Life‐history evolution under fluctuating density‐dependent selection and the adaptive alignment of pace‐of‐life syndromes

We present a novel perspective on life‐history evolution that combines recent theoretical advances in fluctuating density‐dependent selection with the notion of pace‐of‐life syndromes (POLSs) in behavioural ecology. These ideas posit phenotypic co‐variation in life‐history, physiological, morphological and behavioural traits as a continuum from the highly fecund, short‐lived, bold, aggressive and highly dispersive ‘fast’ types at one end of the POLS to the less fecund, long‐lived, cautious, shy, plastic and socially responsive ‘slow’ types at the other. We propose that such variation in life histories and the associated individual differences in behaviour can be explained through their eco‐evolutionary dynamics with population density – a single and ubiquitous selective factor that is present in all biological systems. Contrasting regimes of environmental stochasticity are expected to affect population density in time and space and create differing patterns of fluctuating density‐dependent selection, which generates variation in fast versus slow life histories within and among populations. We therefore predict that a major axis of phenotypic co‐variation in life‐history, physiological, morphological and behavioural traits (i.e. the POLS) should align with these stochastic fluctuations in the multivariate fitness landscape created by variation in density‐dependent selection. Phenotypic plasticity and/or genetic (co‐)variation oriented along this major POLS axis are thus expected to facilitate rapid and adaptively integrated changes in various aspects of life histories within and among populations and/or species. The fluctuating density‐dependent selection POLS framework presented here therefore provides a series of clear testable predictions, the investigation of which should further our fundamental understanding of life‐history evolution and thus our ability to predict natural population dynamics.     

Elevational trends in life histories: revising the pace‐of‐life framework

Life‐history traits in birds, such as lifespan, age at maturity, and rate of reproduction, vary across environments and in combinations imposed by trade‐offs and limitations of physiological mechanisms. A plethora of studies have described the diversity of traits and hypothesized selection pressures shaping components of the survival–reproduction trade‐off. Life‐history variation appears to fall along a slow–fast continuum, with slow pace characterized by higher investment in survival over reproduction and fast pace characterized by higher investment in reproduction over survival. The Pace‐of‐Life Syndrome (POLS) is a framework to describe the slow–fast axis of variation in life‐history traits and physiological traits. The POLS corresponds to latitudinal gradients, with tropical birds exhibiting a slow pace of life. We examined four possible ways that the traits of high‐elevation birds might correspond to the POLS continuum: (i) rapid pace, (ii) tropical slow pace, (iii) novel elevational pace, or (iv) constrained pace. Recent studies reveal that birds breeding at high elevations in temperate zones exhibit a combination of traits creating a unique elevational pace of life with a central trade‐off similar to a slow pace but physiological trade‐offs more similar to a fast pace. A paucity of studies prevents consideration of the possibility of a constrained pace of life. We propose extending the POLS framework to include trait variation of elevational clines to help to investigate complexity in global geographic patterns.     

Evolution of age at primiparity in pinnipeds in the absence of the quality–quantity trade‐off in reproduction

Age at primiparity (AP) is a key life history trait which is crucial to the evolution of life history strategies. This trait is particularly interesting in pinnipeds (walrus, eared seals, and true seals), which are monotocous animals. Thus, the commonly observed trade‐off between offspring quality and quantity does not apply to this taxon. Therefore, comparative studies on the evolution of AP might shed light on other important evolutionary correlates when litter size is fixed. Using phylogenetic generalized least squares analyses, we found a strong negative and robust correlation between relative birth mass (mean pup birth mass as a proportion of mean adult female mass) and AP. Rather than trading‐off an early start of reproduction with light relative offspring mass, this result suggests that pinnipeds exhibit either faster (i.e., higher relative offspring mass leading to shorter lactation length, and thus shorter interbirth interval) or slower life histories and that an early AP and a heavy relative offspring mass co‐evolved into a comparatively fast life history strategy. On the other hand, AP was positively related to lactation length: A later start of reproduction was associated with a longer lactation length. Consequently, variation in AP in pinnipeds seems to be affected by an interplay between costs and benefits of early reproduction mediated by relative investment into the single offspring via relative birth mass and lactation length.     

A review of urban impacts on avian life‐history evolution: Does city living lead to slower pace of life?

The concept of a pace‐of‐life syndrome describes inter‐ and intraspecific variation in several life‐history traits along a slow‐to‐fast pace‐of‐life continuum, with long lifespans, low reproductive and metabolic rates, and elevated somatic defences at the slow end of the continuum and the opposite traits at the fast end. Pace‐of‐life can vary in relation to local environmental conditions (e.g. latitude, altitude), and here we propose that this variation may also occur along an anthropogenically modified environmental gradient. Based on a body of literature supporting the idea that city birds have longer lifespans, we predict that urban birds have a slower pace‐of‐life compared to rural birds and thus invest more in self maintenance and less in annual reproduction. Our statistical meta‐analysis of two key traits related to pace‐of‐life, survival and breeding investment (clutch size), indicated that urban birds generally have higher survival, but smaller clutch sizes. The latter finding (smaller clutches in urban habitats) seemed to be mainly a characteristic of smaller passerines. We also reviewed urbanization studies on other traits that can be associated with pace‐of‐life and are related to either reproductive investment or self‐maintenance. Though sample sizes were generally too small to conduct formal meta‐analyses, published literature suggests that urban birds tend to produce lower‐quality sexual signals and invest more in offspring care. The latter finding is in agreement with the adult survival hypothesis, proposing that higher adult survival prospects favour investment in fewer offspring per year. According to our hypothesis, differences in age structure should arise between urban and rural populations, providing a novel alternative explanation for physiological differences and earlier breeding. We encourage more research investigating how telomere dynamics, immune defences, antioxidants and oxidative damage in different tissues vary along the urbanization gradient, and suggest that applying pace‐of‐life framework to studies of variation in physiological traits along the urbanization gradient might be the next direction to improve our understanding of urbanization as an evolutionary process.     

Lifetime fitness consequences of early‐life ecological hardship in a wild mammal population

Early‐life ecological conditions have major effects on survival and reproduction. Numerous studies in wild systems show fitness benefits of good quality early‐life ecological conditions (“silver‐spoon” effects). Recently, however, some studies have reported that poor‐quality early‐life ecological conditions are associated with later‐life fitness advantages and that the effect of early‐life conditions can be sex‐specific. Furthermore, few studies have investigated the effect of the variability of early‐life ecological conditions on later‐life fitness. Here, we test how the mean and variability of early‐life ecological conditions affect the longevity and reproduction of males and females using 14 years of data on wild banded mongooses (Mungos mungo). Males that experienced highly variable ecological conditions during development lived longer and had greater lifetime fitness, while those that experienced poor early‐life conditions lived longer but at a cost of reduced fertility. In females, there were no such effects. Our study suggests that exposure to more variable environments in early life can result in lifetime fitness benefits, whereas differences in the mean early‐life conditions experienced mediate a life‐history trade‐off between survival and reproduction. It also demonstrates how early‐life ecological conditions can produce different selection pressures on males and females.     

An experimental test of density‐dependent selection on temperament traits of activity,boldness and sociability

Temperament traits are seen in many animal species, and recent evolutionary models predict that they could be maintained by heterogeneous selection. We tested this prediction by examining density‐dependent selection in juvenile common lizards Zootoca vivipara scored for activity, boldness and sociability at birth and at the age of 1 year. We measured three key life‐history traits (juvenile survival, body growth rate and reproduction) and quantified selection in experimental populations at five density levels ranging from low to high values. We observed consistent individual differences for all behaviours on the short term, but only for activity and one boldness measure across the first year of life. At low density, growth selection favoured more sociable lizards, whereas viability selection favoured less active individuals. A significant negative correlational selection on activity and boldness existed for body growth rate irrespective of density. Thus, behavioural traits were characterized by limited ontogenic consistency, and natural selection was heterogeneous between density treatments and fitness traits. This confirms that density‐dependent selection plays an important role in the maintenance of individual differences in exploration‐activity and sociability.     

The early‐life environment and individual plasticity in life‐history traits

We tested whether the early‐life environment can influence the extent of individual plasticity in a life‐history trait. We asked: can the early‐life environment explain why, in response to the same adult environmental cue, some individuals invest more than others in current reproduction? Moreover, can it additionally explain why investment in current reproduction trades off against survival in some individuals, but is positively correlated with survival in others? We addressed these questions using the burying beetle, which breeds on small carcasses and sometimes carries phoretic mites. These mites breed alongside the beetle, on the same resource, and are a key component of the beetle's early‐life environment. We exposed female beetles to mites twice during their lives: during their development as larvae and again as adults during their first reproductive event. We measured investment in current reproduction by quantifying average larval mass and recorded the female's life span after breeding to quantify survival. We found no effect of either developing or breeding alongside mites on female reproductive investment, nor on her life span, nor did developing alongside mites influence her size. In post hoc analyses, where we considered the effect of mite number (rather than their mere presence/absence) during the female's adult breeding event, we found that females invested more in current reproduction when exposed to greater mite densities during reproduction, but only if they had been exposed to mites during development as well. Otherwise, they invested less in larvae at greater mite densities. Furthermore, females that had developed with mites exhibited a trade‐off between investment in current reproduction and future survival, whereas these traits were positively correlated in females that had developed without mites. The early‐life environment thus generates individual variation in life‐history plasticity. We discuss whether this is because mites influence the resources available to developing young or serve as important environmental cues.     

Short‐ and long‐term costs of reproduction in a migratory songbird

Costs of reproduction represent a common life‐history trade‐off. Critical to understanding these costs in migratory species is the ability to track individuals across successive stages of the annual cycle. We assessed the effects of total number of offspring fledged and date of breeding completion on pre‐migratory body condition, the schedule of moult and annual survival in a migratory songbird, the Savannah Sparrow Passerculus sandwichensis. Between 2008 and 2010, moult was delayed for individuals that finished breeding later in the breeding period and resulted in reduced lean tissue mass during the pre‐migratory period, suggesting an indirect trade‐off between the timing of breeding completion and condition just prior to migration. Lean tissue mass decreased as the number of offspring fledged increased in 2009, a particularly cool and wet year, illustrating a direct trade‐off between reproductive effort and condition just prior to migration in years when weather is poor. However, using a 17‐year dataset from the same population, we found that parents that fledged young late in the breeding period had the highest survival and that number of offspring fledged did not affect survival, suggesting that individuals do not experience long‐term trade‐offs between reproduction and survival. Taken together, our results suggest that adult Savannah Sparrows pay short‐term costs of reproduction, but that longer‐term costs are mitigated by individual quality, perhaps through individual variation in resource acquisition.     

Eco‐evolutionary feedback promotes Red Queen dynamics and selects for sex in predator populations

Although numerous hypotheses exist to explain the overwhelming presence of sexual reproduction across the tree of life, we still cannot explain its prevalence when considering all inherent costs involved. The Red Queen hypothesis states that sex is maintained because it can create novel genotypes with a selective advantage. This occurs when the interactions between species induce frequent environmental change. Here, we investigate whether coevolution and eco‐evolutionary feedback dynamics in a predator‐prey system allows for indirect selection and maintenance of sexual reproduction in the predator. Combining models and chemostat experiments of a rotifer‐algae system we show a continuous feedback between population and trait change along with recurrent shifts from selection by predation and competition for a limited resource. We found that a high propensity for sex was indirectly selected and was maintained in rotifer populations within environments containing these eco‐evolutionary dynamics; whereas within environments under constant conditions, predators evolved rapidly to lower levels of sex. Thus, our results indicate that the influence of eco‐evolutionary feedback dynamics on the overall evolutionary change has been underestimated.     

Selection on age at first and at last reproduction in the long‐lived Alpine Swift Apus melba

The way an organism spreads its reproduction over time is defined as a life‐history trait, and selection is expected to favour life‐history traits associated with the highest fitness return. We use a long‐term dataset of 277 life histories to investigate the shape and strength of selection acting on the age at first reproduction and at last reproduction in the long‐lived Alpine Swift. Both traits were under strong directional selection, but in opposite directions, with selection favouring birds starting their reproductive career early and being able to reproduce for longer. There was also evidence for stabilising selection acting on both traits, suggesting that individuals should nonetheless refrain from reproducing in their first 2 years of life (i.e. when inexperienced), and that reproducing after 7 years of age had little effect on lifetime fitness, probably due to senescence.     

Density‐dependent survival varies with species life‐history strategy in a tropical forest

Species coexistence in diverse communities likely results from multiple interacting factors. Mechanisms such as conspecific negative density dependence (CNDD) and varying life‐history strategies related to resource partitioning are known to influence plant fitness, and thereby community composition and diversity. However, we have little understanding of how these mechanisms interact and how they vary across life stages. Here, we document the interaction between CNDD and life‐history strategy, based on growth‐mortality trade‐offs, from seedling to adult tree for 47 species in a tropical forest. Species’ life‐history strategies remained consistent across stages: fast‐growing species had higher mortality than slow‐growing species at all stages. In contrast, mean CNDD was strongest at early life stages (i.e. seedling, sapling). Fast‐growing species tended to suffer greater CNDD than slow‐growing species at several, but not all life stages. Overall, our results demonstrate that coexistence mechanisms interact across multiple life stages to shape diverse tree communities.     

What are the benefits of parental care? The importance of parental effects on developmental rate

The evolution of parental care is beneficial if it facilitates offspring performance traits that are ultimately tied to offspring fitness. While this may seem self‐evident, the benefits of parental care have received relatively little theoretical exploration. Here, we develop a theoretical model that elucidates how parental care can affect offspring performance and which aspects of offspring performance (e.g., survival, development) are likely to be influenced by care. We begin by summarizing four general types of parental care benefits. Care can be beneficial if parents (1) increase offspring survival during the stage in which parents and offspring are associated, (2) improve offspring quality in a way that leads to increased offspring survival and/or reproduction in the future when parents are no longer associated with offspring, and/or (3) directly increase offspring reproductive success when parents and offspring remain associated into adulthood. We additionally suggest that parental control over offspring developmental rate might represent a substantial, yet underappreciated, benefit of care. We hypothesize that parents adjust the amount of time offspring spend in life‐history stages in response to expected offspring mortality, which in turn might increase overall offspring survival, and ultimately, fitness of parents and offspring. Using a theoretical evolutionary framework, we show that parental control over offspring developmental rate can represent a significant, or even the sole, benefit of care. Considering this benefit influences our general understanding of the evolution of care, as parental control over offspring developmental rate can increase the range of life‐history conditions (e.g., egg and juvenile mortalities) under which care can evolve.     

Evidence of reduced individual heterogeneity in adult survival of long‐lived species

The canalization hypothesis postulates that the rate at which trait variation generates variation in the average individual fitness in a population determines how buffered traits are against environmental and genetic factors. The ranking of a species on the slow‐fast continuum – the covariation among life‐history traits describing species‐specific life cycles along a gradient going from a long life, slow maturity, and low annual reproductive output, to a short life, fast maturity, and high annual reproductive output – strongly correlates with the relative fitness impact of a given amount of variation in adult survival. Under the canalization hypothesis, long‐lived species are thus expected to display less individual heterogeneity in survival at the onset of adulthood, when reproductive values peak, than short‐lived species. We tested this life‐history prediction by analysing long‐term time series of individual‐based data in nine species of birds and mammals using capture‐recapture models. We found that individual heterogeneity in survival was higher in species with short‐generation time (< 3 years) than in species with long generation time (> 4 years). Our findings provide the first piece of empirical evidence for the canalization hypothesis at the individual level from the wild.     

Experimentally induced host‐shift changes life‐history strategy in a seed beetle

Expansion of the host range in phytophagous insects depends on their ability to form an association with a novel plant through changes in host‐related traits. Phenotypic plasticity has important effects on initial survival of individuals faced with a new plant, as well as on the courses of evolutionary change during long‐term adaptation to novel conditions. Using experimental populations of the seed beetle that evolved on ancestral (common bean) or novel (chickpea) host and applying reciprocal transplant at both larval and adult stage on the alternative host plant, we studied the relationship between the initial (plastic) phases of host‐shift and the subsequent stages of evolutionary divergence in life‐history strategies between populations exposed to the host‐shift process. After 48 generations, populations became well adapted to chickpea by evolving the life‐history strategy with prolonged larval development, increased body mass, earlier reproduction, shorter lifespan and decreased plasticity of all traits compared with ancestral conditions. In chickpea‐adapted beetles, negative fitness consequences of low plasticity of pre‐adult development (revealed as severe decrease in egg‐to‐adult viability on beans) exhibited mismatch with positive effects of low plasticity (i.e. low host sensitivity) in oviposition and fecundity. In contrast, beetles adapted to the ancestral host showed high plasticity of developmental process, which enabled high larval survival on chickpea, whereas elevated plasticity in adult behaviour (i.e. high host sensitivity) resulted in delayed reproduction and decreased fecundity on chickpea. The analysis of population growth parameters revealed significant fluctuation during successive phases of the host‐shift process in A. obtectus.     

Heterosis in age‐specific selected populations of a seed beetle: Sex differences in longevity and reproductive behavior

We tested mutation accumulation hypothesis for the evolution of senescence using short‐lived and long‐lived populations of the seed‐feeding beetle, Acanthoscelides obtectus (Say), obtained by selection on early‐ and late‐life for many generations. The expected consequence of the mutation accumulation hypothesis is that in short‐lived populations, where the force of natural selection is the strongest early in life, the late‐life fitness traits should decline due to genetic drift which increases the frequency of mutations with deleterious effects in later adult stages. Since it is unlikely that identical deleterious mutations will increase in several independent populations, hybrid vigor for late‐life fitness is expected in offspring obtained in crosses among populations selected for early‐life fitness traits. We tested longevity of both sexes, female fecundity and male reproductive behavior for hybrid vigor by comparing hybrid and nonhybrid short‐lived populations. Hybrid vigor was confirmed for male virility, mating speed and copulation duration, and longevity of both sexes at late ages. In contrast to males, the results on female fecundity in short‐lived populations did not support mutation accumulation as a genetic mechanism for the evolution of this trait. Contrary to the prediction of this hypothesis, male mating ability indices and female fecundity in long‐lived populations exhibited hybrid vigor at all assayed age classes. We demonstrate that nonhybrid long‐lived populations diverged randomly regarding female and male reproductive fitness, indicating that sexually antagonistic selection, when accompanied with genetic drift for female fecundity and male virility, might be responsible for overriding natural selection in the independently evolving long‐lived populations.     

Roles of maternal effects in maintaining genetic variation: Maternal storage effect

Understanding the maintenance of genetic variation remains a central challenge in evolutionary biology. Recent empirical studies suggest the importance of temporally varying selection, as allele frequencies have been found to fluctuate substantially in the wild. However, previous theory suggests that the conditions for the maintenance of genetic variation under temporally fluctuating selection are quite restrictive. Using mathematical models, we demonstrate that maternal genetic effects, whereby maternal genotypes affect offspring phenotypes, can facilitate the maintenance of polymorphism in temporally varying environments. Maternal effects result in mismatches between genotypes and phenotypes, thereby buffering the influence of selection on allele frequency. This decreases the magnitude of allele‐frequency fluctuations and creates conditions for the maintenance of variation when selection causes fluctuations. Therefore, maternal effects may result in a temporal storage effect (“maternal storage effect”). On the other hand, when selection does not cause fluctuations (e.g., linear negative frequency‐dependent selection), maternal genetic effects moderate the relative importance of selection compared to genetic drift and promote stochastic allele extinction in finite populations. Thus, maternal effects can play an important role in the maintenance of polymorphism, but the direction of the effect depends on the nature of selection.     

INTERACTIVE EFFECTS OF OFFSPRING SIZE AND TIMING OF REPRODUCTION ON OFFSPRING REPRODUCTION: EXPERIMENTAL,MATERNAL, AND QUANTITATIVE GENETIC ASPECTS

We demonstrate that egg size in side-blotched lizards is heritable (parent-offspring regressions) and thus will respond to natural selection. Because our estimate of heritability is derived from free-ranging lizards, it is useful for predicting evolutionary response to selection in wild populations. Moreover, our estimate for the heritability of egg size is not likely to be confounded by nongenetic maternal effects that might arise from egg size per se because we estimate a significant parent-offspring correlation for egg size in the face of dramatic experimental manipulation of yolk volume of the egg. Furthermore, we also demonstrate a significant correlation between egg size of the female parent and clutch size of her offspring. Because this correlation is not related to experimentally induced maternal effects, we suggest that it is indicative of a genetic correlation between egg size and clutch size. We synthesize our results from genetic analyses of the trade-off between egg size and clutch size with previously published experiments that document the mechanistic basis of this trade-off. Experimental manipulation of yolk volume has no effect on offspring reproductive traits such as egg size, clutch size, size at maturity, or oviposition date. However, egg size was related to offspring survival during adult phases of the life history. We partitioned survival of offspring during the adult phase of the life history into (1) survival of offspring from winter emergence to the production of the first clutch (i.e., the vitellogenic phase of the first clutch), and (2) survival of the offspring from the production of the first clutch to the end of the reproductive season. Offspring from the first clutch of the reproductive season in the previous year had higher survival during vitellogenesis of their first clutch if these offspring came from small eggs. We did not observe selection during these prelaying phases of adulthood for offspring from later clutches. However, we did find that later clutch offspring from large eggs had the highest survival over the first season of reproduction. The differences in selection on adult survival arising from maternal effects would reinforce previously documented selection that favors the production of small offspring early in the season and large offspring later in the season—a seasonal shift in maternal provisioning. We also report on a significant parent-offspring correlation in lay date and thus significant heritable variation in lay date. We can rule out the possibility of yolk volume as a confounding maternal effect—experimental manipulation of yolk volume has no effect on lay date of offspring. However, we cannot distinguish between genetic effects (i.e., heritable) and nongenetic maternal effects acting on lay date that arise from the maternal trait lay date per se (or other unidentified maternal traits). Nevertheless, we demonstrate how the timing of female reproduction (e.g., date of oviposition and date of hatching) affect reproductive attributes of offspring. Notably, we find that date of hatching has effects on body size at maturity and fecundity of offspring from later clutches. We did not detect comparable effects of lay date on offspring from the first clutch.     

Life‐history strategy varies with the strength of competition in a food‐limited ungulate population

Fluctuating population density in stochastic environments can contribute to maintain life‐history variation within populations via density‐dependent selection. We used individual‐based data from a population of Soay sheep to examine variation in life‐history strategies at high and low population density. We incorporated life‐history trade‐offs among survival, reproduction and body mass growth into structured population models and found support for the prediction that different life‐history strategies are optimal at low and high population densities. Shorter generation times and lower asymptotic body mass were selected for in high‐density environments even though heavier individuals had higher probabilities to survive and reproduce. In contrast, greater asymptotic body mass and longer generation times were optimal at low population density. If populations fluctuate between high density when resources are scarce, and low densities when they are abundant, the variation in density will generate fluctuating selection for different life‐history strategies, that could act to maintain life‐history variation.     

Plant‐soil feedbacks from 30‐year family‐specific soil cultures: phylogeny,soil chemistry and plant life stage

Intraspecific negative feedback effects, where performance is reduced on soils conditioned by conspecifics, are widely documented in plant communities. However, interspecific feedbacks are less well studied, and their direction, strength, causes, and consequences are poorly understood. If more closely related species share pathogens, or have similar soil resource requirements, plants may perform better on soils conditioned by more distant phylogenetic relatives. There have been few empirical tests of this prediction across plant life stages, and none of which attempt to account for soil chemistry. Here, we test the utility of phylogeny for predicting soil feedback effects on plant survival and performance (germination, seedling survival, growth rate, biomass). We implement a full factorial experiment growing species representing five families on five plant family‐specific soil sources. Our experiments exploit soils that have been cultured for over 30 years in plant family‐specific beds at Oxford University Botanic Gardens. Plant responses to soil source were idiosyncratic, and species did not perform better on soils cultured by phylogenetically more distant relatives. The magnitude and sign of feedback effects could, however, be explained by differences in the chemical properties of “home” and “away” soils. Furthermore, the direction of soil chemistry‐related plant‐soil feedbacks was dependent on plant life stage, with the effects of soil chemistry on germination success and accumulation of biomass inversely related. Our results (1) suggest that the phylogenetic distance between plant families cannot predict plant–soil feedbacks across multiple life stages, and (2) highlight the need to consider changes in soil chemistry as an important driver of population responses. The contrasting responses at plant life stages suggest that studies focusing on brief phases in plant demography (e.g., germination success) may not give a full picture of plant–soil feedback effects.     

Reproductive trade‐offs in a long‐lived bird species: condition‐dependent reproductive allocation maintains female survival and offspring quality

Life history theory is an essential framework to understand the evolution of reproductive allocation. It predicts that individuals of long‐lived species favour their own survival over current reproduction, leading individuals to refrain from reproducing under harsh conditions. Here we test this prediction in a long‐lived bird species, the Siberian jay Perisoreus infaustus. Long‐term data revealed that females rarely refrain from breeding, but lay smaller clutches in unfavourable years. Neither offspring body size, female survival nor offspring survival until the next year was influenced by annual condition, habitat quality, clutch size, female age or female phenotype. Given that many nests failed due to nest predation, the variance in the number of fledglings was higher than the variance in the number of eggs and female survival. An experimental challenge with a novel pathogen before egg laying largely replicated these patterns in two consecutive years with contrasting conditions. Challenged females refrained from breeding only in the unfavourable year, but no downstream effects were found in either year. Taken together, these findings demonstrate that condition‐dependent reproductive allocation may serve to maintain female survival and offspring quality, supporting patterns found in long‐lived mammals. We discuss avenues to develop life history theory concerning strategies to offset reproductive costs.