Optimal time to patency in parasitic nematodes: host mortality matters

We develop an optimality model based on classical epidemiological models to investigate the optimal time to patency in parasitic nematodes in relation to host mortality and parasite mortality. We found that the optimal time to patency depends on both host longevity and prepatent mortality of nematodes. We tested our models using a comparative analysis of the relationships between nematode time to patency, nematode mortality and host mortality. Although we confirmed the importance of prepatent mortality, we also found a significant positive influence of host mortality. Host mortality rate affects parasite survivorship and life history strategies in the same way that habitat-specific mortality regimes drive the evolution of life histories in free-living organisms.     

Evolution of late-life mortality in Drosophila melanogaster

Abstract.— Aging appears to cease at late ages, when mortality rates roughly plateau in large-scale demographic studies. This anomalous plateau in late-life mortality has been explained theoretically in two ways: (1) as a strictly demographic result of heterogeneity in life-long robustness between individuals within cohorts, and (2) as an evolutionary result of the plateau in the force of natural selection after the end of reproduction. Here we test the latter theory using cohorts of Drosophila melanogaster cultured with different ages of reproduction for many generations. We show in two independent comparisons that populations that evolve with early truncation of reproduction exhibit earlier onset of mortality-rate plateaus, in conformity with evolutionary theory. In addition, we test two population genetic mechanisms that may be involved in the evolution of late-life mortality: mutation accumulation and antagonistic pleiotropy. We test mutation accumulation by crossing genetically divergent, yet demographically identical, populations, testing for hybrid vigor between the hybrid and nonhybrid parental populations. We found no difference between the hybrid and nonhybrid populations in late-life mortality rates, a result that does not support mutation accumulation as a genetic mechanism for late-life mortality, assuming mutations act recessively. Finally, we test antagonistic pleiotropy by returning replicate populations to a much earlier age of last reproduction for a short evolutionary time, testing for a rapid indirect response of late-life mortality rates. The positive results from this test support antagonistic pleiotropy as a genetic mechanism for the evolution of late-life mortality. Together these experiments comprise the first corroborations of the evolutionary theory of late-life mortality.     

A computational approach to studying ageing at the individual level

The ageing process is actively regulated throughout an organism''s life, but studying the rate of ageing in individuals is difficult with conventional methods. Consequently, ageing studies typically make biological inference based on population mortality rates, which often do not accurately reflect the probabilities of death at the individual level. To study the relationship between individual and population mortality rates, we integrated in vivo switch experiments with in silico stochastic simulations to elucidate how carefully designed experiments allow key aspects of individual ageing to be deduced from group mortality measurements. As our case study, we used the recent report demonstrating that pheromones of the opposite sex decrease lifespan in Drosophila melanogaster by reversibly increasing population mortality rates. We showed that the population mortality reversal following pheromone removal was almost surely occurring in individuals, albeit more slowly than suggested by population measures. Furthermore, heterogeneity among individuals due to the inherent stochasticity of behavioural interactions skewed population mortality rates in middle-age away from the individual-level trajectories of which they are comprised. This article exemplifies how computational models function as important predictive tools for designing wet-laboratory experiments to use population mortality rates to understand how genetic and environmental manipulations affect ageing in the individual.     

Social ageing: exploring the drivers of late-life changes in social behaviour in mammals

Social interactions help group-living organisms cope with socio-environmental challenges and are central to survival and reproductive success. Recent research has shown that social behaviour and relationships can change across the lifespan, a phenomenon referred to as ‘social ageing’. Given the importance of social integration for health and well-being, age-dependent changes in social behaviour can modulate how fitness changes with age and may be an important source of unexplained variation in individual patterns of senescence. However, integrating social behaviour into ageing research requires a deeper understanding of the causes and consequences of age-based changes in social behaviour. Here, we provide an overview of the drivers of late-life changes in sociality. We suggest that explanations for social ageing can be categorized into three groups: changes in sociality that (a) occur as a result of senescence; (b) result from adaptations to ameliorate the negative effects of senescence; and/or (c) result from positive effects of age and demographic changes. Quantifying the relative contribution of these processes to late-life changes in sociality will allow us to move towards a more holistic understanding of how and why these patterns emerge and will provide important insights into the potential for social ageing to delay or accelerate other patterns of senescence.     

Evolution of late-life fecundity in Drosophila melanogaster

Late-life fecundity has been shown to plateau at late ages in Drosophila analogously to late-life mortality rates. In this study, we test an evolutionary theory of late life based on the declining force of natural selection that can explain the occurrence of these late-life plateaus in Drosophila. We also examine the viability of eggs laid by late-age females and test a population genetic mechanism that may be involved in the evolution of late-life fecundity: antagonistic pleiotropy. Together these experiments demonstrate that (i) fecundity plateaus at late ages, (ii) plateaus evolve according to the age at which the force of natural selection acting on fecundity reaches zero, (iii) eggs laid by females in late life are viable and (iv) antagonistic pleiotropy is involved in the evolution of late-life fecundity. This study further supports the evolutionary theory of late life based on the age-specific force of natural selection.     

Beyond the proportional frailty model: Bayesian estimation of individual heterogeneity on mortality parameters

Today, we know that demographic rates can be greatly influenced by differences among individuals in their capacity to survive and reproduce. These intrinsic differences, commonly known as individual heterogeneity, can rarely be measured and are thus treated as latent variables when modeling mortality. Finite mixture models and mixed effects models have been proposed as alternative approaches for inference on individual heterogeneity in mortality. However, in general models assume that individual heterogeneity influences mortality proportionally, which limits the possibility to test hypotheses on the effect of individual heterogeneity on other aspects of mortality such as ageing rates. Here, we propose a Bayesian model that builds upon the mixture models previously developed, but that facilitates making inferences on the effect of individual heterogeneity on mortality parameters other than the baseline mortality. As an illustration, we apply this framework to the Gompertz–Makeham mortality model, commonly used in human and wildlife studies, by assuming that the Gompertz rate parameter is affected by individual heterogeneity. We provide results of a simulation study where we show that the model appropriately retrieves the parameters used for simulation, even for low variances in the heterogeneous parameter. We then apply the model to a dataset on captive chimpanzees and on a cohort life table of 1751 Swedish men, and show how model selection against a null model (i.e., without heterogeneity) can be carried out.     

Heat shock response and ageing: mechanisms and applications

Ageing is associated with a decrease in the ability of cells to cope with environmental challenges. This is due partly to the attenuation of a primordial stress response, the so-called heat shock (HS) response, which induces the expression of heat shock proteins (HSPs), composed of chaperones and proteases. The attenuation of the HS response during ageing may be responsible for the accumulation of damaged proteins as well as abnormal regulation of cell death. Maintenance of the HS response by repeated mild heat stress causes anti-ageing hormetic effects on cells and organisms. Here, we describe the molecular mechanism and the state of the HS response as well as the role of specific HSPs during ageing, and discuss the possibility of hormetic modulation of ageing and longevity by repeated mild stress.     

Pooling robustness in distance sampling: Avoiding bias when there is unmodelled heterogeneity

The pooling robustness property of distance sampling results in unbiased abundance estimation even when sources of variation in detection probability are not modeled. However, this property cannot be relied upon to produce unbiased subpopulation abundance estimates when using a single pooled detection function that ignores subpopulations. We investigate by simulation the effect of differences in subpopulation detectability upon bias in subpopulation abundance estimates. We contrast subpopulation abundance estimates using a pooled detection function with estimates derived using a detection function model employing a subpopulation covariate. Using point transect survey data from a multispecies songbird study, species-specific abundance estimates are compared using pooled detection functions with and without a small number of adjustment terms, and a detection function with species as a covariate. With simulation, we demonstrate the bias of subpopulation abundance estimates when a pooled detection function is employed. The magnitude of the bias is positively related to the magnitude of disparity between the subpopulation detection functions. However, the abundance estimate for the entire population remains unbiased except when there is extreme heterogeneity in detection functions. Inclusion of a detection function model with a subpopulation covariate essentially removes the bias of the subpopulation abundance estimates. The analysis of the songbird point count surveys shows some bias in species-specific abundance estimates when a pooled detection function is used. Pooling robustness is a unique property of distance sampling, producing unbiased abundance estimates at the level of the study area even in the presence of large differences in detectability between subpopulations. In situations where subpopulation abundance estimates are required for data-poor subpopulations and where the subpopulations can be identified, we recommend the use of subpopulation as a covariate to reduce bias induced in subpopulation abundance estimates.     

Density-dependent effects of mortality on the optimal body size to shift habitat: Why smaller is better despite increased mortality risk

Many animal species across different taxa change their habitat during their development. An ontogenetic habitat shift enables the development of early vulnerable-to-predation stages in a safe “nursery” habitat with reduced predation mortality, whereas less vulnerable stages can exploit a more risky, rich feeding habitat. Therefore, the timing of the habitat shift is crucial for individual fitness. We investigate the effect that size selectivity in mortality in the rich feeding habitat has on the optimal body size at which to shift between habitats using a population model that incorporates density dependence. We show that when mortality risk is more size dependent, it is optimal to switch to the risky habitat at a smaller rather than larger body size, despite that individuals can avoid mortality by staying longer in the nursery habitat and growing to safety in size. When size selectivity in mortality is high, large reproducing individuals are abundant and produce numerous offspring that strongly compete in the nursery habitat. A smaller body size at habitat shift is therefore favored because strong competition reduces growth potential. Our results reveal the interdependence among population structure, density dependence, and life history traits, and highlight the need for integrating ecological feedbacks in the study of life history evolution.     

Transgenerational memory effect of ageing in Drosophila

Children born to older parents tend to have lower intelligence and are at higher risk for disorders such as schizophrenia and autism. Such observations of ageing damage being passed on from parents to offspring are not often considered within the evolutionary theory of ageing. Here, we show the 25% memory impairment in Drosophila melanogaster offspring solely dependent on the age of the parents and also passed on to the F2 generation. Furthermore, this parental age effect was not attributed to a generalized reduction in condition of the offspring but was specific to short‐term memory. We also provide evidence implicating oxidative stress as a causal factor by showing that lines selected for resistance to oxidative stress did not display a memory impairment in offspring of old parents. The identification of the parental age‐related memory impairment in a model system should stimulate integration between mechanistic studies of age‐related mortality risk and functional studies of parental age effects on the fitness of future generations.     

The vitality model: A way to understand population survival and demographic heterogeneity

A four-parameter model describing mortality as the first passage of an abstract measure of survival capacity, vitality, is developed and used to explore four classic problems in demography: (1) medfly demographic paradox, (2) effect of diet restriction on longevity, (3) cross-life stage effects on survival curves and (4) mortality plateaus. The model quantifies the sources of mortality in these classical problems into vitality-dependent and independent parts, and characterizes the vitality-dependent part in terms of initial and evolving heterogeneities. Three temporal scales express the balance of these factors: a time scale of death from senescence, a time scale of accidental mortality and a crossover time between evolving vs. initial heterogeneity. The examples demonstrate how the first-passage approach provides a unique and informative perspective into the processes that shape the survival curves of populations.     

Predictive role of mitochondrial genome in the stress resistance of insects and nematodes

Certain insects (e.g., moths and butterflies; order Lepidoptera) and nematodes are considered as excellent experimental models to study the cellular stress signaling mechanisms since these organisms are far more stress-resistant as compared to mammalian system. Multiple factors have been implicated in this unusual response, including the oxidative stress response mechanisms. Radiation or chemical-induced mitochondrial oxidative stress occurs through damage caused to the components of electron transport chain (ETC) leading to leakage of electrons and generation of superoxide radicals. This may be countered through quick replacement of damaged mitochondrial proteins by upregulated expression. Since the ETC comprises of various proteins coded by mitochondrial DNA, variation in the composition, expressivity and regulation of mitochondrial genome could greatly influence mitochondrial role under oxidative stress conditions. Therefore, we carried out in silico analysis of mitochondrial DNA in these organisms and compared it with that of the stress-sensitive humans/mammals. Parameters such as mitochondrial genome organization, codon bias, gene expressivity and GC₃ content were studied. Gene arrangement and Shine-Dalgarno (SD) sequence patterns indicating translational regulation were distinct in insect and nematodes as compared to humans. A higher codon bias (ENC≫35) and lower GC₃ content (≫0.20) were observed in mitochondrial genes of insect and nematodes as compared to humans (ENC>42; GC3>0.20), coupled with low codon adaptation index among insects. These features indeed favour higher expressivity of mitochondrial proteins and might help maintain the mitochondrial physiology under stress conditions. Therefore, our study indicates that mitochondrial genome organization may influence stress-resistance of insects and nematodes.     

Benthic nematodes in acidified lakes: case of a neglected grazer

Abundance and composition of nematode fauna were examined in the benthic microbial mats and upper sediment layer of the littoral of acidified (pH 4.6 to 5.7) lakes. Nematodes constituted from 58% to 90% of all the invertebrates present (excluding protozoans and rotifers). In the examined material, the majority of nematodes was represented by 3 taxa of which Ironus was found specifically associated with the mats. It was concluded that the persistence of benthic mats may be linked to the metabolic activity of the associated nematode fauna.     

Synthetic biology in multicellular organisms: Opportunities in nematodes

Synthetic biology has mainly focused on introducing new or altered functionality in single cell systems: primarily bacteria, yeast, or mammalian cells. Here, we describe the extension of synthetic biology to nematodes, in particular the well-studied model organism Caenorhabditis elegans, as a convenient platform for developing applications in a multicellular setting. We review transgenesis techniques for nematodes, as well as the application of synthetic biology principles to construct nematode gene switches and genetic devices to control motility. Finally, we discuss potential applications of engineered nematodes.     

Role of plant parasitic nematodes and abiotic soil factors in growth heterogeneity of sugarcane on a sandy soil in South Africa

A feature of many sugarcane fields is the patchy growth. This is often thought to be due to physical or chemical differences in the soil. In this paper we investigate the causes of growth heterogeneity of sugarcane on a sandy soil in KwaZulu-Natal, South Africa. To identify the factors that were associated with the good and poor areas, soil texture, pH, organic matter content and a number of soil chemical elements and nematode community data were subjected to principal component analysis (PCA). The numbers of each of the nematode species (Meloidogyne sp., Pratylenchus zeae, Helicotylenchus dihystera, Xiphinema elongatum and Paratrichodorus sp.) were first converted to relative proportions of ectoparasites and endoparasites. The data were collected from the 2nd ratoon crop of a nematicide trial, where half of the plots had been treated with aldicarb in the preceding two crops. Yields of control plots varied from 34.7 to 126.8 t cane ha^–1 and from 85.4 to 138.7 for the treated plots. The yield data were centred and normalised separately for the treated and control plots and the values projected on the trial map to study spatial distribution. Plots with above-average yields, whether treated or untreated, occurred in the lower part of the trial site. The PCA factorial values were also projected onto the map of the trial. According to the first factor of the analysis of the abiotic soil characteristics in the 0–20 cm surface layer, the trial site could be divided into two areas, one on the left and one on the right. PCA of the soil data from the 0–20 and 20–40 cm layers showed that there was little or no difference between the two that might explain the two growth areas. However, analysis of the nematode community distinguished two main areas that largely corresponded to the distribution of the plots of low and high yielding cane. Correlation analysis confirmed the relationship between nematodes and yield. H. dihystera was positively correlated with yield of cane whereas the reverse was true for the Meloidogyne species.     

Causes and consequences of winter mortality in fishes

Winter mortality has been documented in a large number of freshwater fish populations, and a smaller, but increasing, number of marine and estuarine fishes. The impacted populations include a number of important North American and European resource species, yet the sources of winter mortality remain unidentified in most populations where it has been documented. Among the potential sources, thermal stress and starvation have received the most research attention. Other sources including predation and pathogens have significant impacts but have received insufficient attention to date. Designs of more recent laboratory experiments have reflected recognition of the potential for interactions among these co-occurring stressors. Geographic patterns in winter mortality are, in some cases, linked to latitudinal clines in winter severity and variability. However, for many freshwater species in particular, the effects of local community structure (predators and prey) may overwhelm latitudinal patterns. Marine (and estuarine) systems differ from freshwater systems in several aspects important to overwintering fishes, the most important being the lack of isolating barriers in the ocean. While open population boundaries allow fish to adopt migration strategies minimizing exposure to thermal stresses, they may retard rates of evolution to local environments. Geographic patterns in the occurrence and causes of winter mortality are ultimately determined by the interaction of regional and local factors. Winter mortality impacts population dynamics through episodic depressions in stock size and regulation of annual cohort strength. While the former tends to act in a density-independent manner, the latter can be density dependent, as most sources of mortality tend to select against the smallest members of the cohort and population. Most stock assessment and management regimes have yet to explicitly incorporate the variability in winter mortality. Potential management responses include postponement of cohort evaluation (to after first winter of life), harvest restrictions following mortality events and habitat enhancement. Future research should place more emphasis on the ecological aspects of winter mortality including the influences of food-web structure on starvation and predation. Beyond illuminating an understudied life-history phase, studies of overwintering ecology are integral to contemporary issues in fisheries ecology including ecosystem management, habitat evaluation, and impacts of climate change.