Demographic variability and heterogeneity among individuals within and among clonal bacteria strains

Identifying what drives individual heterogeneity has been of long interest to ecologists, evolutionary biologists and biodemographers, because only such identification provides deeper understanding of ecological and evolutionary population dynamics. In natural populations one is challenged to accurately decompose the drivers of heterogeneity among individuals as genetically fixed or selectively neutral. Rather than working on wild populations we present here data from a simple bacterial system in the lab, Escherichia coli. Our system, based on cutting‐edge microfluidic techniques, provides high control over the genotype and the environment. It therefore allows to unambiguously decompose and quantify fixed genetic variability and dynamic stochastic variability among individuals. We show that within clonal individual variability (dynamic heterogeneity) in lifespan and lifetime reproduction is dominating at about 90–92%, over the 8–10% genetically (adaptive fixed) driven differences. The genetic differences among the clonal strains still lead to substantial variability in population growth rates (fitness), but, as well understood based on foundational work in population genetics, the within strain neutral variability slows adaptive change, by enhancing genetic drift, and lowering overall population growth. We also revealed a surprising diversity in senescence patterns among the clonal strains, which indicates diverse underlying cell‐intrinsic processes that shape these demographic patterns. Such diversity is surprising since all cells belong to the same bacteria species, E. coli, and still exhibit patterns such as classical senescence, non‐senescence, or negative senescence. We end by discussing whether similar levels of non‐genetic variability might be detected in other systems and close by stating the open questions how such heterogeneity is maintained, how it has evolved, and whether it is adaptive.     

Twinning in humans: maternal heterogeneity in reproduction and survival

While humans usually give birth to singletons, dizygotic twinning occurs at low rates in all populations worldwide. We evaluate two hypotheses that have differing expectations about the effects of bearing twins on maternal lifetime reproduction and survival. The maternal depletion hypothesis argues that mothers of twins will suffer negative outcomes owing to the higher physiological costs associated with bearing multiples. Alternatively, twinning, while costly, may indicate mothers with a greater capacity to bear that cost. Drawing from the vast natural fertility data in the Utah Population Database, we compared the reproductive and survival events of 4603 mothers who bore twins and 54 183 who had not. These mothers were born between 1807 and 1899, lived at least to the age of 50 years and married once to men who were alive when their wives were 50. Results from proportional hazards and regression analyses are consistent with the second hypothesis. Mothers of twins exhibit lower postmenopausal mortality, shorter average inter-birth intervals, later ages at last birth and higher lifetime fertility than their singleton-only bearing counterparts. From the largest historical sample of twinning mothers yet published, we conclude that bearing twins is more likely for those with a robust phenotype and is a useful index of maternal heterogeneity.     

Wolf in sheep's clothing: Model misspecification undermines tests of the neutral theory for life histories

Understanding the processes behind change in reproductive state along life‐history trajectories is a salient research program in evolutionary ecology. Two processes, state dependence and heterogeneity, can drive the dynamics of change among states. Both processes can operate simultaneously, begging the difficult question of how to tease them apart in practice. The Neutral Theory for Life Histories (NTLH) holds that the bulk of variations in life‐history trajectories is due to state dependence and is hence neutral: Once previous (breeding) state is taken into account, variations are mostly random. Lifetime reproductive success (LRS), the number of descendants produced over an individual's reproductive life span, has been used to infer support for NTLH in natura. Support stemmed from accurate prediction of the population‐level distribution of LRS with parameters estimated from a state dependence model. We show with Monte Carlo simulations that the current reliance of NTLH on LRS prediction in a null hypothesis framework easily leads to selecting a misspecified model, biased estimates and flawed inferences. Support for the NTLH can be spurious because of a systematic positive bias in estimated state dependence when heterogeneity is present in the data but ignored in the analysis. This bias can lead to spurious positive covariance between fitness components when there is in fact an underlying trade‐off. Furthermore, neutrality implied by NTLH needs a clarification because of a probable disjunction between its common understanding by evolutionary ecologists and its translation into statistical models of life‐history trajectories. Irrespective of what neutrality entails, testing hypotheses about the dynamics of change among states in life histories requires a multimodel framework because state dependence and heterogeneity can easily be mistaken for each other.     

Relative contributions of fixed and dynamic heterogeneity to variation in lifetime reproductive success in kestrels (Falco tinnunculus)

Many species show large variation in lifetime reproductive success (LRS), with a few individuals producing the majority of offspring. This variation can be explained by factors related to individuals (fixed heterogeneity) and stochastic differences in survival and reproduction (dynamic heterogeneity). In this study, we study the relative effects of these processes on the LRS of a Dutch Kestrel population, using three different methods. First, we extended neutral simulations by simulating LRS distributions of populations consisting of groups with increasingly different population parameters. Decomposition of total LRS variance into contributions from fixed and dynamic heterogeneity revealed that the proportion of fixed heterogeneity is probably lower than 10% of the total variance. Secondly, we used sensitivities of the mean and variance in LRS to each parameter to analytically show that it is impossible to get equal contributions of fixed and dynamic heterogeneity when only one parameter differs between groups. Finally, we computed the LRS probability distribution to show that even when all individuals have identical survival and reproduction rates, the variance in LRS is large (females: 27.52, males: 12.99). Although each method has its limitations, they all lead to the conclusion that the majority of the variation in kestrel LRS is caused by dynamic heterogeneity. This large effect of dynamic heterogeneity on LRS is similar to results for other species and contributes to the evidence that in most species the majority of individual variation in LRS is due to dynamic heterogeneity.     

From stochastic environments to life histories and back

Environmental stochasticity is known to play an important role in life-history evolution, but most general theory assumes a constant environment. In this paper, we examine life-history evolution in a variable environment, by decomposing average individual fitness (measured by the long-run stochastic growth rate) into contributions from average vital rates and their temporal variation. We examine how generation time, demographic dispersion (measured by the dispersion of reproductive events across the lifespan), demographic resilience (measured by damping time), within-year variances in vital rates, within-year correlations between vital rates and between-year correlations in vital rates combine to determine average individual fitness of stylized life histories. In a fluctuating environment, we show that there is often a range of cohort generation times at which the fitness is at a maximum. Thus, we expect ‘optimal’ phenotypes in fluctuating environments to differ from optimal phenotypes in constant environments. We show that stochastic growth rates are strongly affected by demographic dispersion, even when deterministic growth rates are not, and that demographic dispersion also determines the response of life-history-specific average fitness to within- and between-year correlations. Serial correlations can have a strong effect on fitness, and, depending on the structure of the life history, may act to increase or decrease fitness. The approach we outline takes a useful first step in developing general life-history theory for non-constant environments.     

Divergent life histories among smallmouth bass Micropterus dolomieu inhabiting a connected river–lake system

Annual reproductive surveys monitored nesting location, reproductive success and the age and size of individually tagged male smallmouth bass Micropterus dolomieu that reproduced in Millers Lake, a 45 ha widening of the Mississippi River, Ontario, and in a 1·5 km pool and riffle section of the river directly upstream. The vast majority of males displayed fidelity to either the river or the lake as reproductive habitat throughout their lifetimes. Nearly, half of the males that reproduced in successive years exhibited strong nest‐site fidelity by nesting within 20 m of their previous year’s nest site. In most years, when compared to those in the lake, reproductive males in the river differed significantly in reproductive characteristics including age and size at maturation and nesting success rates. A 3 year telemetry project identified two distinct habitat use patterns: lake‐resident fish remained in the lake throughout the year and potamodromous individuals migrated from the lake to upriver spawning habitat in the spring and then returned to the lake prior to the onset of winter. Integration of habitat use and reproductive data suggests that there are significant differences in the life‐history strategies of fish that reproduce in the river v. the lake.     

Marker-assisted determination of the relationship between body size and reproductive success and consequences for evaluation of adaptive life histories

We tested for differences in the predicted optimal ages at first maturity in brook charr ( Salvelinus fontinalis ) in Freshwater River, Newfoundland, when life-history data were collated based on the marker-assisted estimation of the relationship between body size and reproductive success rather than using fecundity as a surrogate for reproductive success. Jointly with capture–recapture data to estimate the growth and survival costs of reproduction, we found that weak relationships between body size and reproductive success generate selection against delayed maturation. This finding would not have held for females if the relationship between body size and fecundity had been used as a surrogate for the relationship between body size and reproductive success. This shows that predictions of optimal life histories can be qualitatively changed when using molecular markers to directly evaluate age- and/or size-specific effects of body size on reproductive success.     

Predicting trait values and measuring selection in complex life histories: reproductive allocation decisions in Soay sheep

Accurate prediction of life history phenomena and characterisation of selection in free-living animal populations are fundamental goals in evolutionary ecology. In density regulated, structured populations, where individual state influences fate, simple and widely used approaches based on individual lifetime measures of fitness are difficult to justify. We combine recently developed structured population modelling tools with ideas from modern evolutionary game theory (adaptive dynamics) to understand selection on allocation of female reproductive effort to singletons or twins in a size-structured population of feral sheep. In marked contrast to the classical selection analyses, our model-based approach predicts that the female allocation strategy is under negligible directional selection. These differences arise because classical selection analysis ignores components of offspring fitness and fails to consider selection over the complete life cycle.     

Life history evolution in cichlids 1: revisiting the evolution of life histories in relation to parental care

Empirical links between egg size and duration of parental care in fishes have generated a considerable amount of theory concerning life history evolution. However, to date, this link has not been investigated in relation to other important life-history traits such as clutch size and body size, or while controlling for shared ancestry between species. We provide the first phylogenetically based tests using a database with information on egg size, clutch size, body size and care duration in cichlid fishes (Cichlidae). Multiple regression analyses, based on independent contrasts on both the species and the genus level, showed that clutch size is the variable most closely related to duration of care. This pattern appeared to be driven by post-hatch care relationships. Our results show that, contrary to expectation, there is no positive link between egg size and care duration in Cichlidae. Instead, greater reproductive output through increased clutch size investment appears to have coevolved with greater care of offspring. We suggest that re-evaluation of the generality of current models of the evolution of egg size under parental care in fishes is needed.     

Postreproductive lifespans are rare in mammals

A species has a post‐reproductive stage if, like humans, a female entering the adult population can expect to live a substantial proportion of their life after their last reproductive event. However, it is conceptually and statistically challenging to distinguish these true post‐reproductive stages from the usual processes of senescence, which can result in females occasionally surviving past their last reproductive event. Hence, despite considerable interest, the taxonomic prevalence of post‐reproductive stages remains unclear and debated. In this study we use life tables constructed from published data on wild populations of mammals, and statistical measures of post‐reproductive lifespans, to distinguish true post‐reproductive stages from artefacts of senescence and demography in 52 species. We find post‐reproductive stages are rare in mammals and are limited to humans and a few species of toothed whales. By resolving this long‐standing debate, we hope to provide clarity for researchers in the field of evolutionary biology and a solid foundation for further studies investigating the evolution and adaptive significance of this unusual life history trait.     

Environmentally related life history variations in Geophagus brasiliensis

The hypothesis of environmentally related life history variations between two Geophagus brasiliensis populations was investigated by comparing riverine and lacustrine populations. Mean standard length and length at maturity were higher in the lagoon population. Higher fecundity and gonado-somatic indices reflected higher reproductive investment in the river population. In the river, reproduction took place throughout the year, whereas in the lagoon spawning was restricted to spring and summer. Both populations presented synchronous oocyte development, indicating total spawning. Nevertheless, the variation in traits suggests that both populations exhibit environmentally related variations in their life history patternss.     

Recent studies of dental development in Neandertals: Implications for Neandertal life histories

Did Neandertals share with modern humans their prolonged periods of growth and delayed ages of maturation? During the past five years, renewed interest in this question has produced dental studies with seemingly contradictory results. Some suggest fast dental growth, 1 , 2 while others appear to suggest a slower, modern‐human dental growth pattern. 3 , 4 Although some apparent contradictions can be reconciled, there remain questions that can be resolved only with additional data and cross‐validation of methods. Moreover, several difficulties are inherent in using dental development to gauge Neandertal life histories. Even with complete data on Neandertal dental development, questions are likely to remain about the meaning of those data with regard to understanding Neandertal life histories.     

The evolution of life histories in spatially heterogeneous environments: Optimal reaction norms revisited

Summary Natural populations live in heterogeneous environments, where habitat variation drives the evolution of phenotypic plasticity. The key feature of population structure addressed in this paper is the net flow of individuals from source (good) to sink (poor) habitats. These movements make it necessary to calculate fitness across the full range of habitats encountered by the population, rather than independently for each habitat. As a consequence, the optimal phenotype in a given habitat not only depends on conditions there but is linked to the performance of individuals in other habitats. We generalize the Euler-Lotka equation to define fitness in a spatially heterogeneous environment in which individuals disperse among habitats as newborn and then stay in a given habitat for life. In this case, maximizing fitness (the rate of increase over all habitats) is equivalent to maximizing the reproductive value of newborn in each habitat but not to maximizing the rate of increase that would result if individuals in each habitat were an isolated population. The new equation can be used to find optimal reaction norms for life history traits, and examples are calculated for age at maturity and clutch size. In contrast to previous results, the optimal reaction norm differs from the line connecting local adaptations of isolated populations each living in only one habitat. Selection pressure is higher in good and frequent habitats than in poor and rare ones. A formula for the relative importance of these two factors allows predictions of the habitat in which the genetic variance about the optimal reaction norm should be smallest.     

Age-specific life history tactics in organisms with determinate growth: Optimal models for non-optimal behavior?

Among organisms with determinate growth, optimization models predict that reproductive effort should increase as individuals approach old age, but the assumptions of these models may be inappropriate because the senescence that generates the necessary selective pressure may be not itself be optimal. Population genetics models were constructed to examine whether genes for age-specific changes in reproductive effort could invade a population in which senescence was maintained at equilibrium levels by a balance between mutation and selection. In asexually reproducing organisms, it was found that strategies of increasing reproductive effort could not normally invade the population. In sexually reproducing organisms, however, recombination was found to be important and genes for age-specific changes in effort could spread in the population under most circumstances.     

Comparative life histories in the genera Calanus and Neocalanus in high latitudes of the northern hemisphere

At least nine species of Calanidae occupy the area of interest, four in the Atlantic and five in the Pacific. All store wax esters and probably can undergo diapause. Latitudinally overlapping or onshore — offshore associations of two or more species occur in both oceans. Interzonals, with reduced mouth parts in the adult female, are endemic to the Pacific subarctic gyre where their life cycles are completed in one year. Presumably its nearly closed circulation and environmental stability have favored the evolution of endemic species well adapted to those conditions. Lack of ice- and/or salinity-induced stability also limits blooms there. The sub-arctic Atlantic contains several smaller oceanographic features, open to both arctic and Atlantic influences and populated by species of different origins, arctic species can behave as interzonals but may also require two or more years to complete their life cycles. Females may need to feed one year to reproduce the next and therefore they retain functional mouthparts. In some places in the North Atlantic, blooms may start in the sub-ice zone and seed the remaining euphotic zone. There the earliest stages of some the Calanus species can develop close to the ice, using primarily ice algae as food, while the remaining stages are adapted to utilize brief periods of intense primary production in the water column. Salinity-induced stability and shallow water favor blooms in the boundary waters of both oceans, which may be of greater importance in the Atlantic because of the proportionally greater area of continental shelf there. In both oceans the smaller species of Calanidae can produce up to three generations per year.     

The effects of age at mating on female life-history traits in a seed beetle

Age at first reproduction is an important component of lifehistory across taxa and can ultimately affect fitness. Becausegenetic interests of males and females over reproductive decisionscommonly differ, theory predicts that conflict may arise overthe temporal distribution of matings. To determine the potentialfor such sexual conflict, we studied the direct costs and benefitsassociated with mating at different times for females, usingseed beetles (Acanthoscelides obtectus) as a model system. Virginfemales were resistant to male mating attempts at a very earlyage but subsequently reduced their resistance. Although we foundno difference in life span or mortality rates between femalesmated early in life and those mated later, females that matedearly in life suffered a 12% reduction in lifetime fecundity.Thus, there are direct costs associated with mating early inlife for females. Yet, males mate even with newly hatched females.We suggest that these data indicate a potential for sexual conflictover the timing of first mating and that female resistance tomating, at least in part, may represent a female strategy aimedat delaying mating to a later time in life.     

动物生活史进化理论研究进展

综述了生活史性状、生活史对策、权衡、适合度及进化种群统计学等动物生活史进化领域的进展。权衡是生活史性状之间相互联系的纽带,分为生理权衡与进化权衡。适合度是相对的,与个体所处的特定环境条件有关,性状进化与适合度之间关系紧密。适合度是生活史进化理论研究的焦点。探讨动物生活史对策的理论很多,影响最大的是MacArthur和Wilson提出的r对策及K对策理论。随年龄的增长,动物存活率及繁殖率逐步下降的过程,称为衰老;解释衰老的进化理论主要有突变-选择平衡假设和多效对抗假设。进化种群统计学将种群统计学应用于生活史进化研究,为探讨表型适合度的进化提供了有效的手段。将进化种群统计学、数量遗传学及特定种系效应理论进行整合,建立完整的动物生活史进化综合理论体系,是当代此领域的最大挑战。     

The effect of treatment delay on time-to-recovery in the presence of unobserved heterogeneity

We study the effect of delaying treatment in the presence of (unobserved) heterogeneity. In a homogeneous population and assuming a proportional treatment effect, a treatment delay period will result in notably lower cumulative recovery percentages. We show in theoretical scenarios using frailty models that if the population is heterogeneous, the effect of a delay period is much smaller. This can be explained by the selection process that is induced by the frailty. Patient groups that start treatment later have already undergone more selection. The marginal hazard ratio for the treatment will act differently in such a more homogeneous patient group. We further discuss modeling approaches for estimating the effect of treatment delay in the presence of heterogeneity, and compare their performance in a simulation study. The conventional Cox model that fails to account for heterogeneity overestimates the effect of treatment delay. Including interaction terms between treatment and starting time of treatment or between treatment and follow up time gave no improvement. Estimating a frailty term can improve the estimation, but is sensitive to misspecification of the frailty distribution. Therefore, multiple frailty distributions should be used and the results should be compared using the Akaike Information Criterion. Non-parametric estimation of the cumulative recovery percentages can be considered if the dataset contains sufficient long term follow up for each of the delay strategies. The methods are demonstrated on a motivating application evaluating the effect of delaying the start of treatment with assisted reproductive techniques on time-to-pregnancy in couples with unexplained subfertility.