Maciej J. Dańko

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.

Mutation accumulation may be a minor force in shaping life history traits.

Is senescence the adaptive result of tradeoffs between younger and older ages or the nonadaptive burden of deleterious mutations that act at older ages? To shed new light on this unresolved question we combine adaptive and nonadaptive processes in a single model. Our model uses Pennas bit-strings to capture different age-specific mutational patterns. Each pattern represents a genotype and for each genotype we find the life history strategy that maximizes fitness. Genotypes compete with each other and are subject to selection and to new mutations over generations until equilibrium in gene-frequencies is reached. The mutation-selection equilibrium provides information about mutational load and the differential effects of mutations on a life history trait - the optimal age at maturity. We find that mutations accumulate only at ages with negligible impact on fitness and that mutation accumulation has very little effect on the optimal age at maturity. These results suggest that life histories are largely determined by adaptive processes. The non-adaptive process of mutation accumulation seems to be unimportant at evolutionarily relevant ages.

How perceived predation risk shapes patterns of aging in water fleas

Predation is an important selection pressure which shapes aging patterns in natural populations, and it is also a significant factor in the life history decisions of individuals. Exposure to the perceived threat of size-dependent fish predation has been shown to trigger adaptive responses in animal life history including an increase in early reproductive output. In water fleas, this response to perceived predation risk appears to have a cost, as a lifespan in an environment free of predation cues is 20% longer. The aim of this study is to establish the biodemographic basis of phenotypic differences in the water flea lifespan which are induced by the cues of fish predation. We examined mortality by fitting the Gompertz-Makeham model of mortality to large cohorts of two cladoceran species, Daphnia longispina and Diaphanosoma brachyurum. Our findings indicate that perceived exposure to the threat of fish predation (induced through chemical cues) only accelerated the rate of aging in Diaphanosoma, and not in Daphnia where the treatment led to an earlier onset of aging. The second of these two phenotypic responses is consistent with the genetically based differences between Daphnia from habitats that differ with respect to predation risk. In contrast, the response of Diaphanosoma demonstrates that the cue of extrinsic mortality-in this case, fish predation-is a key factor in shaping these cladoceran life histories in the wild, and is one of the few interventions which has been shown to induce a plastic change in the rate of aging.

Mutation accumulation may only be a minor force in shaping life-history traits, even when reproduction is sexual.

In a previous theoretical study we investigated whether adaptive or non-adaptive processes are more important in the evolution of senescence. We built a model that combined both processes and found that mutation accumulation is important only at those ages where mortality has a negligible impact on fitness. This model, however, was limited to haploid organisms. Here we extend our model by introducing diploidy and sexual reproduction. We assume that only recessive (mutated) homozygotes experience detrimental effects. Our results corroborate our previous conclusions, confirming that life histories are largely determined by adaptive processes. We also found that the equilibrium frequencies of mutated alleles are at higher values than in haploid model, because mutations in heterozygotes are hidden for directional selection. Nevertheless, the equilibrium frequencies of recessive homozygotes that make mutations visible to selection are very similar to the equilibrium frequencies of these alleles in our haploid model. Diploidy and sexual reproduction with recombination slows down approaching selection-mutation balance.

Age-related changes of physiological performance and survivorship of bank voles selected for high aerobic capacity

ABSTRACT Variation in lifespans is an intriguing phenomenon, but how metabolic rate influence this variation remains unclear. High aerobic capacity can result in health benefits, but also in increased oxidative damage and accelerated ageing. We tested these contradictory predictions using bank voles (Myodes = Clethrionomys glareolus) from lines selected for high swim‐induced aerobic metabolism (A), which had about 50% higher maximum metabolic rate and a higher basal and routine metabolic rates, than those from unselected control lines (C). We measured sprint speed (VSmax), forced‐running maximum metabolic rate (VO2run), maximum long‐distance running speed (VLmax), running speed at VO2run (VVO2), and respiratory quotient at VO2run (RQ) at three age classes (I: 3–5, II: 12–14, III: 17–19 months), and analysed survivorship. We asked if ageing, understood as the age‐related decline of the performance traits, differs between the A and C lines. At age class I, voles from A lines had 19% higher VO2run, and 12% higher VLmax, but tended to have 19% lower VSmax, than those from C lines. RQ was nearly 1.0 for both A and C lines. The pattern of age‐related changes differed between the lines mainly between age classes I and II, but not in older animals. VSmax increased by 27% in A lines and by 10% in C lines between age class I and II, but between classes II and III, it increased by 16% in both selection directions. VO2run decreased by 7% between age class I and II in A lines only, but in C lines it remained constant across all age classes. VLmax decreased by 8% and VVO2 by 12% between age classes II and III, but similarly in both selection directions. Mortality was higher in A than in C lines only between the age of 1 and 4 months. The only trait for which the changes in old animals differed between the lines was RQ. In A lines, RQ increased between age classes II and III, whereas in C lines such an increase occurred between age classes I and II. Thus, we did not find obvious effects of selection on the pattern of ageing. However, the physiological performance and mortality of bank voles remained surprisingly robust to ageing, at least until the age of 17–19 months, similar to the maximum lifespan under natural conditions. Therefore, it is possible that the selection could affect the pattern of ageing in even older individuals when symptoms of senility might be more profound. HighlightsBank voles selected for high swim‐induced metabolism had increased aerobic capacity.Several other physiological performance traits were increased in selected voles.Age‐related detrimental changes were observed only in some of the performance traits.For most of the traits the deteriorations were similar in selected and control voles.The selection did not cause clear and strong changes in the rate of ageing process.

Density-dependence interacts with extrinsic mortality in shaping life histories

The role of extrinsic mortality in shaping life histories is poorly understood. However, substantial evidence suggests that extrinsic mortality interacts with density-dependence in crucial ways. We develop a model combining Evolutionarily Stable Strategies with a projection matrix that allows resource allocation to growth, tissue repairs, and reproduction. Our model examines three cases, with density-dependence acting on: (i) mortality, (ii) fecundity, and (iii) production rate. We demonstrate that density-independent extrinsic mortality influences the rate of aging, age at maturity, growth rate, and adult size provided that density-dependence acts on fertility or juvenile mortality. However, density-independent extrinsic mortality has no effect on these life history traits when density-dependence acts on survival. We show that extrinsic mortality interacts with density-dependence via a compensation mechanism: the higher the extrinsic mortality the lower the strength of density-dependence. However, this compensation fully offsets the effect of extrinsic mortality only if density-dependence acts on survival independently of age. Both the age-pattern and the type of density-dependence are crucial for shaping life history traits.

Latitudinal and age-specific patterns of larval mortality in the damselfly Lestes sponsa: Senescence before maturity?

Abstract Latitudinal differences in life history traits driven by differences in seasonal time constraints have been widely documented. Yet, latitudinal patterns in (age‐specific) mortality rates have been poorly studied. Here, we studied latitudinal differences in pre‐adult age‐specific mortality patterns in the strictly univoltine damselfly Lestes sponsa. We compared individuals from three latitudes reared from the egg stage in the laboratory at temperatures and photoperiods simulating those at the latitude of origin (main experiment) and under common‐garden conditions at a fixed temperature and photoperiod (supplementary experiment). Results from the main experiment showed that the high‐latitude population exhibited higher mortality rates than the central and southern populations, likely reflecting a cost of their faster development. Age‐specific mortality patterns, also indicated higher ageing rates in the high‐latitude compared to the low‐latitude population, which likely had a genetic basis. The strong within‐population variation in hatching dates in the low‐latitude population caused variation in mortality rates; individuals that hatched later showed higher mortality rates presumably due to their shorter development times compared to larvae that hatched earlier. In both experiments, larvae from all three latitudes showed accelerated mortality rates with age, which is consistent with a pattern of senescence before adulthood. HighlightsPopulations at high latitudes face higher time constraints and develop faster.We studied effects of time constraints on accelerated ageing in damselfly larvae.The high‐latitude population exhibited higher mortality rates and ageing rates.Late hatched individuals showed higher mortality rates.All populations showed accelerated mortality rates with age in the larval stage.

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.

ungroup: An R package for efficient estimation of smooth distributions from coarsely binned data

ungroup is an open source software library written in the R programming language (R Core Team, 2018) that introduces a versatile method for ungrouping histograms (binned count data) assuming that counts are Poisson distributed and that the underlying sequence over a fine grid to be estimated is smooth. The method is based on the composite link model (Thompson & Baker, 1981) and estimation is achieved by maximizing a penalized likelihood (P. H. Eilers, 2007), which extends standard generalized linear models. The penalized composite link model (PCLM) implements the idea that observed counts, interpreted as realizations from Poisson distributions, are indirect observations of a finer (ungrouped) but latent sequence. This latent sequence represents the distribution of expected means on a fine resolution and has to be estimated from the aggregated data. Estimates are obtained by maximizing a penalized likelihood. This maximization is performed efficiently by a version of the iteratively re-weighted least-squares algorithm. Optimal values of the smoothing parameter are chosen by minimizing Bayesian or Akaike’s Information Criterion (Hastie & Tibshirani, 1990).

Extrinsic Mortality Can Shape Life-History Traits, Including Senescence

The Williams’ hypothesis is one of the most widely known ideas in life history evolution. It states that higher adult mortality should lead to faster and/or earlier senescence. Theoretically derived gradients, however, do not support this prediction. Increased awareness of this fact has caused a crisis of misinformation among theorists and empirical ecologists. We resolve this crisis by outlining key issues in the measurement of fitness, assumptions of density dependence, and their effect on extrinsic mortality. The classic gradients apply only to a narrow range of ecological contexts where density-dependence is either absent or present but with unrealistic stipulations. Re-deriving the classic gradients, using a more appropriate measure of fitness and incorporating density, shows that broad ecological contexts exist where Williams’ hypothesis is supported.