The Danaid Theory of Aging

The classical evolutionary theories of aging suggest that aging evolves due to insufficient selective pressure against it. In these theories, declining selection pressure with age leads to aging through genes or resource allocations, implying that aging could potentially be stalled were genes, resource allocation, or selection pressure somewhat different. While these classical evolutionary theories are undeniably part of a description of the evolution of aging, they do not explain the diversity of aging patterns, and they do not constitute the only possible evolutionary explanation. Without denying selection pressure a role in the evolution of aging, we argue that the origin and diversity of aging should also be sought in the nature and evolution of organisms that are, from their very physiological make up, unmaintainable. Drawing on advances in developmental biology, genetics, biochemistry, and complex systems theory since the classical theories emerged, we propose a fresh evolutionary-mechanistic theory of aging, the Danaid theory. We argue that, in complex forms of life like humans, various restrictions on maintenance and repair may be inherent, and we show how such restrictions are laid out during development. We further argue that there is systematic variation in these constraints across taxa, and that this is a crucial factor determining variation in aging and lifespan across the tree of life. Accordingly, the core challenge for the field going forward is to map and understand the mosaic of constraints, trade-offs, chance events, and selective pressures that shape aging in diverse ways across diverse taxa.

Evolution, Chance, and Aging

Aging has provided fruitful challenges for evolutionary theory, and evolutionary theory has deepened our understanding of aging. A great deal of genetic and molecular data now exists concerning mortality regulation and there is a growing body of knowledge concerning the life histories of diverse species. Assimilating all relevant data into a framework for the evolution of aging promises to significantly advance the field. We propose extensions of some key concepts to provide greater precision when applying these concepts to age-structured contexts. Secondary or byproduct effects of mutations are proposed as an important factor affecting survival patterns, including effects that may operate in small populations subject to genetic drift, widening the possibilities for mutation accumulation and pleiotropy. Molecular and genetic studies have indicated a diverse array of mechanisms that can modify aging and mortality rates, while transcriptome data indicate a high level of tissue and species specificity for genes affected by aging. The diversity of mechanisms and gene effects that can contribute to the pattern of aging in different organisms may mirror the complex evolutionary processes behind aging.

Predation has small, short-term, and in certain conditions random effects on the evolution of aging

Background The pace of aging varies considerably in nature. The best-known explanation of the evolution of specific rates of aging is the Williams’ hypothesis suggesting that the aging rate should correlate with the level of extrinsic mortality. However, the current evidence is inconclusive with various examples where the Williams' hypothesis seems to be correct and where it doesn’t. Here we explore the relationship between extrinsic mortality and aging rate by developing a simulation model of the evolution of aging rate in prey subject to predation. Results Our results suggest that more intense predation leads to the evolution of faster pace of aging in prey. However, this effect slowly vanishes when the predator diet breadth is allowed to evolve, too. Furthermore, in our model, the evolution of a specific aging rate is driven mainly by a single parameter, the strength of a trade-off between aging and fecundity. Indeed, in the absence of this trade-off the evolutionary impacts of predation on the prey aging rate appear random. Conclusions We show that the William’s hypothesis appears valid when there is a trade-off between aging and fecundity and predators and prey do not coevolve. However, we also show that when the prey and predators coevolve or if there is no trade-off between aging and fecundity the William`s hypothesis is no longer applicable.

Eusociality and the evolution of aging in superorganisms

Eusocial insects ants, bees, wasps and termites are being recognized as model organisms to unravel the evolutionary paradox of aging for two reasons: (1) queens (and kings, in termites) of social insects outlive similar sized solitary insects by up to several orders of magnitude; (2) all eusocial taxa show a divergence of long queen and shorter worker lifespans, despite their shared genomes and even under risk-free laboratory environments. Traditionally, these observations have been explained by invoking classical evolutionary aging theory: well-protected inside their nests, queens are much less exposed to external hazards than foraging workers, and this provides natural selection the opportunity to favor queens that perform well at advanced ages. Although quite plausible, these verbal arguments have not been backed up by mathematical analysis. Here, for the first time, we provide quantitative models for the evolution of caste specific aging patterns. We show that caste-specific mortality risks are in general neither sufficient nor necessary to explain the evolutionary divergence in lifespan between queens and workers and the extraordinary queen lifespans. Reproductive monopolization and the delayed production of sexual offspring in highly social colonies lead natural selection to inherently favor queens that live much longer than workers, even when exposed to the same external hazards. Factors that reduce a colony's reproductive skew, such as polygyny and worker reproduction, tend to reduce the evolutionary divergence in lifespan between queens and workers. Caste-specific extrinsic hazards also affect lifespan divergence but to a much smaller extent than reproductive monopolization.

The Intersectionality of Person, Space, and Time for Understanding Aging in Place

Aging in place is interpreted differently across times and disciplines in the literature. Multiple interpretations of aging in place can lead to differences in expectations and goals when planning products, services, and technologies for older adults. We conducted a historical review across databases in the fields of anthropology, architecture, gerontol-ogy, medicine, psychology, and sociology to explore the evolution of ‘aging in place’ term across time and disciplines. We included articles that used the terminology “aging in place” or “ageing in place” in titles, abstracts, keywords, or subject. From the aging in place definition excerpts collected, we identified the preliminary themes and grouped them into three main themes: people, space, and time. Although the narrative of aging in place is highly related to living spaces, the cause and influencing factors are tied beyond the space. Person and time-related factors that are related to the aging experience im-pact the way aging in place is defined. When designing products, services, and technolo-gies to support successful aging in place, designers, researchers, policymakers, and care-givers should be aware that aging in place is at the intersection of personal, spatial, and temporal elements of older adults’ lives. Based on the multiple perspectives of disci-plines, we concluded that aging in place is beyond the matter of location, but also takes into account the person’s capacity and the changes over the person’s lifespan. Founda-tional understanding of the multiple factors that influence aging in place is critical to support older adults to have a healthy and optimal aging experience.

Aging, Life History, and Human Evolution

Aging occurs in all sexually reproducing organisms. That is, physical degradation over time occurs from conception until death. While the life span of a species is often viewed as a benchmark of aging, the pace and intensity of physical degradation over time varies owing to environmental influences, genetics, allocation of energetic investment, and phylogenetic history. Significant variation in aging within mammals, primates, and great apes, including humans, is therefore common across species. The evolution of aging in the hominin lineage is poorly known; however, clues can be derived from the fossil record. Ongoing advances continue to shed light on the interactions between life-history variables such as reproductive effort and aging. This review presents our current understanding of the evolution of aging in humans, drawing on population variation, comparative research, trade-offs, and sex differences, as well as tissue-specific patterns of physical degradation. Implications for contemporary health challenges and the future of human evolutionary anthropology research are also discussed.

Deleterious mutations show increasing negative effects with age in Drosophila melanogaster

Background In order for aging to evolve in response to a declining strength of selection with age, a genetic architecture that allows for mutations with age-specific effects on organismal performance is required. Our understanding of how selective effects of individual mutations are distributed across ages is however poor. Established evolutionary theories assume that mutations causing aging have negative late-life effects, coupled to either positive or neutral effects early in life. New theory now suggests evolution of aging may also result from deleterious mutations with increasing negative effects with age, a possibility that has not yet been empirically explored. Results To directly test how the effects of deleterious mutations are distributed across ages, we separately measure age-specific effects on fecundity for each of 20 mutations in Drosophila melanogaster. We find that deleterious mutations in general have a negative effect that increases with age and that the rate of increase depends on how deleterious a mutation is early in life. Conclusions Our findings suggest that aging does not exclusively depend on genetic variants assumed by the established evolutionary theories of aging. Instead, aging can result from deleterious mutations with negative effects that amplify with age. If increasing negative effect with age is a general property of deleterious mutations, the proportion of mutations with the capacity to contribute towards aging may be considerably larger than previously believed.

The Sensitivity of a Honeybee Colony to Worker Mortality Depends on Season and Resource Availability

Background: Honeybees have extraordinary phenotypic plasticity in their senescence rate, making them a fascinating model system for the evolution of aging. Seasonal variation in senescence and extrinsic mortality results in a tenfold increase in worker life expectancy in winter as compared to summer. To understand the evolution of this remarkable pattern of aging, we must understand how individual longevity scales up to effects on the entire colony. We develop a matrix model of colony demographics to ask how worker age-dependent and age-independent mortality affect colony fitness and how these effects differ by seasonal conditions.Results: We find that there are seasonal differences in honeybee colony sensitivity to both senescent and extrinsic worker mortality. Colonies are most sensitive to extrinsic (age-independent) nurse and forager mortality during periods of higher extrinsic mortality and resource availability but most sensitive to age-dependent mortality during periods of lower extrinsic mortality and lower resource availability.Conclusions: These results suggest that seasonal changes in the strength of selection on worker senescence partly explain the observed pattern of seasonal differences in worker aging in honey bees. More broadly, these results extend our understanding of the role of extrinsic mortality in the evolution of senescence to social animals.

Predation Has Small, Short-Term, and in Certain Conditions Random Effect on the Evolution of Aging

The pace of aging varies considerably in nature. Historically, scientists focused mostly on why and how has aging evolved, while only a few studies explored mechanisms driving evolution of specific rates of aging. Here we develop an agent-based model simulating evolution of aging in prey subject to predation. Our results suggest that predation affects the pace of aging in prey only if young, vivid animals are not much more likely to escape predators than the old ones. However, even this effect slowly vanishes when the predator diet composition evolves, too. Furthermore, evolution of a specific aging rate, in our model, is driven mainly by a single parameter, the strength of a trade-off between aging and fecundity. Indeed, in absence of this trade-off the evolutionary impacts of predation on the prey aging rate appear random. Our model produces several testable predictions which may be useful for other areas of aging research.