intact blood cells, BMR was positively related to ROUTINE respiration (i.e., mitochondrial respiration on endogenous substrates) in one of the two studies, but no other mitochondrial traits could explain variation in BMR or RMR in any thermal environment. These studies seem to show that the level of activation of mitochondrial metabolism as well as the permeabilization status of blood cells play a primary role on the extent to which blood metabolism might explain variations in the whole-individual metabolic rate.

physiology↗

How do fluctuating temperatures alter the cost of development?

O_LIQuantifying how variable temperature regimes affect energy expenditure during development is crucial for understanding how future thermal regimes may impact early life survival and population persistence. C_LIO_LIDevelopmental Cost Theory (DCT) suggests that there is an optimal temperature (Topt) that minimises energy expenditure during development (the "cost of development"). Exposure to fluctuating temperatures around an average of Topt are anticipated to increase either development time or metabolic rate. As a result, embryos will rapidly deplete yolk reserves, and consequently hatch at a smaller size or with less residual yolk to support postnatal survival and growth. C_LIO_LIHere, we studied total embryonic energy expenditure (development time and rate of CO2 production) and conversion of yolk into tissue in common wall lizards (Podarcis muralis) under three incubation treatments anticipated, based on DCT, to increase the cost of development: no variance (Topt constant, 24 {degrees}C), low variance (22 - 26 {degrees}C), and high variance (18 - 30 {degrees}C). C_LIO_LIAs predicted, we found that increasing variance around Topt increased the cost of development, despite reducing time to hatching. As a consequence, embryos on average hatched with 59% lower residual yolk reserves under high variance versus constant incubation temperatures. C_LIO_LIOur results highlight how the relative temperature sensitivities of development time and metabolic rate determine the cost of development, which in turn may predict the ability of egg-laying ectotherms to persist in variable environments. We show that DCT can provide a mechanistic framework for understanding the widespread, but often seemingly idiosyncratic, effects of fluctuating incubation temperatures on hatchling tissue and residual yolk mass. C_LI

physiology↗

Thermoregulatory consequences of growing up during a heatwave

Changes in environmental temperature during the developmental period can affect growth, metabolism, and temperature tolerance of the offspring. We know little about whether such changes remain to adulthood, which is important to understand the links between climate change, development, and fitness. We investigated if phenotypic consequences of the thermal environment in early life remained in adulthood in two studies on Japanese quail (Coturnix japonica). Birds were raised under simulated heatwave-, cold snap-or control conditions, from hatching until halfway through the growth period, and then in a common garden until reproductively mature. We measured biometric and thermoregulatory (metabolic heat production [MHP], evaporative water and heat loss [EWL, EHL] and body temperature) responses to variation in submaximal air temperature at the end of the thermal acclimation period and in adulthood. Warm birds had lower MHP than control birds at the end of the thermal acclimation period and, in the warmest temperature studied (40{degrees}C), also had higher evaporative cooling capacity compared to controls. No analogous responses were recorded in cold birds, though they had higher EWL than controls in all but the highest test temperature. None of the effects found at the end of the heatwave-or cold snap period remained until adulthood. This implies that chicks exposed to higher temperatures could be more prepared to counter heat stress as juveniles, but that they do not enjoy any advantages of such developmental conditions when facing high temperatures as adults. Conversely, cold temperature does not seem to confer any priming effects in adolescence.

physiology↗

Population divergence in maternal investment and embryo energy use and allocation reveals adaptive responses to cool climates

The thermal sensitivity of early life stages can play a fundamental role in constraining species distribution. For egg-laying ectotherms, cool temperatures often extend development time and exacerbate developmental energy cost. Despite these costs, egg laying is still observed at high latitudes and altitudes. How embryos overcome the developmental constraints posed by cool climates is crucial knowledge for explaining the persistence of oviparous species in such environments and for understanding thermal adaptation more broadly. Here, we studied maternal investment, and embryo energy use and allocation in wall lizards spanning altitudinal regions, as potential mechanisms of local adaptation to development in cool climates. Specifically, we compared population-level differences in (1) investment from mothers (egg mass, embryo retention and thyroid yolk hormone concentration), (2) embryo energy expenditure during development, and (3) embryo energy allocation from yolk towards tissue. We found evidence that energy expenditure was greater under cool compared with warm incubation temperatures. Females from relatively cool regions did not compensate for this energetic cost of development by producing larger eggs or increasing thyroid hormone concentration in yolk. Instead, embryos from the high-altitude region used less energy to complete development, i.e., they developed faster without a concomitant increase in metabolic rate, compared with those from the low-altitude region. Embryos from high altitudes also allocated relatively more energy towards tissue production, hatching with lower residual yolk:tissue ratios than low-altitude region embryos. These results suggest that local adaptation to cool climate in wall lizards involves mechanisms that regulate embryonic utilisation of yolk reserves and its allocation towards tissue, rather than shifts in maternal investment of yolk content or composition.

evolutionary biology↗