Experimental Evolution of a Mammalian Holobiont? Genetic and Maternal Effects on the Cecal Microbiome in Bank Voles Selectively Bred for Herbivorous Capability.

AbstractMammalian herbivory represents a complex adaptation requiring evolutionary changes across all levels of biological organization, from molecules to morphology to behavior. Explaining the evolution of such complex traits represents a major challenge in biology, as it is simultaneously muddled and enlightened by a growing awareness of the crucial role of symbiotic associations in shaping organismal adaptations. The concept of hologenomic evolution includes the partnered unit of the holobiont, the host with its microbiome, as a selection unit that may undergo adaptation.

Dietary fatty acids and flight-training influence the expression of the eicosanoid hormone prostacyclin in songbirds.

Diet shifts can alter tissue fatty acid composition in birds, which is subsequently related to metabolic patterns. Eicosanoids, short-lived fatty acid-derived hormones, have been proposed to mediate these relationships but neither baseline concentrations nor the responses to diet and exercise have been measured in songbirds. We quantified a stable derivative of the vasodilatory eicosanoid prostacyclin in the plasma of male European Starlings (Sturnus vulgaris, N = 25) fed semisynthetic diets with either high (PUFA) or low (MUFA) amounts of n6 fatty acid precursors to prostacyclin.

Mitochondrial metabolism in blood more reliably predicts whole-animal energy needs compared to other tissues.

Understanding energy metabolism in free-ranging animals is crucial for ecological studies. In birds, red blood cells (RBCs) offer a minimally invasive method to estimate metabolic rate (MR). In this study with European starlings , we examined how RBC oxygen consumption relates to oxygen use in key tissues (brain, liver, heart, and pectoral muscle) and versus the whole organism measured at basal levels.

Repeat Sampling of Female Passerines During Reproduction Reveals Surprising Higher Plasma Oxidative Damage During Resting Compared to Active State.

Traditional models of oxidative stress predict accumulation of damage caused by reactive oxygen species (ROS) production as highly correlated with aerobic metabolism, a prediction under increasing scrutiny. Here, we repeat sampled female great tits (Parus major) at two opposite levels of energy use during the period of maximum food provisioning to nestlings, once at rest and once during activity. Our results were in contrast to the above prediction, namely significantly higher levels of oxidative damage during rest opposed to active phase.

Concerted phenotypic flexibility of avian erythrocyte size and number in response to dietary anthocyanin supplementation.

Background: Endurance flight impose substantial oxidative costs on the avian oxygen delivery system. In particular, the accumulation of irreversible damage in red blood cells can reduce the capacity of blood to transport oxygen and limit aerobic performance. Many songbirds consume large amounts of anthocyanin-rich fruit, which is hypothesized to reduce oxidative costs, enhance post-flight regeneration, and enable greater aerobic capacity.

Measurements of body temperature and oxidative stress reveal differential costs associated with humoral immune function in a passerine bird.

Eco-immunology considers resistance to antigens a costly trait for an organism, but actual quantification of such costs is not straightforward. Costs of the immune response are visible in impaired coloration and reduced growth or reproductive success. Activation of the humoral immune response is a slow, complex and long-lasting process, which makes the quantification of its energetic cost a potential losing game.

Evolution of an increased performance under acute challenge does not exacerbate vulnerability to chronic stress.

An adequate stress response plays a vital role in coping with challenges. However, if selection for improved coping with an acute challenge affects the entire stress response system, susceptibility to adverse effects of chronic stressors can be deepened. Here, we used bank voles from lines selected for high swim-induced aerobic metabolism (A) and unselected control (C), and asked if the selection affected sensitivity to chronic mild stress (CMS).

Flight training and dietary antioxidants have mixed effects on the oxidative status of multiple tissues in a female migratory songbird.

Birds, like other vertebrates, rely on a robust antioxidant system to protect themselves against oxidative imbalance caused by energy-intensive activities such as flying. Such oxidative challenges may be especially acute for females during spring migration, as they must pay the oxidative costs of flight while preparing for reproduction; however, little previous work has examined how the antioxidant system of female spring migrants responds to dietary antioxidants and the oxidative challenges of regular flying. We fed two diets to female European starlings, one supplemented with a dietary antioxidant and one without, and then flew them daily in a windtunnel for 2 weeks during the autumn and spring migration periods.

Rest-Phase Hypothermia Reveals a Link Between Aging and Oxidative Stress: A Novel Hypothesis.

In endotherms, growth, reproduction, and survival are highly depended on energy metabolism. Maintenance of constant body temperature can be challenging for endotherms under continuously changing environmental conditions, such as low or high ambient temperatures or limited food. Thus, many birds may drop body temperature below normothermic values during the night, known as rest-phase hypothermia, presumably to decrease energy metabolism.

Age-Related Changes in the Thermoregulatory Properties in Bank Voles From a Selection Experiment.

As with many physiological performance traits, the capacity of endotherms to thermoregulate declines with age. Aging compromises both the capacity to conserve or dissipate heat and the thermogenesis, which is fueled by aerobic metabolism. The rate of metabolism, however, not only determines thermogenic capacity but can also affect the process of aging.

Does selection for behavioral and physiological performance traits alter glucocorticoid responsiveness in bank voles?

One of the key elements of an animal's Darwinian fitness is its ability to adequately respond to and cope with challenging situations. Glucocorticoid hormones, such as corticosterone, affect an organism's ability to overcome such challenges. We hypothesized that changes in the glucocorticoid response curve contribute to the evolution of increased performance during challenging conditions, and tested it on bank voles () from a multidirectional artificial selection experiment, which involves lines selected for high aerobic exercise metabolism achieved during swimming (A - Aerobic), predatory behavior towards a cricket (P - Predatory) and ability to maintain body mass on a low-quality herbivorous diet (H - Herbivorous), as well as unselected control lines (C - Control).

Dietary antioxidants attenuate the endocrine stress response during long-duration flight of a migratory bird.

Glucocorticoids (GCs) are metabolic hormones that promote catabolic processes, which release stored energy and support high metabolic demands such as during prolonged flights of migrating birds. Dietary antioxidants (e.g.

Cellular Turnover: A Potential Metabolic Rate-Driven Mechanism to Mitigate Accumulation of DNA Damage.

Oxidative stress, the imbalance of reactive oxygen species and antioxidant capacity, may cause damage to biomolecules pivotal for cellular processes (e.g., DNA).

Stress coping and evolution of aerobic exercise performance: corticosterone levels in voles from a selection experiment.

The locomotor performance achieved in a challenging situation depends not only on physiological limitations, such as the aerobic exercise capacity, but also on behavioral characteristics, such as adequate coping with stress. The stress response is mediated largely by the hypothalamic-pituitary-adrenal (HPA) axis, through modulated release of glucocorticoids. We used a unique experimental evolution model system to test the hypothesis that the evolution of an increased aerobic exercise performance can be facilitated by modification of the glucocorticoid-related stress-coping mechanisms.

The effect of monoamines reuptake inhibitors on aerobic exercise performance in bank voles from a selection experiment.

Exercise performance depends on both physiological abilities (e.g., muscle strength) and behavioral characteristics (e.

Experimental evolution of personality traits: open-field exploration in bank voles from a multidirectional selection experiment.

Evolution of complex physiological adaptations could be driven by natural selection acting on behavioral traits. Consequently, animal personality traits and their correlation with physiological traits have become an engaging research area. Here, we applied a unique experimental evolution model-lines of bank voles selected for (A) high exercise-induced aerobic metabolism, (H) ability to cope with low-quality herbivorous diet, and (P) intensity of predatory behavior, that is, traits shaping evolutionary path and diversity of mammals-and asked how the selection affected the voles' personality traits, assessed in an open field test.

Is Experimental Evolution of an Increased Aerobic Exercise Performance in Bank Voles Mediated by Endocannabinoid Signaling Pathway?

Unlabelled: The level of physical activity achieved in a given situation depends on both physiological abilities and behavioral characteristics (motivation). We used a unique animal model to test a hypothesis that evolution of an increased aerobic exercise performance can be facilitated by evolution of motivation to undertake physical activity, mediated by brain endocannabinoid system. Bank voles () from "aerobic" A lines selected for 22 generations for high swim-induced aerobic metabolism (VOswim) achieved 65% higher "voluntary maximum" VOswim than voles from unselected, "control" C lines.

More than just the numbers-contrasting response of snake erythrocytes to thermal acclimation.

Acclimation to lower temperatures decreases energy expenditure in ectotherms but increases oxygen consumption in most endotherms, when dropped below thermoneutrality. Such differences should be met by adjustments in oxygen transport through blood. Changes in hematological variables in correspondence to that in metabolic rates are, however, not fully understood, particularly in non-avian reptiles.

Experimental evolution of aerobic exercise performance and hematological traits in bank voles.

The maximum rate of aerobic exercise metabolism (VOmax) is a trait informative from both medical and evolutionary perspective, and both the physiological mechanisms limiting its level and its evolution are subject to vivid debate. Both comparative analyses and studies on the effects of training or acclimation to aerobically-demanding conditions suggest a role of oxygen transport-related properties of blood in limiting VOmax. Here we used a unique experimental evolution model - lines of bank voles selected for high rate of swim-induced aerobic metabolism (VOswim; A lines), which evolved a 60% higher VOswim than that observed in unselected control lines (C) - and asked how the hematological parameters evolved in response to the selection.

Contrasting response of haematological variables between long-term training and short exercise bouts in zebra finches ().

Physical aerobic activity is oxygen demanding, but - particularly for birds - there is still little understanding of how blood contributes to oxygen supply under various activity levels. In a two-factorial experimental design, we investigated the long-term effect of daily flight training and the immediate effect of a short exercise bout on a set of haematological variables: haemoglobin (Hb) content, haematocrit (Hct), and red blood cell number (RBC) and size (RBC) in zebra finches (). For a period of 6 weeks, birds were either trained daily for 3 h in a flight arena or remained untrained.

High oxidative stress despite low energy metabolism and vice versa: Insights through temperature acclimation in an ectotherm.

Reactive oxygen species (ROS) are inescapable byproducts of energy metabolism and may cause costly damage to biomolecules. Organisms have evolved different means to counter oxidative stress, such as modulation of ROS production, neutralization of produced ROS through free radical scavenging and the repair or removal of the damaged structures. A positive relationship between metabolic rate and ROS production is commonly expected, but the oxidative burden of aerobic metabolism remains poorly understood.

A Shift in the Thermoregulatory Curve as a Result of Selection for High Activity-Related Aerobic Metabolism.

According to the "aerobic capacity model," endothermy in birds and mammals evolved as a result of natural selection favoring increased persistent locomotor activity, fuelled by aerobic metabolism. However, this also increased energy expenditure even during rest, with the lowest metabolic rates occurring in the thermoneutral zone (TNZ) and increasing at ambient temperatures (T) below and above this range, depicted by the thermoregulatory curve. In our experimental evolution system, four lines of bank voles () have been selected for high swim-induced aerobic metabolism and four unselected lines have been maintained as a control.

Age-related changes of physiological performance and survivorship of bank voles selected for high aerobic capacity.

Variation in lifespans is an intriguing phenomenon, but how metabolic rate influence this variation remains unclear. High aerobic capacity can result in health benefits, but also in increased oxidative damage and accelerated ageing. We tested these contradictory predictions using bank voles (Myodes=Clethrionomys glareolus) from lines selected for high swim-induced aerobic metabolism (A), which had about 50% higher maximum metabolic rate and a higher basal and routine metabolic rates, than those from unselected control lines (C).