Showing papers in "The Journal of Experimental Biology in 2018"

Oxygen- and capacity-limited thermal tolerance: blurring ecology and physiology

Abstract: The Commentary by Portner, Bock and Mark ([Portner et al., 2017][1]) elaborates on the oxygen- and capacity-limited thermal tolerance (OCLTT) hypothesis. Journal of Experimental Biology Commentaries allow for personal and controversial views, yet the journal also mandates that ‘opinion and fact

Evolution of neuropeptide signalling systems.

Abstract: Neuropeptides are a diverse class of neuronal signalling molecules that regulate physiological processes and behaviour in animals. However, determining the relationships and evolutionary origins of the heterogeneous assemblage of neuropeptides identified in a range of phyla has presented a huge challenge for comparative physiologists. Here, we review revolutionary insights into the evolution of neuropeptide signalling that have been obtained recently through comparative analysis of genome/transcriptome sequence data and by ‘deorphanisation’ of neuropeptide receptors. The evolutionary origins of at least 30 neuropeptide signalling systems have been traced to the common ancestor of protostomes and deuterostomes. Furthermore, two rounds of genome duplication gave rise to an expanded repertoire of neuropeptide signalling systems in the vertebrate lineage, enabling neofunctionalisation and/or subfunctionalisation, but with lineage-specific gene loss and/or additional gene or genome duplications generating complex patterns in the phylogenetic distribution of paralogous neuropeptide signalling systems. We are entering a new era in neuropeptide research where it has become feasible to compare the physiological roles of orthologous and paralogous neuropeptides in a wide range of phyla. Moreover, the ambitious mission to reconstruct the evolution of neuropeptide function in the animal kingdom now represents a tangible challenge for the future.

Drosophila as a model to study obesity and metabolic disease

Abstract: Excess adipose fat accumulation, or obesity, is a growing problem worldwide in terms of both the rate of incidence and the severity of obesity-associated metabolic disease. Adipose tissue evolved in animals as a specialized dynamic lipid storage depot: adipose cells synthesize fat (a process called lipogenesis) when energy is plentiful and mobilize stored fat (a process called lipolysis) when energy is needed. When a disruption of lipid homeostasis favors increased fat synthesis and storage with little turnover owing to genetic predisposition, overnutrition or sedentary living, complications such as diabetes and cardiovascular disease are more likely to arise. The vinegar fly Drosophila melanogaster (Diptera: Drosophilidae) is used as a model to better understand the mechanisms governing fat metabolism and distribution. Flies offer a wealth of paradigms with which to study the regulation and physiological effects of fat accumulation. Obese flies accumulate triacylglycerols in the fat body, an organ similar to mammalian adipose tissue, which specializes in lipid storage and catabolism. Discoveries in Drosophila have ranged from endocrine hormones that control obesity to subcellular mechanisms that regulate lipogenesis and lipolysis, many of which are evolutionarily conserved. Furthermore, obese flies exhibit pathophysiological complications, including hyperglycemia, reduced longevity and cardiovascular function - similar to those observed in obese humans. Here, we review some of the salient features of the fly that enable researchers to study the contributions of feeding, absorption, distribution and the metabolism of lipids to systemic physiology.

Heterogeneity of adipose tissue in development and metabolic function.

Abstract: Adipose tissue is a central metabolic organ. Unlike other organs, adipose tissue is compartmentalized into individual depots and distributed throughout the body. These different adipose depots show major functional differences and risk associations for developing metabolic syndrome. Recent advances in lineage tracing demonstrate that individual adipose depots are composed of adipocytes that are derived from distinct precursor populations, giving rise to different populations of energy-storing white adipocytes. Moreover, distinct lineages of energy-dissipating brown and beige adipocytes exist in discrete depots or within white adipose tissue depots. In this Review, we discuss developmental and functional heterogeneity, as well as sexual dimorphism, between and within individual adipose tissue depots. We highlight current data relating to the differences between subcutaneous and visceral white adipose tissue in the development of metabolic dysfunction, with special emphasis on adipose tissue expansion and remodeling of the extracellular matrix. Moreover, we provide a detailed overview of adipose tissue development as well as the consensus and controversies relating to adult adipocyte precursor populations.

The effects of obesity on skeletal muscle contractile function.

Abstract: Obesity can cause a decline in contractile function of skeletal muscle, thereby reducing mobility and promoting obesity-associated health risks. We reviewed the literature to establish the current state-of-knowledge of how obesity affects skeletal muscle contraction and relaxation. At a cellular level, the dominant effects of obesity are disrupted calcium signalling and 5'-adenosine monophosphate-activated protein kinase (AMPK) activity. As a result, there is a shift from slow to fast muscle fibre types. Decreased AMPK activity promotes the class II histone deacetylase (HDAC)-mediated inhibition of the myocyte enhancer factor 2 (MEF2). MEF2 promotes slow fibre type expression, and its activity is stimulated by the calcium-dependent phosphatase calcineurin. Obesity-induced attenuation of calcium signalling via its effects on calcineurin, as well as on adiponectin and actinin affects excitation-contraction coupling and excitation-transcription coupling in the myocyte. These molecular changes affect muscle contractile function and phenotype, and thereby in vivo and in vitro muscle performance. In vivo, obesity can increase the absolute force and power produced by increasing the demand on weight-supporting muscle. However, when normalised to body mass, muscle performance of obese individuals is reduced. Isolated muscle preparations show that obesity often leads to a decrease in force produced per muscle cross-sectional area, and power produced per muscle mass. Obesity and ageing have similar physiological consequences. The synergistic effects of obesity and ageing on muscle function may exacerbate morbidity and mortality. Important future research directions include determining: the relationship between time course of weight gain and changes in muscle function; the relative effects of weight gain and high-fat diet feeding per se; the effects of obesity on muscle function during ageing; and if the effects of obesity on muscle function are reversible.

Understanding variation in metabolic rate

Abstract: Metabolic rate reflects an organism's capacity for growth, maintenance and reproduction, and is likely to be a target of selection. Physiologists have long sought to understand the causes and consequences of within-individual to among-species variation in metabolic rates - how metabolic rates relate to performance and how they should evolve. Traditionally, this has been viewed from a mechanistic perspective, relying primarily on hypothesis-driven approaches. A more agnostic, but ultimately more powerful tool for understanding the dynamics of phenotypic variation is through use of the breeder's equation, because variation in metabolic rate is likely to be a consequence of underlying microevolutionary processes. Here we show that metabolic rates are often significantly heritable, and are therefore free to evolve under selection. We note, however, that 'metabolic rate' is not a single trait: in addition to the obvious differences between metabolic levels (e.g. basal, resting, free-living, maximal), metabolic rate changes through ontogeny and in response to a range of extrinsic factors, and is therefore subject to multivariate constraint and selection. We emphasize three key advantages of studying metabolic rate within a quantitative genetics framework: its formalism, and its predictive and comparative power. We make several recommendations when applying a quantitative genetics framework: (i) measuring selection based on actual fitness, rather than proxies for fitness; (ii) considering the genetic covariances between metabolic rates throughout ontogeny; and (iii) estimating genetic covariances between metabolic rates and other traits. A quantitative genetics framework provides the means for quantifying the evolutionary potential of metabolic rate and why variance in metabolic rates within populations might be maintained.

Obese super athletes: fat-fueled migration in birds and bats.

Abstract: Migratory birds are physiologically specialized to accumulate massive fat stores (up to 50-60% of body mass), and to transport and oxidize fatty acids at very high rates to sustain flight for many hours or days. Target gene, protein and enzyme analyses and recent -omic studies of bird flight muscles confirm that high capacities for fatty acid uptake, cytosolic transport, and oxidation are consistent features that make fat-fueled migration possible. Augmented circulatory transport by lipoproteins is suggested by field data but has not been experimentally verified. Migratory bats have high aerobic capacity and fatty acid oxidation potential; however, endurance flight fueled by adipose-stored fat has not been demonstrated. Patterns of fattening and expression of muscle fatty acid transporters are inconsistent, and bats may partially fuel migratory flight with ingested nutrients. Changes in energy intake, digestive capacity, liver lipid metabolism and body temperature regulation may contribute to migratory fattening. Although control of appetite is similar in birds and mammals, neuroendocrine mechanisms regulating seasonal changes in fuel store set-points in migrants remain poorly understood. Triacylglycerol of birds and bats contains mostly 16 and 18 carbon fatty acids with variable amounts of 18:2n-6 and 18:3n-3 depending on diet. Unsaturation of fat converges near 70% during migration, and unsaturated fatty acids are preferentially mobilized and oxidized, making them good fuel. Twenty and 22 carbon n-3 and n-6 polyunsaturated fatty acids (PUFA) may affect membrane function and peroxisome proliferator-activated receptor signaling. However, evidence for dietary PUFA as doping agents in migratory birds is equivocal and requires further study.

The origins and evolution of sleep

Abstract: Sleep is nearly ubiquitous throughout the animal kingdom, yet little is known about how ecological factors or perturbations to the environment shape the duration and timing of sleep. In diverse animal taxa, poor sleep negatively impacts development, cognitive abilities and longevity. In addition to mammals, sleep has been characterized in genetic model organisms, ranging from the nematode worm to zebrafish, and, more recently, in emergent models with simplified nervous systems such as Aplysia and jellyfish. In addition, evolutionary models ranging from fruit flies to cavefish have leveraged natural genetic variation to investigate the relationship between ecology and sleep. Here, we describe the contributions of classical and emergent genetic model systems to investigate mechanisms underlying sleep regulation. These studies highlight fundamental interactions between sleep and sensory processing, as well as a remarkable plasticity of sleep in response to environmental changes. Understanding how sleep varies throughout the animal kingdom will provide critical insight into fundamental functions and conserved genetic mechanisms underlying sleep regulation. Furthermore, identification of naturally occurring genetic variation regulating sleep may provide novel drug targets and approaches to treat sleep-related diseases.

The many roles of fats in overwintering insects.

Abstract: Temperate, polar and alpine insects generally do not feed over winter and hence must manage their energy stores to fuel their metabolism over winter and to meet the energetic demands of development and reproduction in the spring. In this Review, we give an overview of the accumulation, use and conservation of fat reserves in overwintering insects and discuss the ways insects modify fats to facilitate their selective consumption or conservation. Many insects are in diapause and have depressed metabolic rates over winter; together with low temperatures, this means that lipid stores are likely to be consumed predominantly in the autumn and spring, when temperatures are higher but insects remain dormant. Although there is ample evidence for a shift towards less-saturated lipids in overwintering insects, switches between the use of carbohydrate and lipid stores during winter have not been well-explored. Insects usually accumulate cryoprotectants over winter, and the resulting increase in haemolymph viscosity is likely to reduce lipid transport. For freeze-tolerant insects (which withstand internal ice), we speculate that impaired oxygen delivery limits lipid oxidation when frozen. Acetylated triacylglycerols remain liquid at low temperatures and interact with water molecules, providing intriguing possibilities for a role in cryoprotection. Similarly, antifreeze glycolipids may play an important role in structuring water and ice during overwintering. We also touch on the uncertain role of non-esterified fatty acids in insect overwintering. In conclusion, lipids are an important component of insect overwintering energetics, but there remain many uncertainties ripe for detailed exploration.

Hormonally mediated effects of artificial light at night on behavior and fitness: linking endocrine mechanisms with function.

Abstract: Alternation between day and night is a predictable environmental fluctuation that organisms use to time their activities. Since the invention of artificial lighting, this predictability has been disrupted and continues to change in a unidirectional fashion with increasing urbanization. As hormones mediate individual responses to changing environments, endocrine systems might be one of the first systems affected, as well as being the first line of defense to ameliorate any negative health impacts. In this Review, we first highlight how light can influence endocrine function in vertebrates. We then focus on four endocrine axes that might be affected by artificial light at night (ALAN): pineal, reproductive, adrenal and thyroid. Throughout, we highlight key findings, rather than performing an exhaustive review, in order to emphasize knowledge gaps that are hindering progress on proposing impactful and concrete plans to ameliorate the negative effects of ALAN. We discuss these findings with respect to impacts on human and animal health, with a focus on the consequences of anthropogenic modification of the night-time environment for non-human organisms. Lastly, we stress the need for the integration of field and lab experiments as well as the need for long-term integrative eco-physiological studies in the rapidly expanding field of light pollution.

Non-adrenergic control of lipolysis and thermogenesis in adipose tissues.

Abstract: The enormous plasticity of adipose tissues, to rapidly adapt to altered physiological states of energy demand, is under neuronal and endocrine control. In energy balance, lipolysis of triacylglycerols and re-esterification of free fatty acids are opposing processes operating in parallel at identical rates, thus allowing a more dynamic transition from anabolism to catabolism, and vice versa. In response to alterations in the state of energy balance, one of the two processes predominates, enabling the efficient mobilization or storage of energy in a negative or positive energy balance, respectively. The release of noradrenaline from the sympathetic nervous system activates lipolysis in a depot-specific manner by initiating the canonical adrenergic receptor-Gs-protein-adenylyl cyclase-cyclic adenosine monophosphate-protein kinase A pathway, targeting proteins of the lipolytic machinery associated with the interface of the lipid droplets. In brown and brite adipocytes, lipolysis stimulated by this signaling pathway is a prerequisite for the activation of non-shivering thermogenesis. Free fatty acids released by lipolysis are direct activators of uncoupling protein 1-mediated leak respiration. Thus, pro- and anti-lipolytic mediators are bona fide modulators of thermogenesis in brown and brite adipocytes. In this Review, we discuss adrenergic and non-adrenergic mechanisms controlling lipolysis and thermogenesis and provide a comprehensive overview of pro- and anti-lipolytic mediators.

Fructose-containing caloric sweeteners as a cause of obesity and metabolic disorders.

Abstract: Compared with other carbohydrates, fructose-containing caloric sweeteners (sucrose, high-fructose corn syrup, pure fructose and fructose-glucose mixtures) are characterized by: a sweet taste generally associated with a positive hedonic tone; specific intestinal fructose transporters, i.e. GLUT5; a two-step fructose metabolism, consisting of the conversion of fructose carbones into ubiquitous energy substrates in splanchnic organs where fructolytic enzymes are expressed, and secondary delivery of these substrates to extrasplanchnic tissues. Fructose is a dispensable nutrient, yet its energy can be stored very efficiently owing to a rapid induction of intestinal fructose transporters and of splanchnic fructolytic and lipogenic enzymes by dietary fructose-containing caloric sweeteners. In addition, compared with fat or other dietary carbohydrates, fructose may be favored as an energy store because it uses different intestinal absorption mechanisms and different inter-organ trafficking pathways. These specific features make fructose an advantageous energy substrate in wild animals, mainly when consumed before periods of scarcity or high energy turnover such as migrations. These properties of fructose storage are also advantageous to humans who are involved in strenuous sport activities. In subjects with low physical activity, however, these same features of fructose metabolism may have the harmful effect of favoring energy overconsumption. Furthermore, a continuous exposure to high fructose intake associated with a low energy turnover leads to a chronic overproduction of intrahepatic trioses-phosphate production, which is secondarily responsible for the development of hepatic insulin resistance, intrahepatic fat accumulation, and increased blood triglyceride concentrations. In the long term, these effects may contribute to the development of metabolic and cardiovascular diseases.

Exercise-induced adaptations to white and brown adipose tissue.

Abstract: The beneficial effects of exercise on skeletal muscle and the cardiovascular system have long been known. Recent studies have focused on investigating the effects of exercise on adipose tissue and the effects that these exercise-induced adaptations have on overall metabolic health. Examination of exercise-induced adaptations in both white adipose tissue (WAT) and brown adipose tissue (BAT) has revealed marked differences in each tissue with exercise. In WAT, there are changes to both subcutaneous WAT (scWAT) and visceral WAT (vWAT), including decreased adipocyte size and lipid content, increased expression of metabolic genes, altered secretion of adipokines and increased mitochondrial activity. Adaptations specific to scWAT include lipidomic remodeling of phospholipids and, in rodents, the beiging of scWAT. The changes to BAT are less clear: studies evaluating the effect of exercise on the BAT of humans and rodents have revealed contradictory data, making this an important area of current investigation. In this Review, we discuss the exercise-induced changes to WAT and BAT that have been reported by different studies and highlight the current questions in this field.

The fallacy of the Pcrit - are there more useful alternatives?

Abstract: P crit – generally defined as the P O 2 below which the animal can no longer maintain a stable rate of O 2 consumption ( Ṁ O 2 ), such that Ṁ O 2 becomes dependent upon P O 2 – provides a single number into which a vast amount of experimental effort has been invested. Here, with specific reference to water-breathers, I argue that this focus on the P crit is not useful for six reasons: (1) calculation of P crit usually involves selective data editing; (2) the value of P crit depends greatly on the way it is determined; (3) there is no good theoretical justification for the concept; (4) P crit is not the transition point from aerobic to anaerobic metabolism, and it disguises what is really going on; (5) P crit is not a reliable index of hypoxia tolerance; and (6) P crit carries minimal information content. Preferable alternatives are loss of equilibrium (LOE) tests for hypoxia tolerance, and experimental description of full Ṁ O 2 versus P O 2 profiles accompanied by measurements of ventilation, lactate appearance and metabolic rate by calorimetry. If the goal is to assess the ability of the animal to regulate Ṁ O 2 from this profile in a mathematical fashion, promising, more informative alternatives to P crit are the regulation index and Michaelis–Menten or sigmoidal allosteric analyses.

The long and the short of it - a perspective on peptidergic regulation of circuits and behaviour.

Abstract: Neuropeptides are the most diverse class of chemical modulators in nervous systems They contribute to extensive modulation of circuit activity and have profound influences on animal physiology Studies on invertebrate model organisms, including the fruit fly Drosophila melanogaster and the nematode Caenorhabditis elegans, have enabled the genetic manipulation of peptidergic signalling, contributing to an understanding of how neuropeptides pattern the output of neural circuits to underpin behavioural adaptation Electrophysiological and pharmacological analyses of well-defined microcircuits, such as the crustacean stomatogastric ganglion, have provided detailed insights into neuropeptide functions at a cellular and circuit level These approaches can be increasingly applied in the mammalian brain by focusing on circuits with a defined and identifiable sub-population of neurons Functional analyses of neuropeptide systems have been underpinned by systematic studies to map peptidergic networks Here, we review the general principles and mechanistic insights that have emerged from these studies We also highlight some of the challenges that remain for furthering our understanding of the functional relevance of peptidergic modulation

Rethinking the evolution of the human foot: insights from experimental research

Abstract: Adaptive explanations for modern human foot anatomy have long fascinated evolutionary biologists because of the dramatic differences between our feet and those of our closest living relatives, the great apes. Morphological features, including hallucal opposability, toe length and the longitudinal arch, have traditionally been used to dichotomize human and great ape feet as being adapted for bipedal walking and arboreal locomotion, respectively. However, recent biomechanical models of human foot function and experimental investigations of great ape locomotion have undermined this simple dichotomy. Here, we review this research, focusing on the biomechanics of foot strike, push-off and elastic energy storage in the foot, and show that humans and great apes share some underappreciated, surprising similarities in foot function, such as use of plantigrady and ability to stiffen the midfoot. We also show that several unique features of the human foot, including a spring-like longitudinal arch and short toes, are likely adaptations to long distance running. We use this framework to interpret the fossil record and argue that the human foot passed through three evolutionary stages: first, a great ape-like foot adapted for arboreal locomotion but with some adaptations for bipedal walking; second, a foot adapted for effective bipedal walking but retaining some arboreal grasping adaptations; and third, a human-like foot adapted for enhanced economy during long-distance walking and running that had lost its prehensility. Based on this scenario, we suggest that selection for bipedal running played a major role in the loss of arboreal adaptations.

Environmental temperature alters the digestive performance and gut microbiota of a terrestrial amphibian.

Abstract: Environmental temperature and gut microbial communities can both have profound impacts on the digestive performance of ectothermic vertebrates. Additionally, the diversity, composition and function of gut microbial communities themselves are influenced by temperature. It is typically assumed that the temperature-dependent nature of ectotherm digestive performance is due to factors such as host physiological changes and adaptation to local climatic conditions. However, it is also possible that temperature-induced alterations to gut microbiota may influence the relationship between temperature and digestion. To explore the connections between these three factors, we compared digestive performance and gut microbial community diversity and composition in red-backed salamanders housed at three experimental temperatures: 10, 15 and 20°C. We also investigated associations between specific bacterial taxa and temperature or salamander digestive performance. We found that salamander digestive performance was greatest at 15°C, while gut microbial diversity was reduced at 20°C. Further, gut microbial community composition differed among the three temperature treatments. The relative abundance of 25 bacterial genera was dependent on temperature, with high temperatures being associated with reductions in the relative abundance of disease-resistant bacteria and increases in pathogenic taxa. The relative abundance of four bacterial genera was correlated with salamander energy assimilation, two of which are known to digest chitin, a main component of the red-backed salamander diet. These findings suggest that gut microbiota may mediate the relationship between temperature and digestion in ectotherms. We discuss how global climate change may impact ectotherms by altering host–microbe interactions.

Robotics-inspired biology

Abstract: For centuries, designers and engineers have looked to biology for inspiration. Biologically inspired robots are just one example of the application of knowledge of the natural world to engineering problems. However, recent work by biologists and interdisciplinary teams have flipped this approach, using robots and physical models to set the course for experiments on biological systems and to generate new hypotheses for biological research. We call this approach robotics-inspired biology; it involves performing experiments on robotic systems aimed at the discovery of new biological phenomena or generation of new hypotheses about how organisms function that can then be tested on living organisms. This new and exciting direction has emerged from the extensive use of physical models by biologists and is already making significant advances in the areas of biomechanics, locomotion, neuromechanics and sensorimotor control. Here, we provide an introduction and overview of robotics-inspired biology, describe two case studies and suggest several directions for the future of this exciting new research area.

UMATracker: an intuitive image-based tracking platform.

Abstract: Image-based tracking software are regarded as valuable tools in collective animal behaviour studies. For such operations, image preprocessing is a prerequisite, and the users are required to build an appropriate image-processing pipeline for extracting the shape of animals. Even if the users successfully design an image-processing pipeline, unexpected noise in the video frame may significantly reduce the tracking accuracy in the tracking step. To address these issues, we propose UMATracker (Useful Multiple Animal Tracker), which supports flexible image preprocessing by visual programming, multiple tracking algorithms and a manual tracking error-correction system. UMATracker employs a visual programming user interface, wherein the user can intuitively design an image-processing pipeline. Moreover, the software also enables the user to visualize the effect of image processing. We implement four different tracking algorithms to enable the users to choose the most suitable algorithm. In addition, UMATracker provides a manual correction tool for identifying and correcting tracking errors.

Environmental enrichment modulates the response to chronic stress in zebrafish.

Abstract: Several studies have shown that manipulations to the housing environment modulate susceptibility to stress in laboratory animals, mainly in rodents. Environmental enrichment (EE) is one such manipulation that promotes neuroprotection and neurogenesis, besides affecting behaviors such as drug self-administration. Zebrafish are a popular and useful animal model for behavioral neuroscience studies; however, studies evaluating the impact of housing conditions in this species are scarce. In this study, we verified the effects of EE on behavioral (novel tank test) and biochemical [cortisol and reactive oxygen species (ROS)] parameters in zebrafish submitted to unpredictable chronic stress (UCS). Consistent with our previous findings, UCS increased anxiety-like behavior, cortisol and ROS levels in zebrafish. EE for 21 or 28 days attenuated the effects induced by UCS on behavior and cortisol, and prevented the effects on ROS levels. Our findings reinforce the idea that EE exerts neuromodulatory effects across species, reducing vulnerability to stress and its biochemical impact. Also, these results indicate that zebrafish is a suitable model animal to study the behavioral effects and neurobiological mechanisms related to EE.

The utility of transcriptomics in fish conservation.

Abstract: There is growing recognition of the need to understand the mechanisms underlying organismal resilience (i.e. tolerance, acclimatization) to environmental change to support the conservation management of sensitive and economically important species. Here, we discuss how functional genomics can be used in conservation biology to provide a cellular-level understanding of organismal responses to environmental conditions. In particular, the integration of transcriptomics with physiological and ecological research is increasingly playing an important role in identifying functional physiological thresholds predictive of compensatory responses and detrimental outcomes, transforming the way we can study issues in conservation biology. Notably, with technological advances in RNA sequencing, transcriptome-wide approaches can now be applied to species where no prior genomic sequence information is available to develop species-specific tools and investigate sublethal impacts that can contribute to population declines over generations and undermine prospects for long-term conservation success. Here, we examine the use of transcriptomics as a means of determining organismal responses to environmental stressors and use key study examples of conservation concern in fishes to highlight the added value of transcriptome-wide data to the identification of functional response pathways. Finally, we discuss the gaps between the core science and policy frameworks and how thresholds identified through transcriptomic evaluations provide evidence that can be more readily used by resource managers.

The evolution of body fatness: trading off disease and predation risk

Abstract: Human obesity has a large genetic component, yet has many serious negative consequences. How this state of affairs has evolved has generated wide debate. The thrifty gene hypothesis was the first attempt to explain obesity as a consequence of adaptive responses to an ancient environment that in modern society become disadvantageous. The idea is that genes (or more precisely, alleles) predisposing to obesity may have been selected for by repeated exposure to famines. However, this idea has many flaws: for instance, selection of the supposed magnitude over the duration of human evolution would fix any thrifty alleles (famines kill the old and young, not the obese) and there is no evidence that hunter-gatherer populations become obese between famines. An alternative idea (called thrifty late) is that selection in famines has only happened since the agricultural revolution. However, this is inconsistent with the absence of strong signatures of selection at single nucleotide polymorphisms linked to obesity. In parallel to discussions about the origin of obesity, there has been much debate regarding the regulation of body weight. There are three basic models: the set-point, settling point and dual-intervention point models. Selection might act against low and high levels of adiposity because food unpredictability and the risk of starvation selects against low adiposity whereas the risk of predation selects against high adiposity. Although evidence for the latter is quite strong, evidence for the former is relatively weak. The release from predation ∼2-million years ago is suggested to have led to the upper intervention point drifting in evolutionary time, leading to the modern distribution of obesity: the drifty gene hypothesis. Recent critiques of the dual-intervention point/drifty gene idea are flawed and inconsistent with known aspects of energy balance physiology. Here, I present a new formulation of the dual-intervention point model. This model includes the novel suggestion that food unpredictability and starvation are insignificant factors driving fat storage, and that the main force driving up fat storage is the risk of disease and the need to survive periods of pathogen-induced anorexia. This model shows why two independent intervention points are more likely to evolve than a single set point. The molecular basis of the lower intervention point is likely based around the leptin pathway signalling. Determining the molecular basis of the upper intervention point is a crucial key target for future obesity research. A potential definitive test to separate the different models is also described.

Eco-immunology in the cold: the role of immunity in shaping the overwintering survival of ectotherms

Abstract: The effect of temperature on physiology mediates many of the challenges that ectotherms face under climate change. Ectotherm immunity is thermally sensitive and, as such, environmental change is likely to have complex effects on survival, disease resistance and transmission. The effects of temperature on immunity will be particularly profound in winter because cold and overwintering are important triggers and regulators of ectotherm immune activity. Low temperatures can both suppress and activate immune responses independent of parasites, which suggests that temperature not only affects the rate of immune responses but also provides information that allows overwintering ectotherms to balance investment in immunity and other physiological processes that underlie winter survival. Changing winter temperatures are now shifting ectotherm immunity, as well as the demand for energy conservation and protection against parasites. Whether an ectotherm can survive the winter will thus depend on whether new immune phenotypes will shift to match the conditions of the new environment, or leave ectotherms vulnerable to infection or energy depletion. Here, we synthesise patterns of overwintering immunity in ectotherms and examine how new winter conditions might affect ectotherm immunity. We then explore whether it is possible to predict the effects of changing winter conditions on ectotherm vulnerability to the direct and indirect effects of parasites.

Biomechanics of swimming in developing larval fish.

Abstract: Most larvae of bony fish are able to swim almost immediately after hatching. Their locomotory system supports several vital functions: fish larvae make fast manoeuvres to escape from predators, aim accurately during suction feeding and may migrate towards suitable future habitats. Owing to their small size and low swimming speed, larval fish operate in the intermediate hydrodynamic regime, which connects the viscous and inertial flow regimes. They experience relatively strong viscous effects at low swimming speeds, and relatively strong inertial effects at their highest speeds. As the larvae grow and increase swimming speed, a shift occurs towards the inertial flow regime. To compensate for size-related limitations on swimming speed, fish larvae exploit high tail beat frequencies at their highest speeds, made possible by their low body inertia and fast neuromuscular system. The shifts in flow regime and body inertia lead to changing functional demands on the locomotory system during larval growth. To reach the reproductive adult stage, the developing larvae need to adjust to and perform the functions necessary for survival. Just after hatching, many fish larvae rely on yolk and need to develop their feeding systems before the yolk is exhausted. Furthermore, the larvae need to develop and continuously adjust their sensory, neural and muscular systems to catch prey and avoid predation. This Review discusses the hydrodynamics of swimming in the intermediate flow regime, the changing functional demands on the locomotory system of the growing and developing larval fish, and the solutions that have evolved to accommodate these demands.

Developmental phenotypic plasticity helps bridge stochastic weather events associated with climate change.

Abstract: The slow, inexorable rise in annual average global temperatures and acidification of the oceans are often advanced as consequences of global change. However, many environmental changes, especially those involving weather (as opposed to climate), are often stochastic, variable and extreme, particularly in temperate terrestrial or freshwater habitats. Moreover, few studies of animal and plant phenotypic plasticity employ realistic (i.e. short-term, stochastic) environmental change in their protocols. Here, I posit that the frequently abrupt environmental changes (days, weeks, months) accompanying much longer-term general climate change (e.g. global warming over decades or centuries) require consideration of the true nature of environmental change (as opposed to statistical means) coupled with an expansion of focus to consider developmental phenotypic plasticity. Such plasticity can be in multiple forms – obligatory/facultative, beneficial/deleterious – depending upon the degree and rate of environmental variability at specific points in organismal development. Essentially, adult phenotypic plasticity, as important as it is, will be irrelevant if developing offspring lack sufficient plasticity to create modified phenotypes necessary for survival.

Genomic imprinting, growth and maternal–fetal interactions

Abstract: In the 1980s, mouse nuclear transplantation experiments revealed that both male and female parental genomes are required for successful development to term ( McGrath and Solter, 1983; Surani and Barton, 1983). This non-equivalence of parental genomes is because imprinted genes are predominantly expressed from only one parental chromosome. Uniparental inheritance of these genomic regions causes paediatric growth disorders such as Beckwith-Wiedemann and Silver-Russell syndromes (reviewed in Peters, 2014). More than 100 imprinted genes have now been discovered and the functions of many of these genes have been assessed in murine models. The first such genes described were the fetal growth factor insulin-like growth factor 2 (Igf2) and its inhibitor Igf2 receptor (Igf2r) ( DeChiara et al., 1991; Lau et al., 1994; Wang et al., 1994). Since then, it has emerged that most imprinted genes modulate fetal growth and resource acquisition in a variety of ways. First, imprinted genes are required for the development of a functional placenta, the organ that mediates the exchange of nutrients between mother and fetus. Second, these genes act in an embryo-autonomous manner to affect the growth rate and organogenesis. Finally, imprinted genes can signal the nutritional status between mother and fetus, and can modulate levels of maternal care. Importantly, many imprinted genes have been shown to affect postnatal growth and energy homeostasis. Given that abnormal birthweight correlates with adverse adult metabolic health, including obesity and cardiovascular disease, it is crucial to understand how the modulation of this dosage-sensitive, epigenetically regulated class of genes can contribute to fetal and postnatal growth, with implications for lifelong health and disease.

The importance of incorporating natural thermal variation when evaluating physiological performance in wild species.

Abstract: Environmental variability in aquatic ecosystems makes the study of ectotherms complex and challenging. Physiologists have historically overcome this hurdle in the laboratory by using 'average' conditions, representative of the natural environment for any given animal. Temperature, in particular, has widespread impact on the physiology of animals, and it is becoming increasingly important to understand these effects as we face future climate challenges. The majority of research to date has focused on the expected global average increase in temperature; however, increases in climate variability are predicted to affect animals as much or more than climate warming. Physiological responses associated with the acclimation to a new stable temperature are distinct from those in thermally variable environments. Our goal is to highlight these physiological differences as they relate to both thermal acclimation and the 'fallacy of the average' or Jensen's inequality using theoretical models and novel empirical data. We encourage the use of more realistic thermal environments in experimental design to advance our understanding of these physiological responses such that we can better predict how aquatic animals will respond to future changes in our climate.

Ammonia excretion in aquatic invertebrates: new insights and questions.

Abstract: Invertebrates employ a variety of ammonia excretion strategies to facilitate their survival in diverse aquatic environments, including freshwater, seawater and the water film surrounding soil particles Various environmental properties set innate challenges for an organism9s ammonia excretory capacity These include the availability of NaCl and the respective ion-permeability of the organism9s transport epithelia, and the buffering capacity of their immediate surrounding medium To this end, some transporters seem to be conserved in the excretory process This includes the Na+/K+(NH4+)-ATPase (NKA), the NH3/CO2 dual gas-channel Rhesus (Rh)-proteins and novel ammonia transporters (AMTs), which have been identified in several invertebrates but appear to be absent from vertebrates In addition, recent evidence strongly suggests that the hyperpolarization-activated cyclic nucleotide-gated K+ channel (HCN) plays a significant role in ammonia excretion and is highly conserved throughout the animal kingdom Furthermore, microtubule-dependent vesicular excretion pathways have been found in marine and soil-dwelling species, where, unlike freshwater systems, acid-trapping of excreted ammonia is difficult or absent owing to the high environmental buffering capacity of the surroundings Finally, although ammonia is known to be a toxic nitrogenous waste product, certain marine species readily maintain potentially toxic hemolymph ammonia as a sort of ammonia homeostasis, which suggests that ammonia is involved in physiological processes and does not exist simply for excretion Such findings are discussed within this Commentary and are hypothesized to be involved in acid–base regulation We also describe excretory organs and processes that are dependent on environmental constraints and indicate gaps in the current knowledge in these topics

Adipose morphology and metabolic disease

Abstract: Adipose morphology is defined as the number and size distribution of adipocytes (fat cells) within adipose tissue. Adipose tissue with fewer but larger adipocytes is said to have a 'hypertrophic' morphology, whereas adipose with many adipocytes of a smaller size is said to have a 'hyperplastic' morphology. Hypertrophic adipose morphology is positively associated with insulin resistance, diabetes and cardiovascular disease. By contrast, hyperplastic morphology is associated with improved metabolic parameters. These phenotypic associations suggest that adipose morphology influences risk of cardiometabolic disease. Intriguingly, monozygotic twin studies have determined that adipose morphology is in part determined genetically. Therefore, identifying the genetic regulation of adipose morphology may help us to predict, prevent and ameliorate insulin resistance and associated metabolic diseases. Here, we review the current literature regarding adipose morphology in relation to: (1) metabolic and medical implications; (2) the methods used to assess adipose morphology; and (3) transcriptional differences between morphologies. We further highlight three mechanisms that have been hypothesized to promote adipocyte hypertrophy and thus to regulate adipose morphology.

Mechanisms underpinning the beneficial effects of fluctuating thermal regimes in insect cold tolerance.

Abstract: Insects exposed to low temperature often have high mortality or exhibit sublethal effects. A growing number of recent studies have shown beneficial effects of exposing insects to recurrent brief warm pulses during low-temperature stress (fluctuating thermal regime, FTR). The physiological underpinnings of the beneficial effects of FTR on cold survival have been extensively studied over the past few years. Profiling with various '-omics' techniques has provided supporting evidence for different physiological responses between insects exposed to FTR and constant low temperature. Evidence from transcriptomic, metabolomic and lipidomic studies points to a system-wide loss of homeostasis at low temperature that can be counterbalanced by repair mechanisms under FTR. Although there has been considerable progress in understanding the physiological mechanisms underlying the beneficial effects of FTR, here we discuss how many areas still lack clarity, such as the precise role(s) of heat shock proteins, compatible solutes or the identification of regulators and key players involved in the observed homeostatic responses. FTR can be particularly beneficial in applied settings, such as for model insects used in research, integrated pest management and pollination services. We also explain how the application of FTR techniques in large-scale facilities may require overcoming some logistical and technical constraints. FTR definitively enhances survival at low temperature in insects, but before it can be widely used, we suggest that the possible fitness and energy costs of FTR must be explored more thoroughly. Although FTR is not ecologically relevant, similar processes may operate in settings where temperatures fluctuate naturally.