Explaining sex differences in lifespan in terms of optimal energy allocation in the baboon

We provide a quantitative test of the hypothesis that sex role specialization may account for sex differences in lifespan in baboons if such specialization causes the dependency of fitness upon longevity, and consequently the optimal resolution to an energetic trade‐off between somatic maintenance and other physiological functions, to differ between males and females. We present a model in which females provide all offspring care and males compete for access to reproductive females and in which the partitioning of available energy between the competing fitness‐enhancing functions of growth, maintenance, and reproduction is modeled as a dynamic behavioral game, with the optimal decision for each individual depending upon his/her state and the behavior of other members of the population. Our model replicates the sexual dimorphism in body size and sex differences in longevity and reproductive scheduling seen in natural populations of baboons. We show that this outcome is generally robust to perturbations in model parameters, an important finding given that the same behavior is seen across multiple populations and species in the wild. This supports the idea that sex differences in longevity result from differences in the value of somatic maintenance relative to other fitness‐enhancing functions in keeping with the disposable soma theory.     

Sex differences in telomeres and lifespan in Soay sheep: From the beginning to the end

There is tremendous diversity in ageing rates and lifespan not only among taxa but within species, and particularly between the sexes. Women often live longer than men, and considerable research on this topic has revealed some of the potential biological, psychological and cultural causes of sex differences in human ageing and lifespan. However, sex differences in lifespan are widespread in nonhuman animals suggesting biology plays a prominent role in variation in ageing and lifespan. Recently, evolutionary biologists have borrowed techniques from biomedicine to identify whether similar mechanisms causing or contributing to variation in ageing and lifespan in humans and laboratory animals also operate in wild animals. Telomeres are repetitive noncoding DNA sequences capping the ends of chromosomes that are important for chromosomal stability but that can shorten during normal cell division and exposure to stress. Telomere shortening is hypothesized to directly contribute to the ageing process as once telomeres shorten to some length, the cells stop dividing and die. Men tend to have shorter telomeres and faster rates of telomere attrition with age than women, suggesting one possible biological cause of sex differences in lifespan. In this issue of Molecular Ecology, Watson et al. ( 2017 ) show that telomere lengths in wild Soay sheep are similar between females and males near the beginning of life but quickly diverge with age because males but not females showed reduced telomere lengths at older ages. The authors further show that some of the observed sex difference in telomere lengths in old age may be due to male investment in horn growth earlier in life, suggesting that sexually dimorphic allocation to traits involved in sexual selection might underlie sex differences in telomere attrition. This study provides a rare example of how biological mechanisms potentially contributing to sex differences in lifespan in humans may also operate in free‐living animals. However, future studies using a longitudinal approach are necessary to confirm these observations and identify the ultimate and proximate causes of any sex differences in telomere lengths. Collaborations between evolutionary biologists and gerontologists are especially needed to identify whether telomere lengths have a causal role in ageing, particularly in natural conditions, and whether this directly contributes to sex differences in lifespan.     

A comparative analysis of senescence in adult damselflies and dragonflies (Odonata)

Any population whose members are subject to extrinsic mortality should exhibit an increase in mortality with age. Nevertheless, the prevailing opinion is that populations of adult damselflies and dragonflies do not exhibit such senescence. Here, we challenge this contention by fitting a range of demographic models to the data on which these earlier conclusions were based. We show that a model with an exponential increase in age-related mortality (Gompertz) generally provides a more parsimonious fit than alternative models including age-independent mortality, indicating that many odonates do indeed senesce. Controlling for phylogeny, a comparison of the daily mortality of 35 odonate species indicates that although male and female mortalities are positively correlated, mortality tends to be higher in males of those species that exhibit territoriality. Hence, we show for the first time that territoriality may impose a survivorship cost on males, once the underlying phylogenetic relationships are accounted for.     

The free-radical damage theory: Accumulating evidence against a simple link of oxidative stress to ageing and lifespan

Recent work on a small European cave salamander (Proteus anguinus) has revealed that it has exceptional longevity, yet it appears to have unexceptional defences against oxidative damage. This paper comes at the end of a string of other studies that are calling into question the free-radical damage theory of ageing. This theory rose to prominence in the 1990s as the dominant theory for why we age and die. Despite substantial correlative evidence to support it, studies in the last five years have raised doubts over its importance. In particular, these include studies of mice with the major antioxidant genes knocked out (both singly and in combination), which show the expected elevation in oxidative damage but no impact on lifespan. Combined, these findings raise fundamental questions over whether the free-radical damage theory remains useful for understanding the ageing process, and variation in lifespan and life histories.     

Energetic cost of calling: general constraints and species‐specific differences

The energetic cost of acoustic signalling varies tremendously among species. Understanding factors responsible for this heterogeneity is important for understanding the costs and benefits of signalling. Here, we present a general model, based on well‐established principles of bioenergetics, which predicts the energetic cost of call production across species. We test model predictions using an extensive database of resting and calling metabolic rates of insects, amphibians and birds. Results are largely supportive of model predictions. Calling metabolic rates scale predictably with body mass and temperature such that calling and resting metabolic rates are directly proportional to each other. The cost of acoustic signalling is ～8 times higher than resting metabolic rate in ectotherms, and ～2 times higher in birds. Differences in the increase in metabolic rate during calling are explained by the relative size of species’ sound‐producing muscles. Combined with published work, we quantify call efficiency and discuss model implications.     

Amphibian metamorphosis: An exquisite model for hormonal regulation of postembryonic development in vertebrates

Metamorphosis in invertebrates and vertebrates is an ideal model for studying mechanisms of postembryonic development regulated by external signals. Amphibian metamorphosis shares many similarities with mammalian development in the perinatal period. The precocious induction in vivo and in culture of amphibian metamorphosis by exogenous thyroid hormones and its retardation or inhibition by prolactin, have allowed the analysis of such characteristic features of postembryonic development as morphogenesis, tissue remodelling, gene reprogramming and programmed cell death. Recent studies on metamorphosis have revealed the important role played by such processes as auto- and cross-regulation of hormone receptor genes and by cell death or apoptosis, as in the maturation of the central nervous system, tissue restructuring and organolysis.     

Testing the 'free radical theory of aging' hypothesis: physiological differences in long-lived and short-lived colubrid snakes

We test the 'free radical theory of aging' using six species of colubrid snakes (numerous, widely distributed, non-venomous snakes of the family Colubridae) that exhibit long (> 15 years) or short (< 10 years) lifespans. Because the 'rate of living theory' predicts metabolic rates to be correlated with rates of aging and oxidative damage results from normal metabolic processes we sought to answer whether physiological parameters and locomotor performance (which is a good predictor of survival in juvenile snakes) mirrored the evolution of lifespans in these colubrid snakes. We measured whole animal metabolic rate (oxygen consumption Vo2), locomotor performance, cellular metabolic rate (mitochondrial oxygen consumption), and oxidative stress potential (hydrogen peroxide production by mitochondria). Longer-lived colubrid snakes have greater locomotor performance and reduced hydrogen peroxide production than short-lived species, while whole animal metabolic rates and mitochondrial efficiency did not differ with lifespan. We present the first measures testing the 'free radical theory of aging' using reptilian species as model organisms. Using reptiles with different lifespans as model organisms should provide greater insight into mechanisms of aging.     

Cost-free lifespan extension via optimization of gene expression in adulthood aligns with the developmental theory of ageing

Ageing evolves because the force of selection on traits declines with age but the proximate causes of ageing are incompletely understood. The ‘disposable soma’ theory of ageing (DST) upholds that competitive resource allocation between reproduction and somatic maintenance underpins the evolution of ageing and lifespan. In contrast, the developmental theory of ageing (DTA) suggests that organismal senescence is caused by suboptimal gene expression in adulthood. While the DST predicts the trade-off between reproduction and lifespan, the DTA predicts that age-specific optimization of gene expression can increase lifespan without reproduction costs. Here we investigated the consequences for lifespan, reproduction, egg size and individual fitness of early-life, adulthood and post-reproductive onset of RNAi knockdown of five ‘longevity’ genes involved in key biological processes in Caenorhabditis elegans. Downregulation of these genes in adulthood and/or during post-reproductive period increases lifespan, while we found limited evidence for a link between impaired reproduction and extended lifespan. Our findings demonstrate that suboptimal gene expression in adulthood often contributes to reduced lifespan directly rather than through competitive resource allocation between reproduction and somatic maintenance. Therefore, age-specific optimization of gene expression in evolutionarily conserved signalling pathways that regulate organismal life histories can increase lifespan without fitness costs.     

Complex genetic architecture of population differences in adult lifespan of a beetle: nonadditive inheritance, gender differences, body size and a large maternal effect

Evolutionary responses to selection can be complicated when there is substantial nonadditivity, which limits our ability to extrapolate from simple models of selection to population differentiation and speciation. Studies of Drosophila melanogaster indicate that lifespan and the rate of senescence are influenced by many genes that have environment- and sex-specific effects. These studies also demonstrate that interactions among alleles (dominance) and loci (epistasis) are common, with the degree of interaction differing between the sexes and among environments. However, little is known about the genetic architecture of lifespan or mortality rates for organisms other than D. melanogaster. We studied genetic architecture of differences in lifespan and shapes of mortality curves between two populations of the seed beetle, Callosobruchus maculatus (South India and Burkina Faso populations). These two populations differ in various traits (such as body size and adult lifespan) that have likely evolved via host-specific selection. We found that the genetic architecture of lifespan differences between populations differs substantially between males and females; there was a large maternal effect on male lifespan (but not on female lifespan), and substantial dominance of long-life alleles in females (but not males). The large maternal effect in males was genetically based (there was no significant cytoplasmic effect) likely due to population differences in maternal effects genes that influence lifespan of progeny. Rearing host did not affect the genetic architecture of lifespan, and there was no evidence that genes on the Y-chromosome influence the population differences in lifespan. Epistatic interactions among loci were detectable for the mortality rate of both males and females, but were detectable for lifespan only after controlling for body size variation among lines. The detection of epistasis, dominance, and sex-specific genetic effects on C. maculatus lifespan is consistent with results from line cross and quantitative trait locus studies of D. melanogaster.     

Effect of membrane stiffness and cytoskeletal element density on mechanical stimuli within cells: an analysis of the consequences of ageing in cells

A finite element model of a single cell was created and used to compute the biophysical stimuli generated within a cell under mechanical loading. Major cellular components were incorporated in the model: the membrane, cytoplasm, nucleus, microtubules, actin filaments, intermediate filaments, nuclear lamina and chromatin. The model used multiple sets of tensegrity structures. Viscoelastic properties were assigned to the continuum components. To corroborate the model, a simulation of atomic force microscopy indentation was performed and results showed a force/indentation simulation with the range of experimental results. A parametric analysis of both increasing membrane stiffness (thereby modelling membrane peroxidation with age) and decreasing density of cytoskeletal elements (thereby modelling reduced actin density with age) was performed. Comparing normal and aged cells under indentation predicts that aged cells have a lower membrane area subjected to high strain as compared with young cells, but the difference, surprisingly, is very small and may not be measurable experimentally. Ageing is predicted to have a more significant effect on strain deep in the nucleus. These results show that computation of biophysical stimuli within cells are achievable with single-cell computational models; correspondence between computed and measured force/displacement behaviours provides a high-level validation of the model. Regarding the effect of ageing, the models suggest only small, although possibly physiologically significant, differences in internal biophysical stimuli between normal and aged cells.     

Viability and membrane potential analysis of Bacillus megaterium cells by impedance flow cytometry

Single cell analysis is an important tool to gain deeper insights into microbial physiology for the characterization and optimization of bioprocesses. In this study a novel single cell analysis technique was applied for estimating viability and membrane potential (MP) of Bacillus megaterium cells cultured in minimal medium. Its measurement principle is based on the analysis of the electrical cell properties and is called impedance flow cytometry (IFC). Comparatively, state-of-the-art fluorescence-based flow cytometry (FCM) was used to verify the results obtained by IFC. Viability and MP analyses were performed with cells at different well-defined growth stages, focusing mainly on exponential and stationary phase cells, as well as on dead cells. This was done by PI and DiOC(2)(3) staining assays in FCM and by impedance measurements at 0.5 and 10 MHz in IFC. In addition, transition growth stages of long-term cultures and agar plate colonies were characterized with both methods. FCM and IFC analyses of all experiments gave comparable results, quantitatively and qualitatively, indicating that IFC is an equivalent technique to FCM for the study of physiological cell states of bacteria.     

Predicting natural mortality rates of plants and animals

Understanding the factors that control the mortality rates of species in their natural environments is important for understanding the structure and dynamics of populations, communities and ecosystems. Here, we test a model of natural mortality that yields explicit, quantitative predictions based on the constraints of body size and temperature on individual metabolism. Extensive field data from plants, invertebrates, fish, birds and mammals indicate that much of the heterogeneity in rates of natural mortality can be predicted, despite the many extrinsic sources of mortality in natural systems. These results suggest that common 'rule(s)' govern mortality rates in ecological communities for organisms as diverse as plants and animals.     

Metabolic control analysis of mitochondrial aconitase: influence over respiration and mitochondrial superoxide and hydrogen peroxide production

Abstract

The Fe-S cluster of mitochondrial aconitase is rapidly and selectively inactivated by oxidants, yielding an inactive enzyme that can be reactivated by reductants and iron in vivo. In order to elucidate the metabolic impact of oxidant-dependent aconitase inhibition over the citric acid cycle, the respiratory chain reactions, and reactive species formation, we performed a metabolic analysis using isolated mitochondria from different rat tissues. Titrations with fluorocitrate showed IC₅₀ for aconitase inhibition ranging from 7 to 24 μM. The aconitase inhibition threshold in mitochondrial oxygen consumption was determined to range from 63 to 98%. Of the tissues examined, brain and heart exhibited the highest values in the flux control coefficient (> 0.95). Aconitase-specific activity varied widely among tissues examined from ?60 mU/mg in liver to 321 mU/mg in kidney at 21% O₂. In brain and heart, aconitase-specific activity increased by 42 and 12%, respectively, at 2% O₂ reflecting aconitase inactivation by oxygen-derived oxidants at 21% O₂. Both mitochondrial membrane potential and hydrogen peroxide production significantly decreased upon aconitase inhibition in heart and brain mitochondria. These results indicate that aconitase can exert control over respiration (with tissue specificity) and support the hypothesis that inactivation of aconitase may provide a control mechanism to prevent O₂^●? and H₂O₂ formation by the respiratory chain.     

Within‐species variation in long‐term trajectories of growth,fecundity and mortality in the Collembola Folsomia candida

Senescence – the progressive deterioration of organisms with age – affects many traits of which survival and reproduction are the most commonly studied. Recent comparative studies have revealed a remarkable amount of variation in the patterns of ageing across the tree of life. This between‐species diversity raises many questions about the evolution of senescence and of the shapes of the life‐history age trajectories. Here, we study how the different components of the shapes of these life‐history age trajectories can vary within a single species to shed light on the possible constraints involved in their evolution. To do so, we closely followed in controlled laboratory conditions, and for more than 450 days, the mortality, body length and fecundity of small cohorts of two clonal lineages of the Collembola Folsomia candida. We studied three components of the adult mortality trajectory: the baseline mortality, onset and speed of senescence. We found that they can differ between strains of a single species in such a way that, remarkably, an increased life expectancy is not synonymous with a delayed senescence: the strain that grows bigger has the longest life expectancy but suffers from a precocious senescence. We observed marked differences between the strains in the asymptotic body length and reproductive investment. More generally, our results highlight the importance of finely describing the long‐term trajectories of several life‐history traits in order to better understand how the patterns of senescence have been shaped by natural selection.     

Sex differences in the genetic architecture of lifespan in a seed beetle: extreme inbreeding extends male lifespan

Background  

Sex differences in lifespan are ubiquitous throughout the animal kingdom but the causes underlying this phenomenon remain poorly understood. Several explanations based on asymmetrical inheritance patterns (sex chromosomes or mitochondrial DNA) have been proposed, but these ideas have rarely been tested experimentally. Alternatively, sexual dimorphism in lifespan could result from sex-specific selection, caused by fundamental differences in how males and females optimize their fitness by allocating resources into current and future reproduction.