Diversity of ageing across the tree of life.

Evolution drives, and is driven by, demography. A genotype moulds its phenotype's age patterns of mortality and fertility in an environment; these two patterns in turn determine the genotype's fitness in that environment. Hence, to understand the evolution of ageing, age patterns of mortality and reproduction need to be compared for species across the tree of life. However, few studies have done so and only for a limited range of taxa. Here we contrast standardized patterns over age for 11 mammals, 12 other vertebrates, 10 invertebrates, 12 vascular plants and a green alga. Although it has been predicted that evolution should inevitably lead to increasing mortality and declining fertility with age after maturity, there is great variation among these species, including increasing, constant, decreasing, humped and bowed trajectories for both long- and short-lived species. This diversity challenges theoreticians to develop broader perspectives on the evolution of ageing and empiricists to study the demography of more species.

Constant mortality and fertility over age in Hydra.

Senescence, the increase in mortality and decline in fertility with age after maturity, was thought to be inevitable for all multicellular species capable of repeated breeding. Recent theoretical advances and compilations of data suggest that mortality and fertility trajectories can go up or down, or remain constant with age, but the data are scanty and problematic. Here, we present compelling evidence for constant age-specific death and reproduction rates in Hydra, a basal metazoan, in a set of experiments comprising more than 3.9 million days of observations of individual Hydra. Our data show that 2,256 Hydra from two closely related species in two laboratories in 12 cohorts, with cohort age ranging from 0 to more than 41 y, have extremely low, constant rates of mortality. Fertility rates for Hydra did not systematically decline with advancing age. This falsifies the universality of the theories of the evolution of aging that posit that all species deteriorate with age after maturity. The nonsenescent life history of Hydra implies levels of maintenance and repair that are sufficient to prevent the accumulation of damage for at least decades after maturity, far longer than the short life expectancy of Hydra in the wild. A high proportion of stem cells, constant and rapid cell turnover, few cell types, a simple body plan, and the fact that the germ line is not segregated from the soma are characteristics of Hydra that may make nonsenescence feasible. Nonsenescence may be optimal because lifetime reproduction may be enhanced more by extending adult life spans than by increasing daily fertility.

Unraveling the non-senescence phenomenon in Hydra.

Unlike other metazoans, Hydra does not experience the distinctive rise in mortality with age known as senescence, which results from an increasing imbalance between cell damage and cell repair. We propose that the Hydra controls damage accumulation mainly through damage-dependent cell selection and cell sloughing. We examine our hypothesis with a model that combines cellular damage with stem cell renewal, differentiation, and elimination. The Hydra individual can be seen as a large single pool of three types of stem cells with some features of differentiated cells. This large stem cell community prevents "cellular damage drift," which is inevitable in complex conglomerate (differentiated) metazoans with numerous and generally isolated pools of stem cells. The process of cellular damage drift is based on changes in the distribution of damage among cells due to random events, and is thus similar to Muller's ratchet in asexual populations. Events in the model that are sources of randomness include budding, cellular death, and cellular damage and repair. Our results suggest that non-senescence is possible only in simple Hydra-like organisms which have a high proportion and number of stem cells, continuous cell divisions, an effective cell selection mechanism, and stem cells with the ability to undertake some roles of differentiated cells.

FOXO in aging: did evolutionary diversification of FOXO function distract it from prolonging life?

In this paper we contrast the simple role of FOXO in the seemingly non-aging Hydra with its more diversified function in multicellular eukaryotes that manifest aging and limited life spans. From this comparison we develop the concept that, whilst once devoted to life-prolonging cell-renewal (in Hydra), evolutionary accumulation of coupled functionality in FOXO has since 'distracted' it from this role. Seen in this light, aging may not be the direct cost of competing functions, such as reproduction or growth, but the result of a shift in emphasis in a protein, which is accompanied by advantages such as greater organismal complexity and adaptability, but also disadvantages such as reduced regeneration capacity. Studying the role of FOXO in non-aging organisms might, therefore, illuminate the path to extend life span in aging organisms.

Aging and potential for self-renewal: hydra living in the age of aging - a mini-review.

Hydra present an interesting deviation from typical life histories: they have an extensive capacity to regenerate and self-renew and seem to defy the aging process. Hydra have the ability to decouple the aging process from their life history and therefore provide us with a unique opportunity to gain insight into the aging process not only for basal hydrozoans but also for other species across the tree of life. We argue that under steady feeding and asexual reproduction Hydra species are able to escape aging as a result of high levels of cell proliferation and regenerative ability. We further highlight cellular processes for stem cell maintenance, such as the telomere dynamic, which prevent the accumulation of damage and protect against diseases and pathogens that mediate this condition. In addition, we discuss the causes of aging in other Hydra species.

Two parthenogenetic populations of Chara canescens differ in their capacity to acclimate to irradiance and salinity.

The parthenogens of Chara canescens (Charophyceae) occupy broader geographical and ecological ranges than their sexual counterparts. Two possible hypotheses explain the ubiquity of parthenogens: the occurrence of one or several parthenogens with wide niches, or of many parthenogens that are restricted to narrow ecological niches. For the purposes of this study, C. canescens individuals from two neighbouring populations of the Baltic Sea (Bodstedter Bodden = BB; Salzhaff = SH), which differed significantly in water transparency and salinity, were investigated for significant differences in physiological capacity. Individuals of both habitats acclimated quickly to daily changes in irradiances in the field, but the photosynthetic efficiency of PS II showed a significant decrease with increasing daily irradiance in the habitat BB, which has lower levels of salinity and water transparency. In addition to the field study, individuals were reared under different levels of environmental factors in the laboratory: four irradiances (70-600 µmol m(-2) s(-1)) and five salinity levels (0-24 psu). The individuals of both habitats grew almost equally well at intermediate salinity levels. Growth under the artificial light supply was highest at levels corresponding to the in situ conditions for each population. Total chlorophyll was highest at intermediate salinities (BB), or hardly changed with salinity (SH). The physiological capacity for individuals from SH clearly depends upon changing growth irradiance, whereas the capacity for individuals from BB was relatively independent of salinity and irradiance. These findings indicate that both parthenogenetic C. canescens populations are locally adapted to light. However, to test adaptive potential of the parthenogens, more than two populations should be tested in future.

Population density shapes patterns of survival and reproduction in Eleutheria dichotoma (Hydrozoa: Anthoathecata).

Budding hydromedusae have high reproductive rates due to asexual reproduction and can occur in high population densities along the coasts, specifically in tidal pools. In laboratory experiments, we investigated the effects of population density on the survival and reproductive strategies of a single clone of Eleutheria dichotoma. We found that sexual reproduction occurs with the highest rate at medium population densities. Increased sexual reproduction was associated with lower budding (asexual reproduction) and survival probability. Sexual reproduction results in the production of motile larvae that can, in contrast to medusae, seek to escape unfavorable conditions by actively looking for better environments. The successful settlement of a larva results in starting the polyp stage, which is probably more resistant to environmental conditions. This is the first study that has examined the life-history strategies of the budding hydromedusa E. dichotoma by conducting a long-term experiment with a relatively large sample size that allowed for the examination of age-specific mortality and reproductive rates. We found that most sexual and asexual reproduction occurred at the beginning of life following a very rapid process of maturation. The parametric models fitted to the mortality data showed that population density was associated with an increase in the rate of aging, an increase in the level of late-life mortality plateau, and a decrease in the hidden heterogeneity in individual mortality rates. The effects of population density on life-history traits are discussed in the context of resource allocation and the r/K-strategies' continuum concept.

Worker lifespan is an adaptive trait during colony establishment in the long-lived ant Lasius niger.

Eusociality has been recognized as a strong driver of lifespan evolution. While queens show extraordinary lifespans of 20years and more, worker lifespan is short and variable. A recent comparative study found that in eusocial species with larger average colony sizes the disparities in the lifespans of the queen and the worker are also greater, which suggests that lifespan might be an evolved trait. Here, we tested whether the same pattern holds during colony establishment: as colonies grow larger, worker lifespan should decrease. We studied the mortality of lab-reared Lasius niger workers from colonies at two different developmental stages (small and intermediate-sized) in a common garden experiment. Workers were kept in artificial cohorts that differed only with respect to the stage of the colony they were born in. We found that the stage of the birth colony affected the body size and the survival probability of the workers. The workers that had emerged from early stage colonies were smaller and had lower mortality during the first 400days of their life than the workers born in colonies at a later stage. Our results suggest that early stage colonies produce small workers with an increased survival probability. These workers are gradually augmented by larger workers with a decreased survival probability that serve as a redundant workforce with easily replaceable individuals. We doubt that the observed differences in lifespan are driven by differences in body size. Rather, we suspect that physiological mechanisms are the basis for the observed differences in lifespan.

Age-related cellular changes in the long-lived bivalve A. islandica.

One of the biggest challenges to studying causes and effects of aging is identifying changes in cells that are related to senescence instead of simply the passing of chronological time. We investigated two populations of the longest living non-colonial metazoan, Arctica islandica, with lifespans that differed sixfolds. Of four investigated parameters (nucleic acid oxidation, protein oxidation, lipid oxidation, and protein instability), only nucleic acid oxidation increased with age and correlated with relative lifespan. Nucleic acid oxidation levels increased significantly faster and were significantly higher in the shorter-lived than the longer-lived population. In contrast, neither protein oxidation, lipid oxidation, nor protein stability changed over time. Protein resistance to unfolding stress when treated with urea was significantly lower overall in the shorter-lived population, and lipid peroxidation levels were higher in the longer-lived population. With the exception of nucleic acid oxidation, damage levels of A. islandica do not change with age, indicating excellent cellular maintenance in both populations. Since correlations between nucleic acid oxidation and age have also been shown previously in other organisms, and nucleic acid oxidation accumulation rate correlates with relative age in both investigated populations, nucleic acid oxidation may reflect intrinsic aging mechanisms.

Telomere-independent ageing in the longest-lived non-colonial animal, Arctica islandica.

The shortening of telomeres as a causative factor in ageing is a widely discussed hypothesis in ageing research. The study of telomere length and its regenerating enzyme telomerase in the longest-lived non-colonial animal on earth, Arctica islandica, should inform whether the maintenance of telomere length plays a role in reaching the extreme maximum lifespan (MLSP) of >500years in this species. Since longitudinal measurements on living animals cannot be achieved, a cross-sectional analysis of a short-lived (MLSP 40years from the Baltic Sea) and a long-lived population (MLSP 226years Northeast of Iceland) and in different tissues of young and old animals from the Irish Sea was performed. A high heterogeneity of telomere length was observed in investigated A. islandica over a wide age range (10-36years for the Baltic Sea, 11-194years for Irish Sea, 6-226years for Iceland). Constant telomerase activity and telomere lengths were detected at any age and in different tissues; neither correlated with age or population habitat. Stable telomere maintenance might contribute to the long lifespan of A. islandica. Telomere dynamics are no explanation for the distinct MLSPs of the examined populations and thus the cause of it remains to be investigated.

Life span evolution in eusocial workers--a theoretical approach to understanding the effects of extrinsic mortality in a hierarchical system.

While the extraordinary life span of queens and division of labor in eusocial societies have been well studied, it is less clear which selective forces act on the short life span of workers. The disparity of life span between the queen and the workers is linked to a basic issue in sociobiology: How are the resources in a colony allocated between colony maintenance and reproduction? Resources for somatic maintenance of the colony can either be invested into quality or quantity of workers. Here, we present a theoretical optimization model that uses a hierarchical trade-off within insect colonies and extrinsic mortality to explain how different aging phenotypes could have evolved to keep resources secure in the colony. The model points to the significance of two factors. First, any investment that would generate a longer intrinsic life span for workers is lost if the individual dies from external causes while foraging. As a consequence, risky environments favor the evolution of workers with a shorter life span. Second, shorter-lived workers require less investment than long-lived ones, allowing the colony to allocate these resources to sexual reproduction or colony growth.

Environmental challenges improve resource utilization for asexual reproduction and maintenance in hydra.

Variation in life history can reflect genetic differences, and may be caused by environmental effects on phenotypes. Understanding how these two sources of life history variation interact to express an optimal allocation of resources in a changing environment is central to life history theory. This study addresses variation in the allocation of resources to asexual reproduction and to maintenance of Hydra magnipapillata in relation to differences in temperature and food availability. Hydra is a non-senescent, persistent species with primarily clonal reproduction. We recorded changes in budding rate and mean survival under starvation, which indicate changes in the allocation of resources to asexual reproduction and maintenance. In constant conditions we observed a clear trade-off between asexual reproduction and maintenance, where budding increased linearly with food intake while starvation survival stayed rather constant. In contrast, an environment with fluctuations in temperature or food availability promotes maintenance and increases the survival chances of hydra under starvation. Surprisingly, asexual reproduction also tends to be positively affected by fluctuating environmental conditions, which suggests that in this case there is no clear trade-off between asexual reproduction and maintenance in hydra. Environmental stresses have a beneficial impact on the fitness-related phenotypical traits of the basal metazoan hydra. The results indicate that, if the stress occurs in hormetic doses, variable stressful and fluctuating environments can be salutary for hydra. A closer examination of this dynamic can therefore enable us to develop a deeper understanding of the evolution of aging and longevity.