High Extrinsic Mortality Research Articles

Balance between asymmetric allocation and repair of somatic damage in unicellular life forms as an ancient form of r/K selection

Over the course of multiple divisions, cells accumulate diverse nongenetic, somatic damage including misfolded and aggregated proteins and cell wall defects. If the rate of damage accumulation exceeds the rate of dilution through cell growth, a dedicated mitigation strategy is required to prevent eventual population collapse. Strategies for somatic damage control can be divided into two categories, asymmetric allocation and repair, which are not, in principle, mutually exclusive. We explore a mathematical model to identify the optimal strategy, maximizing the total cell number, over a wide range of environmental and physiological conditions. The optimal strategy is primarily determined by extrinsic, damage-independent mortality and the physiological model for damage accumulation that can be either independent (linear) or increasing (exponential) with respect to the prior accumulated damage. Under the linear regime, the optimal strategy is either exclusively repair or asymmetric allocation, whereas under the exponential regime, the optimal strategy is a combination of asymmetry and repair. Repair is preferred when extrinsic mortality is low, whereas at high extrinsic mortality, asymmetric damage allocation becomes the strategy of choice. We hypothesize that at an early stage of life evolution, optimization over repair and asymmetric allocation of somatic damage gave rise to r and K selection strategists.

Directional selection coupled with kin selection favors the establishment of senescence.

Conventional wisdom in evolutionary theory considers aging as a non-selected byproduct of natural selection. Based on this, conviction aging was regarded as an inevitable phenomenon. It was also thought that in the wild organisms tend to die from diseases, predation and other accidents before they could reach the time when senescence takes its course. Evidence has accumulated, however, that aging is not inevitable and there are organisms that show negative aging even. Furthermore, old age does play a role in the deaths of many different organisms in the wild also. The hypothesis of programmed aging posits that a limited lifespan can evolve as an adaptation (i.e., positively selected for) in its own right, partly because it can enhance evolvability by eliminating "outdated" genotypes. A major shortcoming of this idea is that non-aging sexual individuals that fail to pay the demographic cost of aging would be able to steal good genes by recombination from aging ones. Here, we show by a spatially explicit, individual-based simulation model that aging can positively be selected for if a sufficient degree of kin selection complements directional selection. Under such conditions, senescence enhances evolvability because the rate of aging and the rate of recombination play complementary roles. The selected aging rate is highest at zero recombination (clonal reproduction). In our model, increasing extrinsic mortality favors evolved aging by making up free space, thereby decreasing competition and increasing drift, even when selection is stabilizing and the level of aging is set by mutation-selection balance. Importantly, higher extrinsic mortality is not a substitute for evolved aging under directional selection either. Reduction of relatedness decreases the evolved level of aging; chance relatedness favors non-aging genotypes. The applicability of our results depends on empirical values of directional and kin selection in the wild. We found that aging can positively be selected for in a spatially explicit population model when sufficiently strong directional and kin selection prevail, even if reproduction is sexual. The view that there is a conceptual link between giving up clonal reproduction and evolving an aging genotype is supported by computational results.

Getting old gracefully, and risk of dying before getting there: a new guide to theory on extrinsic mortality and senescence

Do environments or species traits that lower the mortality of individuals create selection for delaying senescence? Reading the literature creates an impression that mathematically oriented biologists cannot agree on the validity of George Williams' prediction (who claimed 'yes'). The abundance of models and opinions may bewilder those that are new to the field. Here we provide heuristics as well as simple models that outline when the Williams prediction holds, why there is a ‘null model’ where extrinsic mortality does not change the evolution of senescence at all, and why it is also possible to expect the opposite of William’s prediction, where increased extrinsic mortality favours slower senescence. We hope to offer intuition by quantifying how much delaying the ‘placement’ of an offspring into the population reduces its expected contribution to the gene pool of the future. Our first example shows why sometimes increased extrinsic mortality has no effect (the null result), and why density dependence can change that. Thereafter, a model with ten different choices for population regulation shows that high extrinsic mortality favours fast life histories (Williams) if increasing density harms the production of juveniles or their chances to recruit into the population. If instead increasing density harms the survival of older individuals in a population, then high extrinsic mortality favours slow life histories (anti-Williams). We discuss the possibility that empirically found Williams-like patterns provide indirect evidence for population regulation operating via harming the production or fitness prospects of juveniles, as opposed to the survival of established breeders.

The correlated evolution of foraging mode and reproductive effort in lizards.

Life-history theory suggests that the optimal reproductive effort of an organism is affected by factors such as energy acquisition and predation risk. The observation that some organisms actively search for their prey and others ambush them creates the expectation of different energy needs and predation risk associated with each foraging behaviour, the so-called 'foraging-mode paradigm'. Although this paradigm has been around for decades, the empirical evidence consists of conflicting results derived from competing models based on different mechanisms. For instance, models within the foraging-mode paradigm suggest that widely foraging females have evolved low reproductive effort, because a heavy reproductive load decreases their ability to escape from predators. By contrast, a long-standing prediction of evolutionary theory indicates that organisms subject to high extrinsic mortality, should invest more in reproduction. Here, we present the first partial evidence that widely foraging species have evolved greater reproductive effort than have sit-and-wait species, which we attribute to a larger body size and greater mortality among mobile foragers. According to our findings, we propose a theoretical model that could explain the observed pattern in lizards, suggesting ways for evolutionary ecologists to test mechanistic hypotheses at the intraspecific level.

The sensitivity of a honeybee colony to worker mortality depends on season and resource availability

BackgroundHoneybees 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. In addition, threats to the health of honey bees and other social insects are typically measured at the individual level. To predict the effects of environmental change on social insect populations, we must understand how individual effects impact colony performance. 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.ResultsWe find that there are seasonal differences in honeybee colony elasticity to both senescent and extrinsic worker mortality. Colonies are most elastic to extrinsic (age-independent) nurse and forager mortality during periods of higher extrinsic mortality and resource availability but most elastic to age-dependent mortality during periods of lower extrinsic mortality and lower resource availability.ConclusionsThese 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 and improve our ability to model the effects of environmental change on social insect populations of economic or conservation concern.

Why so many Agta boys? Explaining 'extreme' sex ratios in Philippine foragers.

Male-biased sex ratios have been observed in multiple small-scale societies. Although intentional and systematic female-biased mortality has been posited as an explanation, there is often a lack of ethnographic evidence of systematic female neglect and/or infanticide. The Agta, a foraging population from the Philippines, have a skewed sex ratio of 1.29 (129 males per 100 females) aged 15 years or under. We hypothesised that this skew was not caused by greater female deaths, but due to an adaptive response, where more males were produced at birth in reaction to high male-biased extrinsic mortality. To test this hypothesis we utilise census, childcare and mortality data from 915 Agta. The Agta's sex ratio is significantly male-biased in the <1 (n = 48, 2:1) and 1-5 year (n = 170, 1.39:1) age cohorts; however, we find no evidence of systematic female neglect in patterns of childcare. Furthermore, the sex ratio decreases over cohorts, becoming balanced by the end of the juvenile period, owing to significantly higher male mortality. Taken together, these results are not supportive of female infanticide or neglect, and instead suggest an adaptive mechanism, acting in utero as a response to male-biased juvenile mortality, following Fisherian principles of equalising parental investment.

How Life History Shapes Optimal Patterns of Senescence: Implications from Individuals to Societies.

One evolutionary view of aging, the disposable soma theory, suggests that an organism's rate of senescence depends on the amount of energy invested in somatic maintenance. Since organisms have limited energy to allocate among growth, maintenance, and reproduction, the optimal amount of energy to invest in maintenance is influenced by the probability of death from extrinsic causes and the effect of somatic investment on survival. In eusocial animals, the disposable soma theory can be used to explain colonies' energy investment in the longevity of workers, who act as the somatic elements of a superorganism. There have been few theoretical considerations of how changes in the costliness of worker maintenance or in the effect of individual life span on group fitness influence a colony's investment in worker longevity. We develop a decision theory model to evaluate how changing the marginal costs and benefits of longevity and extrinsic mortality influence optimal worker life span in a social insect colony. Our model predicts that higher extrinsic mortality favors shorter life span. However, increased life span is favored when marginal benefits are an increasing function of longevity. In honeybees, this explains how greater somatic investment is sometimes favored despite high mortality. Our approach expands the disposable soma theory to make quantitative predictions about the selective pressures shaping senescence in social systems.

Reports of the Death of Extrinsic Mortality Moulding Senescence Have Been Greatly Exaggerated

The classic evolutionary theory of aging posits that senescence evolves because the weakening of selection with age allows mutations with late-acting deleterious effects to accumulate. Because extrinsic mortality is an important cause of weakening selection, the central prediction of the theory has been that higher extrinsic mortality should lead to the evolution of a higher rate of senescence. However, the validity of this prediction has been questioned, even to the extent of suggesting that it is not a prediction of the theory at all, primarily on the basis that changes in population growth rate will compensate for changes in extrinsic mortality. The implication is that empiricists have been using the wrong prediction to test the theory. This claim is misleading, however, because it does not apply on an evolutionary timescale, when population size must be roughly constant. With a constant population size, Hamilton’s fitness sensitivities show that extrinsic mortality determines the rate at which the strength of selection declines with age, and thus determines the rate of senescence. The central prediction has been confirmed in the few controlled experiments with model organisms that have been conducted, but clearly this is an area ripe for further investigation.

Repeated intraspecific divergence in life span and aging of African annual fishes along an aridity gradient.

Life span and aging are substantially modified by natural selection. Across species, higher extrinsic (environmentally related) mortality (and hence shorter life expectancy) selects for the evolution of more rapid aging. However, among populations within species, high extrinsic mortality can lead to extended life span and slower aging as a consequence of condition-dependent survival. Using within-species contrasts of eight natural populations of Nothobranchius fishes in common garden experiments, we demonstrate that populations originating from dry regions (with short life expectancy) had shorter intrinsic life spans and a greater increase in mortality with age, more pronounced cellular and physiological deterioration (oxidative damage, tumor load), and a faster decline in fertility than populations from wetter regions. This parallel intraspecific divergence in life span and aging was not associated with divergence in early life history (rapid growth, maturation) or pace-of-life syndrome (high metabolic rates, active behavior). Variability across four study species suggests that a combination of different aging and life-history traits conformed with or contradicted the predictions for each species. These findings demonstrate that variation in life span and functional decline among natural populations are linked, genetically underpinned, and can evolve relatively rapidly.

The effect of extrinsic mortality on genome size evolution in prokaryotes

Mortality has a significant role in prokaryotic ecology and evolution, yet the impact of variations in extrinsic mortality on prokaryotic genome evolution has received little attention. We used both mathematical and agent-based models to reveal how variations in extrinsic mortality affect prokaryotic genome evolution. Our results suggest that the genome size of bacteria increases with increased mortality. A high extrinsic mortality increases the pool of free resources and shortens life expectancy, which selects for faster reproduction, a phenotype we called ‘scramblers’. This phenotype is realised by the expansion of gene families involved in nutrient acquisition and metabolism. In contrast, a low mortality rate increases an individual’s life expectancy, which results in natural selection favouring tolerance to starvation when conditions are unfavourable. This leads to the evolution of small, streamlined genomes (‘stayers’). Our models predict that large genomes, gene family expansion and horizontal gene transfer should be observed in prokaryotes occupying ecosystems exposed to high abiotic stress, as well as those under strong predator- and/or pathogen-mediated selection. A comparison of genome size of cyanobacteria in relatively stable marine versus more turbulent freshwater environments corroborates our predictions, although other factors between these environments could also be responsible.

Evolutionary theory of ageing and the problem of correlated Gompertz parameters

The Gompertz mortality model is often used to evaluate evolutionary theories of ageing, such as the Medawar–Williams' hypothesis that high extrinsic mortality leads to faster ageing. However, fits of the Gompertz mortality model to data often find the opposite result that mortality is negatively correlated with the rate of ageing. This negative correlation has been independently discovered in several taxa and is known in actuarial studies of ageing as the Strehler–Mildvan correlation. We examine the role of mortality selection in determining late-life variation in susceptibility to death, which has been suggested to be the cause of this negative correlation. We demonstrate that fixed-frailty models that account for heterogeneity in frailty do not remove the correlation and that the correlation is an inherent statistical property of the Gompertz distribution. Linking actuarial and biological rates of ageing will continue to be a pressing challenge, but the Strehler–Mildvan correlation itself should not be used to diagnose any biological, physiological, or evolutionary process. These findings resolve some key tensions between theory and data that affect evolutionary and biological studies of ageing and mortality. Tests of evolutionary theories of ageing should include direct measures of physiological performance or condition.

Growth trajectories in wild geladas (Theropithecus gelada).

Life history and socioecological factors have been linked to species-specific patterns of growth across female vertebrates. For example, greater maternal investment in offspring has been associated with more discrete periods of growth and reproduction. However, in primates it has been difficult to test such hypotheses because very few studies have obtained growth measurements from wild populations. Here we utilize a promising noninvasive photogrammetric method-parallel lasers-to examine shoulder-rump (SR) growth in a wild primate, the gelada (Theropithecus gelada, Simien Mountains National Park, Ethiopia). In this species, a graminivorous diet coupled with high extrinsic infant mortality risk suggests that maternal investment in neonates is low. Therefore, in contrast with other closely related papionins, we expected female geladas to exhibit less discrete periods of growth and reproduction. For both sexes, we compared size-for-age patterns (N = 154 females; N = 110 males) and changes in growth velocity relative to major life history milestones. Female geladas finished 88.5% of SR growth by first sexual swelling, and 97.2% by first reproduction, reaching adult body size by 7.72 years of age. Compared to closely related papionins, gelada females finished more growth by first reproduction, despite producing relatively small, and presumably "cheap," neonates. Male geladas finished 85.4% of growth at dispersal, and 96.0% at estimated first birth. Contrary to other polygynous primates, males are larger than females because they grow for a longer period of time (not because they grow faster), surpassing females around 6 years of age when female growth slows. Our results demonstrate that parallel lasers are an easy and promising new method that can be used to construct comprehensive life history perspectives that were once out of reach for wild populations. Am. J. Primatol. 78:707-719, 2016. © 2016 Wiley Periodicals, Inc.

A ‘slow pace of life’ in Australian old-endemic passerine birds is not accompanied by low basal metabolic rates

Life history theory suggests that species experiencing high extrinsic mortality rates allocate more resources toward reproduction relative to self-maintenance and reach maturity earlier ('fast pace of life') than those having greater life expectancy and reproducing at a lower rate ('slow pace of life'). Among birds, many studies have shown that tropical species have a slower pace of life than temperate-breeding species. The pace of life has been hypothesized to affect metabolism and, as predicted, tropical birds have lower basal metabolic rates (BMR) than temperate-breeding birds. However, many temperate-breeding Australian passerines belong to lineages that evolved in Australia and share 'slow' life-history traits that are typical of tropical birds. We obtained BMR from 30 of these 'old-endemics' and ten sympatric species of more recently arrived passerine lineages (derived from Afro-Asian origins or introduced by Europeans) with 'faster' life histories. The BMR of 'slow' temperate-breeding old-endemics was indistinguishable from that of new-arrivals and was not lower than the BMR of 'fast' temperate-breeding non-Australian passerines. Old-endemics had substantially smaller clutches and longer maximal life spans in the wild than new arrivals, but neither clutch size nor maximum life span was correlated with BMR. Our results suggest that low BMR in tropical birds is not functionally linked to their 'slow pace of life' and instead may be a consequence of differences in annual thermal conditions experienced by tropical versus temperate species.

Developmental energetics, sibling death, and parental instability as predictors of maturational tempo and life history scheduling in males from Cebu, Philippines.

Cross-species comparisons show that high extrinsic mortality favors the evolution of "faster" life histories. There is interest in applying this principle to human life history plasticity, based on the idea that psychosocial stressors that correlate with extrinsic mortality accelerate reproductive pace. Most prior studies have been conducted in settings in which psychosocial stressors co-occur with the maturation-accelerating influence of nutritional abundance. We evaluate cues of local mortality (sibling death) or low parental investment (paternal instability; maternal absence) and energetic measures during development as predictors of life history scheduling among males (n = 754) in a Philippine population with marginal developmental nutritional. Males who had more favorable nutritional status during childhood, as reflected in linear growth, skinfold thickness, and caloric intake, were more maturationally advanced in adolescence (all P < 0.05). Taller stature and higher caloric intake during childhood also predicted earlier ages at first sex (both P < 0.01), which persisted after controlling for the effect of nutrition on pubertal maturation. While psychosocial stressors did not predict accelerated maturation, males who as children grew up with an unstable paternal presence had sex earlier (P < 0.05) and tended to become fathers sooner than those with a stable fatherly presence. Those who had a sibling die became fathers sooner than those who did not (P < 0.05). Our findings point to important energetic constraints on the onset of reproductive maturity, while psychosocial stressors accelerate entry to parenthood, which may be comparatively more socially, rather than biologically, constrained. Am J Phys Anthropol 158:175-184, 2015. © 2015 Wiley Periodicals, Inc.

Effects of Extrinsic Mortality on the Evolution of Aging: A Stochastic Modeling Approach

The evolutionary theories of aging are useful for gaining insights into the complex mechanisms underlying senescence. Classical theories argue that high levels of extrinsic mortality should select for the evolution of shorter lifespans and earlier peak fertility. Non-classical theories, in contrast, posit that an increase in extrinsic mortality could select for the evolution of longer lifespans. Although numerous studies support the classical paradigm, recent data challenge classical predictions, finding that high extrinsic mortality can select for the evolution of longer lifespans. To further elucidate the role of extrinsic mortality in the evolution of aging, we implemented a stochastic, agent-based, computational model. We used a simulated annealing optimization approach to predict which model parameters predispose populations to evolve longer or shorter lifespans in response to increased levels of predation. We report that longer lifespans evolved in the presence of rising predation if the cost of mating is relatively high and if energy is available in excess. Conversely, we found that dramatically shorter lifespans evolved when mating costs were relatively low and food was relatively scarce. We also analyzed the effects of increased predation on various parameters related to density dependence and energy allocation. Longer and shorter lifespans were accompanied by increased and decreased investments of energy into somatic maintenance, respectively. Similarly, earlier and later maturation ages were accompanied by increased and decreased energetic investments into early fecundity, respectively. Higher predation significantly decreased the total population size, enlarged the shared resource pool, and redistributed energy reserves for mature individuals. These results both corroborate and refine classical predictions, demonstrating a population-level trade-off between longevity and fecundity and identifying conditions that produce both classical and non-classical lifespan effects.

Phenoptosis as genetically determined aging influenced by signals from the environment

Aging is a complex and not well understood process. Two opposite concepts try to explain its causes and mechanisms - programmed aging and aging of "wear and tear" (stochastic aging). To date, much evidence has been obtained that contradicts the theories of aging as being due to accumulation of various damages. For example, creation of adequate conditions for the functioning of the organism's components (appropriate microenvironment, humoral background, etc.) has been shown to cause partial or complete reversibility of signs of its aging. Programmed aging and death of an organism can be termed phenoptosis by analogy to the term apoptosis for programmed cell death (this term was first suggested by V. P. Skulachev). The necessity of this phenomenon, since A. Weismann, has been justified by the need for population renewal according to ecological and evolutionary requirements. Species-specific lifespan, age-dependent changes in expression pattern of genes, etc. are compatible with the concept of phenoptosis. However, the intraspecific rate of aging was shown to vary over of a wide range depending on living conditions. This means that the "aging program" is not set rigidly; it sensitively adjusts an individual to the specific realities of its habitat. Moreover, there are indications that in rather severe conditions of natural habitat the aging program can be completely cancelled, as the need for it disappears because of the raised mortality from external causes (high extrinsic mortality), providing fast turnover of the population.

The worm that lived: Evolution of rapid aging under high extrinsic mortality revisited.

Organisms age because of the “selection shadow”—the decline of the force of natural selection with age. Seemingly straightforward corollary of this theory is the Medawar-Williams prediction, which maintains that increased extrinsic (non-aging) mortality will result in the evolution of accelerated aging and decreased longevity. Despite its centrality to modern thinking about the ultimate causes of aging, this prediction ignores the fact that mortality is often a non-random process depending on individual condition. Increased condition-dependent mortality inescapably results in increased selection for resistance against the agent of mortality. Provided that resistance to various stressors is commonly associated with increased longevity, the evolutionary outcome is no longer certain. We recently documented this experimentally by showing that populations of Caenorhabditis remanei evolved to live shorter under high extrinsic mortality, but only when mortality was applied haphazardly. On the contrary, when extrinsic mortality was caused by heat-shock, populations experiencing the same rate of increased mortality evolved greater longevities, notwithstanding increased “selection shadow.” Intriguingly, stress-resistant and long-lived worms were also more fecund. We discuss these results in the light of recent theoretical developments, such as condition-environment interactions and hyperfunction theory of aging.

Longer Life Span Evolves under High Rates of Condition-Dependent Mortality

Aging affects nearly all organisms, but how aging evolves is still unclear. The central prediction of classic theory is that high extrinsic mortality leads to accelerated aging and shorter intrinsic life span. However, this prediction considers mortality as a random process, whereas mortality in nature is likely to be condition dependent. Therefore, the novel theory maintains that condition dependence may dramatically alter, and even reverse, the classic pattern. We present experimental evidence for the evolution of longer life span under high condition-dependent mortality. We employed an experimental evolution design, using a nematode, Caenorhabditis remanei, that allowed us to disentangle the effects of mortality rate (high versus low) and mortality source (random versus condition dependent). We observed the evolution of shorter life span under high random mortality, confirming the classic prediction. In contrast, high condition-dependent mortality led to the evolution of longer life span, supporting a key role of condition dependence in the evolution of aging. This life-span extension was not the result of a trade-off with reproduction. By simultaneously corroborating the classic results [8-10] and providing the first experimental evidence for the novel theory, our study resolves apparent contradictions in the study of aging and challenges the traditional paradigm by demonstrating that condition-environment interactions dictate the evolutionary trajectory of aging.

Resource Availability, Mortality, and Fertility: A Path Analytic Approach to Global Life-History Variation

Humans exhibit considerable diversity in timing and rate of reproduction. Life-history theory (LHT) suggests that ecological cues of resource richness and survival probabilities shape human phenotypes across populations. Populations experiencing high extrinsic mortality due to uncertainty in resources should exhibit faster life histories. Here we use a path analytic (PA) approach informed by LHT to model the multiple pathways between resources, mortality rates, and reproductive behavior in 191 countries. Resources that account for the most variance in population mortality rates are predicted to explain the most variance in total fertility rates. Results indicate that resources (e.g., calories, sanitation, education, and health-care expenditures) influence fertility rates in paths through communicable and noncommnunicable diseases. Paths acting through communicable disease are more strongly associated with fertility than are paths through noncommunicable diseases. These results suggest that a PA approach may help disaggregate extrinsic and intrinsic mortality factors in cross-cultural analyses. Such knowledge may be useful in developing targeted policies to decrease teenage pregnancy, total fertility rates, and thus issues associated with overpopulation.

Resource Availability, Mortality, and Fertility: A Path Analytic Approach to Global Life-History Variation

Humans exhibit considerable diversity in timing and rate of reproduction. Life-history theory (LHT) suggests that ecological cues of resource richness and survival probabilities shape human phenotypes across populations. Populations experiencing high extrinsic mortality due to uncertainty in resources should exhibit faster life histories. Here we use a path analytic (PA) approach informed by LHT to model the multiple pathways between resources, mortality rates, and reproductive behavior in 191 countries. Resources that account for the most variance in population mortality rates are predicted to explain the most variance in total fertility rates. Results indicate that resources (e.g., calories, sanitation, education, and health-care expenditures) influence fertility rates in paths through communicable and noncommunicable diseases. Paths acting through communicable disease are more strongly associated with fertility than are paths through noncommunicable diseases. These results suggest that a PA approach may help disaggregate extrinsic and intrinsic mortality factors in cross-cultural analyses. Such knowledge may be useful in developing targeted policies to decrease teenage pregnancy, total fertility rates, and thus issues associated with overpopulation.