Static and dynamic expression of life history traits in the northern fulmar Fulmarus glacialis

Understanding the static and dynamic expression of life history traits is a prerequisite for the development of a causal theory of the evolution of aging and of life histories. We analyzed the statics and dynamics of reproduction and survival in a wild population of the northern fulmar, Fulmarus glacialis (Procellaridae). Survival rate is most influenced by year as compared to age and cohort. When temporal variation is ignored, survival rate increases slowly with age and then declines more rapidly at late ages. Survival rate contingent upon reproductive ‘stratum’ (producing an egg, hatching an egg, fledging a hatchling) also exhibits this pattern. Survival and reproduction have a positive static association in that survival rate increases as the apparent energy allocated to reproduction increases (as indexed by stratum). There is a broad distribution of realized lifetime reproductive success, which could be due to ‘fixed’ heterogeneity, with some individuals always having low survival and reproduction and others always having high survival and reproduction, or be due to ‘dynamic’ heterogeneity, with all individuals having the same expected reproductive and survival rates. Analysis of stochastic stratum dynamics indicates that individuals do not remain long in any given stratum and suggest that the variation among individuals with respect to lifetime reproductive success is due to dynamic heterogeneity. The probability of producing an egg increases with age for both sexes, whereas the probability of producing a fledgling initially declines with age and then increases. These results underscore the necessity of understanding the static and dynamic expression of demographic traits when making a causal claim about their evolution.     

Physiological tipping points in the relationship between foraging success and lifetime fitness of a long-lived mammal

Although anthropogenic change is often gradual, the impacts on animal populations may be precipitous if physiological processes create tipping points between energy gain, reproduction or survival. We use 25 years of behavioural, diet and demographic data from elephant seals to characterise their relationships with lifetime fitness. Survival and reproduction increased with mass gain during long foraging trips preceding the pupping seasons, and there was a threshold where individuals that gained an additional 4.8% of their body mass (26 kg, from 206 to 232 kg) increased lifetime reproductive success three-fold (from 1.8 to 4.9 pups). This was due to a two-fold increase in pupping probability (30% to 76%) and a 7% increase in reproductive lifespan (6.0 to 6.4 years). The sharp threshold between mass gain and reproduction may explain reproductive failure observed in many species and demonstrates how small, gradual reductions in prey from anthropogenic disturbance could have profound implications for animal populations.     

Individual heterogeneity in fitness in a long‐lived herbivore

Heterogeneity in the intrinsic quality and nutritional condition of individuals affects reproductive success and consequently fitness. Black brant (Branta bernicla nigricans) are long‐lived, migratory, specialist herbivores. Long migratory pathways and short summer breeding seasons constrain the time and energy available for reproduction, thus magnifying life‐history trade‐offs. These constraints, combined with long lifespans and trade‐offs between current and future reproductive value, provide a model system to examine the role of individual heterogeneity in driving life‐history strategies and individual heterogeneity in fitness. We used hierarchical Bayesian models to examine reproductive trade‐offs, modeling the relationships between within‐year measures of reproductive energy allocation and among‐year demographic rates of individual females breeding on the Yukon‐Kuskokwim Delta, Alaska, using capture–recapture and reproductive data from 1988 to 2014. We generally found that annual survival tended to be buffered against variation in reproductive investment, while breeding probability varied considerably over the range of clutch size‐laying date combinations. We provide evidence for relationships between breeding probability and clutch size, breeding probability and nest initiation date, and an interaction between clutch size and initiation date. Average lifetime clutch size also had a weak positive relationship with apparent survival probability. Our results support the use of demographic buffering strategies for black brant. These results also indirectly suggest associations among environmental conditions during growth, fitness, and energy allocation, highlighting the effects of early growth conditions on individual heterogeneity, and subsequently, lifetime reproductive investment.     

Dispersal as a source of variation in age-specific reproductive strategies in a wild population of lizards

Dispersal syndromes describe the patterns of covariation of morphological, behavioural, and life-history traits associated with dispersal. Studying dispersal syndromes is critical to understanding the demographic and genetic consequences of movements. Among studies describing the association of life-history traits with dispersal, there is anecdotal evidence suggesting that dispersal syndromes can vary with age. Recent theory also suggests that dispersive and philopatric individuals might have different age-specific reproductive efforts. In a wild population of the common lizard (Zootoca vivipara), we investigated whether dispersive and philopatric individuals have different age-specific reproductive effort, survival, offspring body condition, and offspring sex ratio. Consistent with theoretical predictions, we found that young dispersive females have a higher reproductive effort than young philopatric females. Our results also suggest that the early high investment in reproduction of dispersive females trades-off with an earlier onset of senescence than in philopatric females. We further found that young dispersive females produce smaller offspring in lower body condition than do young philopatric females. Overall, our results provide empirical evidence that dispersive and philopatric individuals have different age-specific life-history traits.     

Dynamic heterogeneity in life histories

Longitudinal data on natural populations have been analysed using multistage models in which survival depends on reproductive stage, and individuals change stages according to a Markov chain. These models are special cases of stage-structured population models. We show that stage-structured models generate dynamic heterogeneity: life-history differences produced by stochastic stratum dynamics. We characterize dynamic heterogeneity in a range of species across taxa by properties of the Markov chain: the entropy, which describes the extent of heterogeneity, and the subdominant eigenvalue, which describes the persistence of reproductive success during the life of an individual. Trajectories of reproductive stage determine survivorship, and we analyse the variance in lifespan within and between trajectories of reproductive stage. We show how stage-structured models can be used to predict realized distributions of lifetime reproductive success. Dynamic heterogeneity contrasts with fixed heterogeneity: unobserved differences that generate variation between life histories. We show by an example that observed distributions of lifetime reproductive success are often consistent with the claim that little or no fixed heterogeneity influences this trait. We propose that dynamic heterogeneity provides a 'neutral' model for assessing the possible role of unobserved 'quality' differences between individuals. We discuss fitness for dynamic life histories, and the implications of dynamic heterogeneity for the evolution of life histories and senescence.     

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.     

Individual heterogeneity in life-history trade-offs with age at first reproduction in capital breeding elephant seals

Recruitment age plays a key role in life-history evolution. Because individuals allocate limited resources among competing life-history functions, theory predicts trade-offs between current reproduction and future growth, survival and/or reproduction. Reproductive costs tend to vary with recruitment age, but may also be overridden by fixed individual differences leading to persistent demographic heterogeneity and positive covariation among demographic traits at the population level. We tested for evidence of intra- and inter-generational trade-offs and individual heterogeneity relating to age at first reproduction using three decades of detailed individual life-history data of 6,439 capital breeding female southern elephant seals. Contrary to the predictions from trade-off hypotheses, we found that recruitment at an early age was associated with higher population level survival and subsequent breeding probabilities. Nonetheless, a survival cost of first reproduction was evident at the population level, as first-time breeders always had lower survival probabilities than prebreeders and experienced breeders of the same age. However, models accounting for hidden persistent demographic heterogeneity revealed that the trade-off between first reproduction and survival was only expressed in “low quality” individuals, comprising 35% of the population. The short-term somatic costs associated with breeding at an early age had no effect on the ability of females to allocate resources to offspring in the next breeding season. Our results provide strong evidence for individual heterogeneity in the life-history trajectories of female elephant seals. By explicitly modeling hidden persistent demographic heterogeneity we show that individual heterogeneity governs the expression of trade-offs with first reproduction in elephant seals.     

Breeding phenology in relation to NDVI variability in free-ranging African elephant

The phenology of reproduction is often correlated with resource availability and is hypothesized to be shaped by selective forces in order to maximize lifetime reproductive success. African elephants have the distinctive life history traits of a 22 month gestation and extended offspring investment, necessitating a long-term strategy of energy acquisition and reproductive expenditure to ensure successful offspring recruitment.
We investigated the relationship between the reproductive phenology of a wild elephant population and resource availability using remotely sensed Normalized Differential Vegetation Index (NDVI) data as a measure of time-specific primary productivity and hence forage quality.
The initiation of female elephants' 3+yr reproductive bout was dependent on conditions during the season of conception but timed so parturition occurred during the most likely periods of high primary productivity 22 months later. Thus, the probability of conception is linked to the stochastic variation in seasonal quality and the phenology of parturition is related to the predictable seasonality of primary productivity, indicating elephants integrate information on known current and expected future conditions when reproducing.
Juvenile mortality was not correlated with ecological variability, hence female fecundity rather than calf mortality appears to drive demographic processes in the study population.
Extreme climatic events, such as those associated with the El Niño-Southern-Oscillation (ENSO), acted to synchronize female fecundity in the population. This study suggests that the relationship between fecundity and ecological variability instigates the characteristic demographic fluctuations in elephant populations, rather than the mortality-driven fluctuations observed in many ungulate populations.     

The marginal valuation of fertility

Substantial theoretical and empirical evidence demonstrates that fertility entails economic, physiological, and demographic trade-offs. The existence of trade-offs suggests that fitness should be maximized by an intermediate level of fertility, but this hypothesis has not had much support in the human life-history literature. We suggest that the difficulty of finding intermediate optima may be a function of the way fitness is calculated. Evolutionary analyses of human behavior typically use lifetime reproductive success as their fitness criterion. This fitness measure implicitly assumes that women are indifferent to the timing of reproduction and that they are risk-neutral in their reproductive decision-making. In this paper, we offer an alternative, easily-calculated fitness measure that accounts for differences in reproductive timing and yields clear preferences in the face of risky reproductive decision-making. Using historical demographic data from a genealogically-detailed dataset from 19th century Utah, we show that this measure is highly concave with respect to reproductive effort. This result has three major implications: (1) if births are properly timed, a lower-fertility reproductive strategy can have the same fitness as a high-fertility strategy, (2) intermediate optima are far more likely using fitness measures that are strongly concave with respect to effort, (3) we expect mothers to have strong investment preferences with respect to the risk inherent in reproduction.     

Individual heterogeneity in reproductive rates and cost of reproduction in a long‐lived vertebrate

Individual variation in reproductive success is a key feature of evolution, but also has important implications for predicting population responses to variable environments. Although such individual variation in reproductive outcomes has been reported in numerous studies, most analyses to date have not considered whether these realized differences were due to latent individual heterogeneity in reproduction or merely random chance causing different outcomes among like individuals. Furthermore, latent heterogeneity in fitness components might be expressed differently in contrasted environmental conditions, an issue that has only rarely been investigated. Here, we assessed (i) the potential existence of latent individual heterogeneity and (ii) the nature of its expression (fixed vs. variable) in a population of female Weddell seals (Leptonychotes weddellii), using a hierarchical modeling approach on a 30‐year mark–recapture data set consisting of 954 individual encounter histories. We found strong support for the existence of latent individual heterogeneity in the population, with “robust” individuals expected to produce twice as many pups as “frail” individuals. Moreover, the expression of individual heterogeneity appeared consistent, with only mild evidence that it might be amplified when environmental conditions are severe. Finally, the explicit modeling of individual heterogeneity allowed us to detect a substantial cost of reproduction that was not evidenced when the heterogeneity was ignored.     

The observed range for temporal mean-variance scaling exponents can be explained by reproductive correlation

The mean-variance scaling relationship known as Taylor's power law has been well documented empirically over the past four decades but a general theoretical explanation for the phenomenon does not exist. Here we provide an explanation that relates empirical patterns of temporal mean-variance scaling to individual level reproductive behavior. Initially, we review the scaling behavior of population growth models to establish theoretical limits for the scaling exponent b that is in agreement with the empirically observed range (1≤b≤2). We go on to show that the degree of reproductive covariance among individuals determines the scaling exponent b. Independent reproduction results in an exponent of one, while completely correlated reproduction results in the upper limit of two. Intermediate exponents, which are common empirically, can be generated through the decay of reproductive covariance with increasing population size. Finally, we describe how the link between reproductive correlation and the scaling exponent provides a way to infer properties of individual-level reproductive behavior, such as the relative influence of demographic stochasticity, from a macroecological pattern.     

Determinants and long‐term costs of early reproduction in males of a long‐lived polygynous mammal

In long‐lived polygynous species, male reproductive success is often monopolized by a few mature dominant individuals. Young males are generally too small to be dominant and may employ alternative tactics; however, little is known about the determinants of reproductive success for young males. Understanding the causes and consequences of variability in early reproductive success may be crucial to assess the strength of sexual selection and possible long‐term trade‐offs among life‐history traits. Selective pressures driven by fluctuating environmental conditions may depend on age class. We evaluated the determinants of reproduction in male bighorn sheep (Ovis canadensis) aged 2–4 years using 30 years of individual‐level data. These young males cannot defend estrous ewes and use alternative mating tactics. We also investigated how the age of first detected reproduction was correlated to lifetime reproductive success and longevity. We found that reproductive success of males aged 3 years was positively correlated to body mass, to the proportion of males aged 2–4 years in the competitor pool, and to the number of females available per adult male. These results suggest that reproductive success depends on both competitive ability and population age–sex structure. None of these variables, however, had significant effects on the reproductive success of males aged 2 or 4 years. Known reproduction before the age of five increased lifetime reproductive success but decreased longevity, suggesting a long‐term survival cost of early reproduction. Our analyses reveal that both individual‐level phenotypic and population‐level demographic variables influence reproductive success by young males and provide a rare assessment of fitness trade‐offs in wild polygynous males.     

Empirical evidence for competition-driven semelparity in wild medaka

Metabolic theory predicts that maintenance rate increases faster with animal body size than food intake rate, such that the critical resource density R* at which ingested energy exactly covers maintenance requirements increases with body size. Small-sized (low R*) juveniles may thus exclude their larger-sized (high R*) parents in resource competition, resulting in apparent semelparous life histories and non-overlapping generations. However, empirical support for such a competition-driven semelparity (CDS) remains scarce. Here, we report a high consistency of cohort dynamics with CDS in wild medaka (Oryzias latipes). As predicted by the theory, there was a strong juvenile-adult diet overlap, and all individuals died after reproduction as semelparous age-1 adults, synchronous with a rapid somatic growth of age-0 juveniles into the adult stage and with dropping abundances of zooplankton food resources. In addition to the theory, we found evidence for increased reproductive allocation under food stress, translating into immune depression and elevated parasite prevalence. Therefore, CDS in medaka emerges both from intercohort competitive exclusion and from food-dependent energy reallocation from maintenance to reproduction, the later presumably representing an adaptive response to the former. The literature data show that the strengths of both intercohort competition and reproductive allocation increase at higher temperatures in many ectotherms, pointing to climate warming as a potentially powerful magnifier of CDS in the wild.     

Trivers-willard rules for sex allocation

We present a quantitative model of sex allocation to investigate whether the simple “rules of thumb” suggested by Trivers and Willard (1973) would really maximize numbers of grandchildren in human populations. Using demographic data from the !Kung of southern Africa and the basic assumptions of the Trivers-Willard hypothesis, we calculate expected numbers of grandchildren based on age- and sex-specific reproductive value. Patterns of parental investment that would maximize numbers of expected grandchildren often differ from the Trivers-Willard rules. In particular, the optimum parental behavior is sensitive to population dynamics, type of parental investment, and, most important, relative ages of sons and daughters. It is doubtful whether a parent blindly following the simple Trivers-Willard rules would maximize numbers of expected grandchildren, on average. In addition, we show that sex-specific infanticide will almost never achieve the goal of maximizing expected numbers of grandchildren.     

Altitudinal variation of demographic life-history traits does not mimic latitudinal variation in natterjack toads (Bufo calamita)

In anuran amphibians, age- and size-related life-history traits vary along latitudinal and altiudinal gradients. In the present study, we tested the hypothesis that altitudinal and latitudinal effects cause similar responses by assessing demographic life-history traits in nine Bufo calamita populations inhabiting elevations from sea level to 2270 m. Skeletochronologically determined age at maturity and longevity increased at elevations exceeding 2000 m, but female potential reproductive lifespan (PRLS) did not increase with altitude, as it did with latitude. Integrating the available evidence, it was found that lifetime fecundity of natterjacks decreased at the upper altitudinal range because PRLS was about the same as in lowland populations but females were smaller. In contrast, small size of northern females was compensated for by increased PRLS which minimised latitudinal variation of lifetime fecundity. Thus, this study provides evidence that altitudinal effects on life-history traits do not mimic latitudinal effects. Life-history trait variation along the altitudinal gradient seems to respond directly to the shortening of the annual activity period. As there is no evidence for increasing mortality in highland populations, reduced lifetime fecundity may be the ultimate reason for the natterjacks' inability to colonise elevations exceeding 2500 m.     

Experience versus effort: what explains dynamic heterogeneity with respect to age?

Age‐related patterns of survival and reproduction have been explained by accumulated experience (‘experience hypothesis’), increased effort (‘effort hypothesis’), and intrinsic differences in phenotypes (‘selection hypothesis’). We examined the experience and effort hypotheses using a 40‐year data set in a population of Leach's storm‐petrels Oceanodroma leucorhoa, long‐lived seabirds for which the effect of phenotypic variation has been previously demonstrated. Age was quantified by time since recruitment (‘breeding age’). The best model of adult survival included a positive effect of breeding age (1, 2, 3+ years), sex (male > female), and year. Among‐individuals variation (fixed heterogeneity) accounted for 31.6% of the variance in annual reproductive success. We further examined within‐individual patterns in reproductive success (dynamic heterogeneity) in the subset of individuals with at least five breeding attempts. Three distinct phases characterized reproductive success – early increase, long asymptotic peak, late decline. No effect of early reproductive output on longevity was found, however, early success was positively correlated with lifetime reproductive success. Reproductive success was lower earlier than later in life. Among the few natally philopatric individuals in the population, age of first breeding had no effect on longevity, lifetime reproductive success, or early reproductive success. No support for the effort hypothesis was found in this population. Instead, age‐specific patterns of survival and reproduction in these birds are best explained by the experience hypothesis over and above the effect of intrinsic differences among individuals.     

The influence of temperature and host availability on the host exploitation strategies of sexual and asexual parasitic wasps of the same species

In the hymenopteran parasitoid Venturia canescens, asexual (obligate thelytoky not induced by Wolbachia bacteria) and sexual (arrhenotokous) wasps coexist in field conditions despite the demographic cost incurred due to the production of males by sexual females. Arrhenotoky predominates in field conditions, whereas populations in indoor conditions (mills, granaries) are exclusively thelytokous. These differences in the relative abundance of the two modes of reproduction between environments suggest that the individuals of each reproductive mode may have developed strategies adapted to the conditions prevailing in each kind of habitat. The two environments contrast in temperature variability and in the spatial heterogeneity of host availability. In this study, we considered the combined effect of temperature and host availability on host patch exploitation by thelytokous and arrhenotokous V. canescens. As expected, arrhenotokous females were more sensitive to temperature changes. If the temperature decreased before foraging, they remained longer and exploited patches more thoroughly. This is consistent with the expected behaviour of parasitoids in response to signs of unfavourable conditions that entail increasing risk of time limitation or a reduced probability of attaining further patches. Both arrhenotokous and thelytokous females increased patch exploitation with host availability. However, unexpectedly, we found no difference in the way the two types of wasp responded to differences in host availability. Differences in the strategies adopted under different environmental conditions may indicate divergence of niche-specific life history traits between the two modes of reproduction. Niche displacement may partly account for the coexistence of these two modes of reproduction at a geographical scale.     

Variance in animal longevity: contributions of heterogeneity and stochasticity

Variance in longevity among individuals may arise as an effect of heterogeneity (differences in mortality rates experienced at the same age or stage) or as an effect of individual stochasticity (the outcome of random demographic events during the life cycle). Decomposing the variance into components due to heterogeneity and stochasticity is crucial for evolutionary analyses.In this study, we analyze longevity from ten studies of invertebrates in the laboratory, and use the results to partition the variance in longevity into its components. To do so, we fit finite mixtures of Weibull survival functions to each data set by maximum likelihood, using the EM algorithm. We used the Bayesian Information Criterion to select the most well supported model. The results of the mixture analysis were used to construct an age × stage-classified matrix model, with heterogeneity groups as stages, from which we calculated the variance in longevity and its components. Almost all data sets revealed evidence of some degree of heterogeneity. The median contribution of unobserved heterogeneity to the total variance was 35%, with the remaining 65% due to stochasticity. The differences among groups in mean longevity were typically on the order of 30% of the overall life expectancy. There was considerable variation among data sets in both the magnitude of heterogeneity and the proportion of variance due to heterogeneity, but no clear patterns were apparent in relation to sex, taxon, or environmental conditions.     

Inbreeding avoidance and reproductive skew in a cooperative mammal

In animal social groups, socially subordinate individuals frequently show low reproductive success or completely fail to breed. This suppression of subordinate reproduction is currently typically attributed to control by dominant individuals. However, subordinates in cooperative groups often lack access to unrelated mates, and an alternative possibility is that their reproduction is limited by inbreeding avoidance. Using the eusocial Damaraland mole-rat Cryptomys damarensis, this paper provides the first experimental evidence, to our knowledge, for this explanation. Subordinate, non-breeding female mole-rats were given access to unrelated mates while remaining in the presence of dominant females, and many became reproductively active soon after unrelated males were introduced. Inbreeding avoidance and the availability of unrelated mates provides a plausible and untested explanation for variation in reproductive skew across animal societies.     

Termination of reproduction in nonhuman and human female primates

We examined demographic records from 13 captive primate species and a human population to determine age-related changes in female reproduction. In most species age-specific fertility declined and interbirth intervals increased with age. Using an operational definition of termination of reproduction based on individual variance in interbirth intervals, a proportion of females in most nonhuman species had terminated reproduction before death. Compared to other primates, a greater proportion of chimpanzees and human females ceased reproduction, and humans, in particular, were reproductively inactive for relatively longer than would be expected from their body weight. These empirical data quantify the extent of reproductive termination and thereby extend hitherto anecdotal accounts of this phenomenon in primates.