Ralf Schaible

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

Significance How an organism changes with age and why the pattern of change differs across species are questions that have intrigued biologists since Aristotle. Patterns of change can be described by trajectories of birth and death rates over age. For humans and many other mammals, mortality increases and fertility declines with age among adults. For other species, however, a remarkable variety of patterns has been observed. Although roughly constant mortality and fertility trajectories have been reported for some species, the data are problematic because sample sizes are small, especially at older ages. Here, we present compelling evidence for constant mortality and reproduction of Hydra using data from careful, large-scale studies over 8 y with 2,256 individuals. 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.

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.

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.

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.

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.

Genetic characterisation of sexually and parthenogenetically reproductive populations of Chara canescens (Charophyceae) using AFLP, rbcL, and SNP markers

R. Schaible, I. Bergmann, M. Bögle, A. Schoor and H. Schubert. 2009. Genetic characterisation of sexually and parthenogenetically reproductive populations of Chara canescens (Charophyceae) using AFLP, rbcL, and SNP markers. Phycologia 48: 105–117. DOI: 10.2216/08-58.1 Parthenogenetically reproducing Chara canescens (Charophyceae) populations have been described from several European locations. Sexually reproducing populations with female and male individuals are known only from the Neusiedler See located in Seewinkel National Park, Austria. Sexual and parthenogenetic populations probably coexist in this area, but no morphological attribute is known to differentiate between females of the two reproductive modes. To find markers associated with parthenogenesis, DNA samples from individuals of both reproductive modes were screened via amplified fragment length polymorphism (AFLP) analysis. Although no unique monomorphic loci for the reproduction systems could be identified, neighbour-joining analysis separated the individuals into two groups representing the two reproductive modes. The rbcL gene sequence analysis also revealed two nucleotide differences among these groups. Sequence characterization of the flanking region of one microsatellite locus from C. canescens individuals identified one insertion/deletion (indel) between the reproductive modes. This indel was converted via polymerase chain reaction into a marker associated with sexual reproduction. Further analysis of the AFLP data showed a high level of polymorphism and genetic diversity between and within populations of the reproductive modes. A larger sample size is needed to confirm the gene pool cluster and the degree of genetic diversity between the reproductive modes finally, but the successful development of a promising marker system for the reproduction mode provides a tool for future research to characterise geographical parthenogenesis of C. canescens in detail.

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.

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.

The occurrence of sexual Chara canescens populations (Charophyceae) is not related to ecophysiological potentials with respect to salinity and irradiance

Ecophysiological characteristics of a sexual population of Chara canescens from Austria (NS) were compared with those from a parthenogenetical propagating population of the Baltic Sea (BS) to find out whether differences in salinity or irradiance acclimation abilities are responsible for the absence of male organisms in the Baltic Sea. Growth, photosynthesis main characteristics and pigmentation were examined at two irradiance levels and four salinities. Shoot elongations were highest for all specimens from both populations at low salinities. Reduction of growth at 12.4 PSU was less pronounced for NS female algae, whereas BS female and NS male algae showed strong growth reduction. Algae from NS had highest Pmax (maximum photosynthesis rate) and α-values (efficiency of light utilization at limiting irradiance) at 1.9 PSU, strongly decreasing at higher salinities. Both parameters were independent of salinity for BS algae. No significant differences between the experimental groups were found with respect to irradiance acclimation. Our results indicate that the absence of male C. canescens in the Baltic Sea is not related to sex-specific ecophysiological characteristics.