Search

The scarcity of asexual reproduction in vertebrates alludes to an inherent cost. Several groups of asexual vertebrates exhibit lower endurance capacity (a trait predominantly sourced by mitochondrial respiration) compared with congeneric sexual species. Here we measure endurance capacity in five species of

Erythrocyte enucleation is thought to have evolved in mammals to support their energetic cost of high metabolic activities. However, birds face similar selection pressure yet possess nucleated erythrocytes. Current hypotheses on the mammalian erythrocyte enucleation claim that the absence of cell organelles allows erythrocytes to 1) pack more hemoglobin into the cells to increase oxygen carrying capacity and 2) decrease erythrocyte size for increased surface area-to-volume ratio, and improved ability to traverse small capillaries. In this article, we first empirically tested current hypotheses using both conventional and phylogenetically informed analysis comparing literature values of mean cell hemoglobin concentration (MCHC) and mean cell volume (MCV) between 181 avian and 194 mammalian species. We found no difference in MCHC levels between birds and mammals using both conventional and phylogenetically corrected analysis. MCV was higher in birds than mammals according to conventional analysis, but the difference was lost when we controlled for phylogeny. These results suggested that avian and mammalian erythrocytes may employ different strategies to solve a common problem. To further investigate existing hypotheses or develop new hypothesis, we need to understand the functions of various organelles in avian erythrocytes. Consequently, we covered potential physiological functions of various cell organelles in avian erythrocytes based on current knowledge, while making explicit comparisons with their mammalian counterparts. Finally, we proposed by taking an integrative and comparative approach, using tools from molecular biology to evolutionary biology, would allow us to better understand the fundamental physiological functions of various components of avian and mammalian erythrocytes.

Reproduction and environmental stressors are generally thought to be associated with a cost to the individual experiencing them, but the physiological mechanisms mediating costs of reproduction and maternal effects remain poorly understood. Studies examining the effects of environmental stressors on a female's physiological state and body condition during reproduction, as well as physiological condition of offspring, have yielded equivocal results. Mitochondrial physiology and oxidative stress have been implicated as important mediators of life-history trade-offs. The goal of this investigation was to uncover the physiological mechanisms responsible for the enhanced trade-off between self-maintenance and offspring investment when an animal is exposed to stressful conditions during reproduction. To that end, we manipulated circulating corticosterone (CORT) levels by orally supplementing lactating female mice with CORT and investigated mitochondrial physiology and oxidative stress of both the reproductive females and their young. We found that maternal CORT exposure resulted in lower litter mass at weaning, but mitochondrial performance and oxidative status of females were not impacted. We also found potential beneficial effects of maternal CORT on mitochondrial function (e.g. higher respiratory control ratio) and oxidative stress (e.g. lower reactive oxygen species production) of offspring in adulthood, suggesting that elevated maternal CORT may be a signal for early-life adversity and prepare the organism with a predictive, adaptive response for future stressors.

Considerable progress has been made in understanding the physiological basis for variation in the life-history patterns of animals, particularly with regard to the roles of oxidative stress and hormonal regulation. However, an underappreciated and understudied area that could play a role in mediating inter- and intraspecific variation of life history is endoplasmic reticulum (ER) stress, and the resulting unfolded protein response (UPRER ). ER stress response and the UPRER maintain proteostasis in cells by reducing the intracellular load of secretory proteins and enhancing protein folding capacity or initiating apoptosis in cells that cannot recover. Proper modulation of the ER stress response and execution of the UPRER allow animals to respond to intracellular and extracellular stressors and adapt to constantly changing environments. ER stress responses are heritable and there is considerable individual variation in UPRER phenotype in animals, suggesting that ER stress and UPRER phenotype can be subjected to natural selection. The variation in UPRER phenotype presumably reflects the way animals respond to ER stress and environmental challenges. Most of what we know about ER stress and the UPRER in animals has either come from biomedical studies using cell culture or from experiments involving conventional laboratory or agriculturally important models that exhibit limited genetic diversity. Furthermore, these studies involve the assessment of experimentally induced qualitative changes in gene expression as opposed to the quantitative variations that occur in naturally existing populations. Almost all of these studies were conducted in controlled settings that are often quite different from the conditions animals experience in nature. Herein, we review studies that investigated ER stress and the UPRER in relation to key life-history traits including growth and development, reproduction, bioenergetics and physical performance, and ageing and senescence. We then ask if these studies can inform us about the role of ER stress and the UPRER in mediating the aforementioned life-history traits in free-living animals. We propose that there is a need to conduct experiments pertaining to ER stress and the UPRER in ecologically relevant settings, to characterize variation in ER stress and the UPRER in free-living animals, and to relate the observed variation to key life-history traits. We urge others to integrate multiple physiological systems and investigate how interactions between ER stress and oxidative stress shape life-history trade-offs in free-living animals.

The life-history patterns that animals display are a product of their ability to maximize reproductive performance while concurrently balancing numerous metabolic demands. For example, the energetic costs of reproduction may reduce an animal's ability to support self-maintenance and longevity. In this work, we evaluated the impact of parity on mitochondrial physiology in laboratory mice. The theory of mitohormesis suggests that modest exposure to reactive oxygen species can improve performance, while high levels of exposure are damaging. Following this theory, we hypothesized that females that experienced one bout of reproduction (primiparous) would display improved mitochondrial capacity and reduced oxidative damage relative to non-reproductive (nulliparous) mice, while females that had four reproductive events (multiparous) would have lower mitochondrial performance and greater oxidative damage than both nulliparous and primiparous females. We observed that multiple reproductive events enhanced the mitochondrial respiratory capacity of liver mitochondria in females with high body mass. Four-bout females showed a positive relationship between body mass and mitochondrial capacity. In contrast, non-reproductive females showed a negative relationship between body mass and mitochondrial capacity and primiparous females had a slope that did not differ from zero. Other measured variables, too, were highly dependent on body mass, suggesting that a female's body condition has strong impacts on mitochondrial physiology. We also evaluated the relationship between how much females allocated to reproduction (cumulative mass of all young weaned) and mitochondrial function and oxidative stress in the multiparous females. We found that females that allocated more to reproduction had lower basal respiration (state 4), lower mitochondrial density, and higher protein oxidation in liver mitochondria than females that allocated less. These results suggest that, at least through their first four reproductive events, female laboratory mice may experience bioenergetic benefits from reproduction but only those females that allocated the most to reproduction appear to experience a potential cost of reproduction.

Mitochondrial energetics is a central theme in animal biochemistry and physiology, with researchers using mitochondrial respiration as a metric to investigate metabolic capability. To obtain the measures of mitochondrial respiration, fresh biological samples must be used, and the entire laboratory procedure must be completed within approximately 2 h. Furthermore, multiple pieces of specialized equipment are required to perform these laboratory assays. This creates a challenge for measuring mitochondrial respiration in the tissues of wild animals living far from physiology laboratories as live tissue cannot be preserved for very long after collection in the field. Moreover, transporting live animals over long distances induces stress, which can alter mitochondrial energetics. This manuscript introduces the Auburn University (AU) MitoMobile, a mobile mitochondrial physiology laboratory that can be taken into the field and used on-site to measure mitochondrial metabolism in tissues collected from wild animals. The basic features of the mobile laboratory and the step-by-step methods for measuring isolated mitochondrial respiration rates are presented. Additionally, the data presented validate the success of outfitting the mobile mitochondrial physiology laboratory and making mitochondrial respiration measurements. The novelty of the mobile laboratory lies in the ability to drive to the field and perform mitochondrial measurements on the tissues of animals captured on site.

Naked mole-rats (NMR) and Damaraland mole-rats (DMR) are the only two eusocial mammals known. Both species exhibit extraordinary longevity for their body size, high tolerance to hypoxia and oxidative stress and high reproductive output; these collectively defy the concept that all life-history traits should be negatively correlated. However, when life-history traits share similar underpinning physiological mechanisms, these may be positively associated with each other. Here, we propose that the bioenergetic properties of mole-rats share a potential common mechanism. We adopted a top-down perspective measuring the bioenergetic properties at the organismal, cellular, and molecular level in both species and the biological significance of these properties were compared with the same measures in Siberian hamsters and C57BL/6 mice, chosen for their similar body size to the mole-rat species. We found mole-rats shared several bioenergetic properties that differed from their comparator species, including low basal metabolic rates, a high dependence on glycolysis rather than on oxidative phosphorylation for ATP production, and low proton conductance across the mitochondrial inner membrane. These shared mole-rat features could be a result of evolutionary adaptation to tolerating variable oxygen atmospheres, in particular hypoxia, and may in turn be one of the molecular mechanisms underlying their extremely long lifespans.

Ecological traits related to pace of life, such as foraging strategies and activity levels, influence daily energy expenditure (DEE) and can affect fitness. A fast pace of life tends to be supported by high-energy aerobic activity and is positively correlated with high DEE and basal and maximal metabolic rates in some endotherms. Given that maximal capacities for exercise and thermogenesis are both functions of aerobic muscle output and are often positively correlated with each other, high-energy aerobic lifestyles might be associated with high aerobic capacities, which would be expected to produce high thermogenic capacities as a side effect. We tested whether the high-energy aerial insectivore lifestyle in swallows is correlated with elevated basal and maximal thermogenic metabolic rates. We measured basal (BMR) and summit (Msum = maximum cold-induced metabolic rate) metabolic rates in 6 species of swallows (Hirundinidae) and combined these data with literature data for additional swallows (n = 10 for BMR; n = 8 for Msum) and non-aerial insectivore birds (n = 215 for BMR; n = 64 for Msum) to address the hypothesis that swallows have higher BMR and Msum than non-aerial insectivores. BMR in swallows was significantly higher than for non-aerial insectivore birds for phylogenetically adjusted analyses after correcting for body mass and region of origin (tropical vs. temperate). In contrast, Msum did not differ significantly between swallows and non-aerial insectivores. Thermogenic scope (Msum – BMR), however, was lower in tropical non-aerial insectivore birds compared with tropical swallows and temperate birds. This suggests that the aerial insectivore lifestyle elevates maintenance costs, but maximum thermogenic capacities are not clearly upregulated, despite tropical swallows having higher thermogenic scope than tropical non-aerial insectivores. These data suggest that the high-energy aerial insectivore lifestyle does not produce strong thermogenic side effects in swallows.LAY SUMMARYAnimals have different lifestyles or paces of life that influence the amount of energy used per day.Swallows are aerial insectivores and have an active lifestyle that could lead to higher metabolic capacities at both basal and maximal levels.We measured basal and maximum cold-induced metabolic rates in swallows and compared these with non-aerial insectivore birds to test if swallows have higher basal and maximum metabolic capacities.We found that swallows have higher basal metabolic rates but not maximum cold-induced metabolic rates compared with other non-aerial insectivore birds.The results suggest that the active lifestyle of swallows required more energy for maintenance but did not produce high thermogenic capacities as a byproduct.

Foraging at elevated rates to provision offspring is thought to be an energetically costly activity and it has been suggested that there are physiological costs associated with the high workload involved. However, for the most part, evidence for costs of increased foraging and/or reproductive effort is weak. Furthermore, despite some experimental evidence demonstrating negative effects of increased foraging and parental effort, the physiological mechanisms underlying costs associated with high workload remain poorly understood. To examine how high workload affects haematology, oxidative stress and reproductive output, we experimentally manipulated foraging effort in captive zebra finches, Taeniopygia guttata, using a previously described technique, and allowed individuals to breed first in low foraging effort conditions and then in high foraging effort conditions. We found that birds upregulated haematocrit and haemoglobin concentration in response to training. Birds subjected to increased workload during reproduction had lower fecundity, although final reproductive output was not significantly different than that of controls. Offspring of parents subjected to high workload during reproduction also had higher oxidative stress when they were 90 days of age. Total antioxidant capacity and reactive oxygen metabolites of birds responded differently in the two breeding attempts, but we did detect an overall increase in oxidative stress in response to training in either attempt, which could explain the lower fecundity observed in birds subjected to increased workload during reproduction.

Free-living animals often engage in behaviour that involves high rates of workload and results in high daily energy expenditure (DEE), such as reproduction. However, the evidence for elevated DEE accompanying reproduction remains equivocal. In fact, many studies have found no difference in DEE between reproducing and non-reproducing females. One of the hypotheses explaining the lack of difference is the concept of an ‘energetic ceiling’. However, it is unclear whether the lack of increase in energy expenditure is due to the existence of an energetic ceiling and/or compensation by males during parental care. To investigate whether an energetic ceiling exists, we experimentally manipulated foraging effort in captive zebra finches, Taeniopygia guttata, creating two groups with high and low foraging efforts followed by both groups breeding in the low foraging effort common garden condition. DEE was measured in both sexes throughout the experiment. We show sex-specific energy management strategies in response to training for increased foraging effort prior to reproduction. Specifically, males and females responded differently to the high foraging effort treatment and subsequently to chick rearing in terms of energy expenditure. Our results also suggest that there is an energetic ceiling in females and that energetic costs incurred prior to reproduction can be carried over into subsequent stages of reproduction in a sex-specific manner.

The zebra finch is a common model organism in neuroscience, endocrinology, and ethology. Zebra finches are generally considered opportunistic breeders, but the extent of their opportunism depends on the predictability of their habitat. This plasticity in the timing of breeding raises the question of how domestication, a process that increases environmental predictability, has affected their reproductive physiology. Here, we compared circulating steroid levels in various "strains" of zebra finches. In Study 1, using radioimmunoassay, we examined circulating testosterone levels in several strains of zebra finches (males and females). Subjects were wild or captive (Captive Wild-Caught, Wild-Derived, or Domesticated). In Study 2, using liquid chromatography-tandem mass spectrometry (LC-MS/MS), we examined circulating sex steroid profiles in wild and domesticated zebra finches (males and females). In Study 1, circulating testosterone levels in males differed across strains. In Study 2, six steroids were detectable in plasma from wild zebra finches (pregnenolone, progesterone, dehydroepiandrosterone (DHEA), testosterone, androsterone, and 5α-dihydrotestosterone (5α-DHT)). Only pregnenolone and progesterone levels changed across reproductive states in wild finches. Compared to wild zebra finches, domesticated zebra finches had elevated levels of circulating pregnenolone, progesterone, DHEA, testosterone, androstenedione, and androsterone. These data suggest that domestication has profoundly altered the endocrinology of this common model organism. These results have implications for interpreting studies of domesticated zebra finches, as well as studies of other domesticated species.

The life-history patterns that animals display are a product of their ability to maximize reproductive performance while concurrently balancing numerous metabolic demands. For example, the energetic costs of reproduction may reduce an animal's ability to support self-maintenance and longevity. In this work, we evaluated the impact of parity on mitochondrial physiology in laboratory mice. The theory of mitohormesis suggests that modest exposure to reactive oxygen species can improve performance, while high levels of exposure are damaging. Following this theory, we hypothesized that females that experienced one bout of reproduction (primiparous) would display improved mitochondrial capacity and reduced oxidative damage relative to non-reproductive (nulliparous) mice, while females that had four reproductive events (multiparous) would have lower mitochondrial performance and greater oxidative damage than both nulliparous and primiparous females. We observed that multiple reproductive events enhanced the mitochondrial respiratory capacity of liver mitochondria in females with high body mass. Four-bout females showed a positive relationship between body mass and mitochondrial capacity. In contrast, non-reproductive females showed a negative relationship between body mass and mitochondrial capacity and primiparous females had a slope that did not differ from zero. Other measured variables, too, were highly dependent on body mass, suggesting that a female's body condition has strong impacts on mitochondrial physiology. We also evaluated the relationship between how much females allocated to reproduction (cumulative mass of all young weaned) and mitochondrial function and oxidative stress in the multiparous females. We found that females that allocated more to reproduction had lower basal respiration (state 4), lower mitochondrial density, and higher protein oxidation in liver mitochondria than females that allocated less. These results suggest that, at least through their first four reproductive events, female laboratory mice may experience bioenergetic benefits from reproduction but only those females that allocated the most to reproduction appear to experience a potential cost of reproduction.

An animal's pace of life is mediated by the physiological demands and stressors it experiences (e.g., reproduction) and one likely mechanism that underlies these effects is oxidative stress. Reproduction has been shown to increase or reduce oxidative stress under different conditions and modify mitochondrial performance. We hypothesized that the changes associated with reproduction can alter how animals respond to future oxidative stressors. We tested this theory by comparing the organ-specific mitochondrial response in female wild-derived house mice. Specifically, we compared mice that reproduced or were virgins to mice that were exposed to an oxidant (i.e., radiation) or not-exposed to radiation. We measured liver and skeletal muscle mitochondrial density, respiratory performance, enzyme activity, and oxidant production, as well as markers of oxidative damage to tissues. In the liver, prior reproduction prevented a radiation-induced reduction in mitochondrial density and increased mitochondrial respiratory performance. In skeletal muscle, prior reproduction resulted in a radiation-induced decline in mitochondrial density which could reduce the bioenergetic capacity of skeletal muscle mitochondria. Yet, electron transport chain complex I activity in skeletal muscle, which dropped with reproduction, returned to control levels following oxidant exposure. The results of this investigation indicate that prior reproduction alters the response of mitochondria to an oxidative challenge in an organ-specific manner. Such changes could have differential effects on future reproductive performance and risk of death.

Aerobic capacity is assumed to be a main predictor of workload ability and haematocrit (Hct) and haemoglobin (Hb) have been suggested as key determinants of aerobic performance. Intraspecific studies have reported increases in Hct and Hb in response to increased workload. Furthermore, Hct and Hb vary markedly among individuals and throughout the annual cycle in free-living birds and it has been suggested that this variation reflects adaptive modulation of these traits to meet seasonal changes in energy demands. We used a comparative dataset of haematological traits, measures of metabolic rate (57 species), and life-history traits (160 species) to test several hypotheses for adaptive variation in haematology in relation to migration and altitude. We then extended these general ideas to test relationships between Hct and basal metabolic rate, daily energy expenditure and activity energy expenditure, using the 57 species that we have metabolic rate information for. We found that at the interspecific level, full migrants have higher Hct and Hb than partial migrants and non-migrants, and that altitude is positively correlated with Hb but not Hct. Hct is positively associated with activity energy expenditure (energy spent specifically on costly activities), suggesting that haematological traits could be adaptively modulated based on life-history traits and that Hct is a potential physiological mediator of energetic constraint.

Skeletal muscle remodeling is an important component of phenotypic flexibility in birds and impacts organismal metabolism and performance, which could potentially influence fitness. One regulator of skeletal muscle remodeling is myostatin, an autocrine/paracrine muscle growth inhibitor that may be down-regulated under conditions promoting heavier muscle masses. In this study, we employed protocols requiring hovering while foraging to increase foraging costs and modify phenotypes of zebra finches (Taeniopygia guttata). We examined the effects of high-cost foraging (HF) on skeletal muscle masses and used real-time reverse-transcription polymerase chain reaction and Western blots to measure gene and protein expression of myostatin and its metalloproteinase activators tolloid-like proteases TLL-1 and TLL-2 in pectoralis muscle. Female finches average shorter wings and higher wing loading than males, so increased flight costs might be expected to disproportionately affect females. Indeed, HF female finches exhibited reduced total fat masses, increased pectoralis muscle masses, and lower myostatin protein levels than controls. Male finches showed no significant differences in pectoralis muscle masses or myostatin protein levels between HF and control birds. Myostatin, TLL-1, and TLL-2 messenger RNA (mRNA) expression remained stable between treatments for both female and male finches. Myostatin mRNA and protein levels showed variable directions of correlations with pectoralis mass residuals among treatments. Thus, these data offer only mixed support for a regulatory role for myostatin in mediating the flexibility of pectoralis muscle phenotypes of small birds.

SYNOPSIS Many behaviors crucial for survival and reproductive success in free-living animals, including migration, foraging, and escaping from predators, involve elevated levels of physical activity. However, although there has been considerable interest in the physiological and biomechanical mechanisms that underpin individual variation in exercise performance, to date, much work on the physiology of exercise has been conducted in laboratory settings that are often quite removed from the animal's ecology. Here we review current, laboratory-based model systems for exercise (wind or swim tunnels for migration studies in birds and fishes, manipulation of exercise associated with non-migratory activity in birds, locomotion in lizards, and wheel running in rodents) to identify common physiological markers of individual variation in exercise capacity and/or costs of increased activity. Secondly, we consider how physiological responses to exercise might be influenced by (1) the nature of the activity (i.e., voluntary or involuntary, intensity, and duration), and (2) resource acquisition and food availability, in the context of routine activities in free-living animals. Finally, we consider evidence that the physiological effects of experimentally-elevated activity directly affect components of fitness such as reproduction and survival. We suggest that developing more ecologically realistic laboratory systems, incorporating resource-acquisition, functional studies across multiple physiological systems, and a life-history framework, with reproduction and survival end-points, will help reveal the mechanisms underlying the consequences of exercise, and will complement studies in free-living animals taking advantage of new developments in wildlife-tracking.

International audience; Monogamous pair bonds can be transient or long-lasting, which varies across species. The neuroendocrine mechanisms regulating pair maintenance behaviours are largely unknown, yet fundamental to our understanding of monogamy. Furthermore, the expression and regulation of pair maintenance behaviour is likely to be greatly influenced by social and environmental contexts. Our previous research suggested that androgens might regulate long-term pair maintenance behaviour in the monogamous zebra finch, Taeniopygia guttata. Here, we tested the hypothesis that testosterone treatment to males affects long-term pair maintenance behaviour in zebra finches. Established pairs were randomly assigned to one of two groups: control (N = 8) or testosterone (N = 7). Males were given either an empty or a testosterone-filled Silastic implant. Physical and acoustic affiliative behaviours and plasma testosterone levels were examined at three time points: pre-implantation, 30 days post-implant and 60 days post-implant. Importantly, we examined affiliative behaviours under two contexts: in the home cage (baseline) and following a brief chase (post stressor). Male testosterone treatment had no effects on behaviour during the baseline period, but significantly affected behaviours during the post stressor period. Specifically, testosterone-treated males spent less time in close proximity to their partner and sang more. To our knowledge, this is the first report of a context-dependent effect in the neuroendocrine regulation of pair maintenance behaviour, as well as the first report of an inhibitory effect of testosterone on zebra finch pairing behaviours. These results raise interesting questions about the function of affiliative behaviours in established pair bonds.

Here, we studied the life-long monogamous zebra finch, to examine the relationship between circulating sex steroid profiles and pair-maintenance behavior in pairs of wild-caught zebra finches (paired in the laboratory for >1 month). We used liquid chromatography-tandem mass spectrometry to examine a total of eight androgens and progestins [pregnenolone, progesterone, dehydroepiandrosterone (DHEA), androstenediol, pregnan-3,17-diol-20-one, androsterone, androstanediol, and testosterone]. In the plasma, only pregnenolone, progesterone, DHEA, and testosterone were above the limit of quantification. Sex steroid profiles were similar between males and females, with only circulating progesterone levels significantly different between the sexes (female > male). Circulating pregnenolone levels were high in both sexes, suggesting that pregnenolone might serve as a circulating prohormone for local steroid synthesis in zebra finches. Furthermore, circulating testosterone levels were extremely low in both sexes. Additionally, we found no correlations between circulating steroid levels and pair-maintenance behavior. Taken together, our data raise several interesting questions about the neuroendocrinology of zebra finches.

Zebra finches are highly social songbirds that maintain life-long monogamous pair-bonds. They rely heavily upon these pair-bonds to survive their ever-changing and unpredictable habitat in the Australian desert. These pair-bonds are maintained via a large repertoire of affiliative behaviors that for most of an individual’s life are predominately associated with pair maintenance. Water restriction reduces circulating testosterone levels in male zebra finches and the size of the ovary and oviduct in female zebra finches, but water restriction has little or no effects on pair-maintenance behaviors and local levels of testosterone and estradiol in behaviorally-relevant brain regions. These data suggest that in water-restricted zebra finches, local synthesis of testosterone and estradiol in the brain may support the expression of pair-maintenance behaviors. Here, we directly test whether pair-maintenance behaviors are regulated by estradiol, acting via non-genomic or genomic mechanisms, in water-restricted (i.e., non-breeding) zebra finches. In two experiments, subjects were treated with an aromatase inhibitor (fadrozole) either acutely or chronically, and a variety of pair-maintenance behaviors were quantified. Additionally, we quantified the effect of acute fadrozole treatment on brain and circulating estradiol and testosterone levels. Acute fadrozole administration rapidly decreased estradiol levels in the circulation and brain of males and also rapidly increased testosterone levels in the circulation and brain of both males and females. However, neither the acute nor chronic fadrozole treatment decreased pair-maintenance behaviors. In one case, acute fadrozole treatment promoted affiliation. These data suggest that pair-maintenance behavior in non-breeding zebra finches is not promoted by estradiol acting via either non-genomic or genomic mechanisms.