Early-Life Silver Spoon Improves Survival and Breeding Performance of Adult Zebra Finches.

AbstractDevelopmental plasticity allows organisms to increase the fit between their phenotype and their early-life environment. The extent to which such plasticity also enhances adult fitness is not well understood, however, particularly when early-life and adult environments differ substantially. Using a cross-factorial design that manipulated diet at two life stages, we examined predictions of major hypotheses-silver spoon, environmental matching, and thrifty phenotype-concerning the joint impacts of early-life and adult diets on adult morphology/display traits, survival, and reproductive allocation. Overall, results aligned with the silver spoon hypothesis, which makes several predictions based on the premise that development in poor-quality environments constrains adult performance. Males reared and bred on a low-protein diet had lower adult survivorship than other male treatment groups; females' survivorship was higher than males' and not impacted by early diet. Measures of allocation to reproduction primarily reflected breeding diet, but where natal diet impacted reproduction, results supported the silver spoon. Both sexes showed reduced expression of display traits when reared on a low-protein diet. Results accord with other studies in supporting the relevance of the silver spoon hypothesis to birds and point to significant ramifications of sex differences in early-life viability selection on the applicability/strength of silver spoon effects.

Testing frameworks for early life effects: the developmental constraints and adaptive response hypotheses do not explain key fertility outcomes in wild female baboons.

In evolutionary ecology, two classes of explanations are frequently invoked to explain "early life effects" on adult outcomes. Developmental constraints (DC) explanations contend that costs of early adversity arise from limitations adversity places on optimal development. Adaptive response (AR) hypotheses propose that later life outcomes will be worse when early and adult environments are poorly "matched." Here, we use recently proposed mathematical definitions for these hypotheses and a quadratic-regression based approach to test the long-term consequences of variation in developmental environments on fertility in wild baboons. We evaluate whether low rainfall and/or dominance rank during development predict three female fertility measures in adulthood, and whether any observed relationships are consistent with DC and/or AR. Neither rainfall during development nor the difference between rainfall in development and adulthood predicted any fertility measures. Females who were low-ranking during development had an elevated risk of losing infants later in life, and greater change in rank between development and adulthood predicted greater risk of infant loss. However, both effects were statistically marginal and consistent with alternative explanations, including adult environmental quality effects. Consequently, our data do not provide compelling support for either of these common explanations for the evolution of early life effects.

Are parental condition transfer effects more widespread than is currently appreciated?

It has long been recognized that the environment experienced by parents can influence the traits of offspring (i.e. 'parental effects'). Much research has explored whether mothers respond to predictable shifts in environmental signals by modifying offspring phenotypes to best match future conditions. Many organisms experience conditions that theory predicts should favor the evolution of such 'anticipatory parental effects', but such predictions have received limited empirical support. 'Condition transfer effects' are an alternative to anticipatory effects that occur when the environment experienced by parents during development influences offspring fitness. Condition transfer effects occur when parents that experience high-quality conditions produce offspring that exhibit higher fitness irrespective of the environmental conditions in the offspring generation. Condition transfer effects are not driven by external signals but are instead a byproduct of past environmental quality. They are also likely adaptive but have received far less attention than anticipatory effects. Here, we review the generality of condition transfer effects and show that they are much more widespread than is currently appreciated. Condition transfer effects are observed across taxa and are commonly associated with experimental manipulations of resource conditions experienced by parents. Our Review calls for increased research into condition transfer effects when considering the role of parental effects in ecology and evolution.

Early life conditions influence fledging success and subsequent local recruitment rates in a declining migratory songbird, the Whinchat Saxicola rubetra.

Life history traits and environmental conditions influence reproductive success in animals, and consequences of these can influence subsequent survival and recruitment into breeding populations. Understanding influences on demographic rates is required to determine the causes of decline. Migratory species experience spatially and temporally variable conditions across their annual cycle, making identifying where the factors influencing demographic rates operate challenging. Here, we use the Whinchat Saxicola rubetra as a model declining long-distance migrant bird. We analyse 10 years of data from 247 nesting attempts and 2519 post-fledging observations of 1193 uniquely marked nestlings to examine the influence of life history traits, habitat characteristics and weather on survival of young from the nestling stage to local recruitment into the natal population. We detected potential silver spoon effects where conditions during the breeding stage influence subsequent apparent local recruitment rates, with higher recruitment for fledglings from larger broods, and recruitment rate negatively related to rainfall that chicks experienced in-nest. Additionally, extreme temperatures experienced pre- and post-fledging increased fledging success and recruitment rate. However, we could not determine whether this was driven by temperature influencing mortality during the post-fledging period or later in the annual cycle. Brood size declined with hatching date. In-nest survival increased with brood size and was highest at local temperature extremes. Furthermore, nest survival was highest at nests surrounded with 40%-60% vegetation cover of Bracken Pteridium aquilinum within 50 m of the nest. Our results show that breeding phenology and environmental factors may influence fledging success and recruitment in songbird populations, with conditions experienced during the nestling stage influencing local recruitment rates in Whinchats (i.e. silver spoon effect). Recruitment rates are key drivers of songbird population dynamics. Our results help identify some of the likely breeding season mechanisms that could be important population drivers.

Seychelles warblers with silver spoons: Juvenile body mass is a lifelong predictor of annual survival, but not annual reproduction or senescence.

The environment experienced during development, and its impact on intrinsic condition, can have lasting outcomes for individual phenotypes and could contribute to variation in adult senescence trajectories. However, the nature of this relationship in wild populations remains uncertain, owing to the difficulties in summarizing natal conditions and in long-term monitoring of individuals from free-roaming long-lived species. Utilizing a closely monitored, closed population of Seychelles warblers (Acrocephalus sechellensis), we determine whether juvenile body mass is associated with natal socioenvironmental factors, specific genetic traits linked to fitness in this system, survival to adulthood, and senescence-related traits. Juveniles born in seasons with higher food availability and into smaller natal groups (i.e., fewer competitors) were heavier. In contrast, there were no associations between juvenile body mass and genetic traits. Furthermore, size-corrected mass-but not separate measures of natal food availability, group size, or genetic traits-was positively associated with survival to adulthood, suggesting juvenile body mass is indicative of natal condition. Heavier juveniles had greater body mass and had higher rates of annual survival as adults, independent of age. In contrast, there was no association between juvenile mass and adult telomere length attrition (a measure of somatic stress) nor annual reproduction. These results indicate that juvenile body mass, while not associated with senescence trajectories, can influence the likelihood of surviving to old age, potentially due to silver-spoon effects. This study shows that measures of intrinsic condition in juveniles can provide important insights into the long-term fitness of individuals in wild populations.

Effects of Different Legume Seeds on Individual Performance in the Bean Bug, Riptortus pedestris (Hemiptera: Alydidae).

The bean bug, Riptortus pedestris (Fabricius), is a serious pest of legume crops in East Asia. Here, we report how the consumption of different types of legume seeds affects various aspects of nymphal and adult traits related to fitness in R. pedestris. Two experiments were conducted. In the first experiment, we assessed how R. pedestris nymphs and adults performed on one of 10 different legume seeds: adzuki bean, chickpea, cowpea, two kidney bean varieties (red, white), mung bean, peanut, small black bean, and two soybean varieties (black, yellow). Riptortus pedestris fed on yellow soybean and chickpea performed well in terms of nymphal survivorship and fecundity. However, R. pedestris fed on two kidney bean varieties suffered 100% nymphal mortality and reduced fecundity. Small black bean and black soybean supported high fecundity, but were not suitable for nymphal development. Lipid content was 4- to 11-folds higher in R. pedestris raised on peanuts than those on the others. In the second experiment, we recorded the key parameters of adult performance from R. pedestris assigned to one of nine combinations of three nymphal and three adult diets (yellow soybean, adzuki bean, peanut). Riptortus pedestris raised on yellow soybean during development produced more eggs over their lifetime than those raised on the others. However, this beneficial effect of consuming yellow soybean during development occurred only when yellow soybean was consumed during adulthood. Our data have implications for predicting the occurrence and population dynamics of this pest.

Distributions of LRS in varying environments.

The lifetime reproductive success (LRS) of individuals is affected by random events such as death, realized growth or realized reproduction, and the outcomes of these events can differ even when individuals have identical probabilities. Another source of randomness arises when these probabilities also change over time in variable environments. For structured populations in stochastic environments, we extend our recent method to determine how birth environment and birth stage determine the random distribution of the LRS. Our results provide a null model that quantifies effects on LRS of just the birth size or stage. Using Roe deer Capreolus capreolus as a case study, we show that the effect of an individual's birth environment on LRS varies with the frequency of environments and their temporal autocorrelation, and that lifetime performance is affected by changes in the pattern of environmental states expected as a result of climate change.

Thermal and nutritional environments during development exert different effects on adult reproductive success in Drosophila melanogaster.

Environments experienced during development have long-lasting consequences for adult performance and fitness. The "environmental matching" hypothesis predicts that individuals perform best when adult and developmental environments match whereas the "silver spoon" hypothesis expects that fitness is higher in individuals developed under favorable environments regardless of adult environments. Temperature and nutrition are the two most influential determinants of environmental quality, but it remains to be elucidated which of these hypotheses better explains the long-term effects of thermal and nutritional histories on adult fitness traits. Here we compared how the temperature and nutrition of larval environment would affect adult survivorship and reproductive success in the fruit fly, Drosophila melanogaster. The aspect of nutrition focused on in this study was the dietary protein-to-carbohydrate (P:C) ratio. The impact of low developmental and adult temperature was to improve adult survivorship. High P:C diet had a negative effect on adult survivorship when ingested during the adult stage, but had a positive effect when ingested during development. No matter whether adult and developmental environments matched or not, females raised in warm and protein-enriched environments produced more eggs than those raised in cool and protein-limiting environments, suggesting the presence of a significant silver spoon effect of larval temperature and nutrition. The effect of larval temperature on adult egg production was weak but persisted across the early adult stage whereas that of larval nutrition was initially strong but diminished rapidly after day 5 posteclosion. Egg production after day 5 was strongly influenced by the P:C ratio of the adult diet, indicating that the diet contributing mainly to reproduction had shifted from larval to adult diet. Our results highlight the importance of thermal and nutritional histories in shaping organismal performance and fitness and also demonstrate how the silver spoon effects of these aspects of environmental histories differ fundamentally in their nature, strength, and persistence.

Development time mediates the effect of larval diet on ageing and mating success of male antler flies in the wild.

High-quality developmental environments often improve individual performance into adulthood, but allocating toward early life traits, such as growth, development rate and reproduction, may lead to trade-offs with late-life performance. It is, therefore, uncertain how a rich developmental environment will affect the ageing process (senescence), particularly in wild insects. To investigate the effects of early life environmental quality on insect life-history traits, including senescence, we reared larval antler flies (Protopiophila litigata) on four diets of varying nutrient concentration, then recorded survival and mating success of adult males released in the wild. Declining diet quality was associated with slower development, but had no effect on other life-history traits once development time was accounted for. Fast-developing males were larger and lived longer, but experienced more rapid senescence in survival and lower average mating rate compared to slow developers. Ultimately, larval diet, development time and body size did not predict lifetime mating success. Thus, a rich environment led to a mixture of apparent benefits and costs, mediated by development time. Our results indicate that 'silver spoon' effects can be complex and that development time mediates the response of adult life-history traits to early life environmental quality.

Silver-spoon upbringing improves early-life fitness but promotes reproductive ageing in a wild bird.

Early-life conditions can have long-lasting effects and organisms that experience a poor start in life are often expected to age at a faster rate. Alternatively, individuals raised in high-quality environments can overinvest in early-reproduction resulting in rapid ageing. Here we use a long-term experimental manipulation of early-life conditions in a natural population of collared flycatchers (Ficedula albicollis), to show that females raised in a low-competition environment (artificially reduced broods) have higher early-life reproduction but lower late-life reproduction than females raised in high-competition environment (artificially increased broods). Reproductive success of high-competition females peaked in late-life, when low-competition females were already in steep reproductive decline and suffered from a higher mortality rate. Our results demonstrate that 'silver-spoon' natal conditions increase female early-life performance at the cost of faster reproductive ageing and increased late-life mortality. These findings demonstrate experimentally that natal environment shapes individual variation in reproductive and actuarial ageing in nature.

Silver spoon effects are constrained under extreme adult environmental conditions.

Early-life environmental conditions may generate cohort differences in individual fitness, subsequently affecting population growth rates. Three, nonmutually exclusive hypotheses predict the nature of these fitness differences: (1) silver spoon effects, where individuals born in good conditions perform better across the range of adult environments; (2) the "environmental saturation" hypothesis, where fitness differences only occur in intermediate adult environmental conditions; and (3) the "environmental matching" or "predictive adaptive response" (PAR) hypothesis, where fitness is highest when adult environmental conditions match those experienced in early life. We quantified the context-dependent effect of early-life environment on subsequent reproductive success, survival, and population growth rate (λ) of Svalbard reindeer, and explored how well it was explained by the three hypotheses. We found that good early-life conditions increased reproductive success compared to poor early-life conditions, but only when experiencing intermediate adult environmental conditions. This is the first example of what appears to be both "beneficial" and "detrimental environmental saturation" in a natural system. Despite weak early-life effects on survival, cohorts experiencing good early-life conditions contributed to higher population growth rates, when simulating realistic variation in adult environmental conditions. Our results show how the combination of a highly variable environment and biological constraints on fitness components can suppress silver spoon effects at both extremes of the adult environmental gradient.

Intergenerational fitness effects of the early life environment in a wild rodent.

The early life environment can have profound, long-lasting effects on an individual's fitness. For example, early life quality might (a) positively associate with fitness (a silver spoon effect), (b) stimulate a predictive adaptive response (by adjusting the phenotype to the quality of the environment to maximize fitness) or (c) be obscured by subsequent plasticity. Potentially, the effects of the early life environment can persist beyond one generation, though the intergenerational plasticity on fitness traits of a subsequent generation is unclear. To study both intra- and intergenerational effects of the early life environment, we exposed a first generation of bank voles to two early life stimuli (variation in food and social environment) in a controlled environment. To assess possible intra-generational effects, the reproductive success of female individuals was investigated by placing them in large outdoor enclosures in two different, ecologically relevant environments (population densities). Resulting offspring were raised in the same population densities where they were conceived and their growth was recorded. When adult, half of the offspring were transferred to opposite population densities to evaluate their winter survival, a crucial fitness trait for bank voles. Our setup allowed us to assess: (a) do early life population density cues elicit an intra-generational adaptive response, that is a higher reproductive success when the density matches the early life cues and (b) can early life stimuli of one generation elicit an intergenerational adaptive response in their offspring, that is a higher growth and winter survival when the density matches the early life cues of their mother. Our results show that the early life environment directly affects the phenotype and reproductive success of the focal generation, but adaptive responses are only evident in the offspring. Growth of the offspring is maintained only when the environment matches their mother's early life environment. Furthermore, winter survival of offspring also tended to be higher in high population densities if their mothers experienced an competitive early life. These results show that the early life environment can contribute to maintain high fitness in challenging environments, but not necessarily in the generation experiencing the early life cues.

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.

Ageing with a silver-spoon: A meta-analysis of the effect of developmental environment on senescence.

What determines variation between individuals in how they senesce, and are environmental conditions experienced during development relevant to late-life performance? We report a meta-analysis of studies of wild populations to determine how the quality of the environment experienced during development affects rates of survival and reproductive senescence. From studies of 14 bird or mammal species, we calculated effect sizes for the interaction between the effects of environmental quality during development and age in predicting survival (N = 18) or reproduction (N = 30) over time in late life. We found no evidence that developmental environment affected rates of survival senescence (ßmean = -1.2 × 10-4 ± 0.022SE). However, a better developmental environment was associated with slower rates of reproductive senescence in late life (ßmean = 0.062 ± 0.023SE), indicating a small, but significant, "silver-spoon" effect of early-life conditions that persisted through to late life. Our results illustrate how the effects of environmental conditions during development can persist throughout life, and indicate one possible cause of phenotypic plasticity in senescence.

Carryover effects from natal habitat type upon competitive ability lead to trait divergence or source-sink dynamics.

Local adaptation to rare habitats is difficult due to gene flow, but can occur if the habitat has higher productivity. Differences in offspring phenotypes have attracted little attention in this context. We model a scenario where the rarer habitat improves offspring's later competitive ability - a carryover effect that operates on top of local adaptation to one or the other habitat type. Assuming localised dispersal, so the offspring tend to settle in similar habitat to the natal type, the superior competitive ability of offspring remaining in the rarer habitat hampers immigration from the majority habitat. This initiates a positive feedback between local adaptation and trait divergence, which can thereafter be reinforced by coevolution with dispersal traits that match ecotype to habitat type. Rarity strengthens selection on dispersal traits and promotes linkage disequilibrium between locally adapted traits and ecotype-habitat matching dispersal. We propose that carryover effects may initiate isolation by ecology.

Direct and indirect effects of early-life environment on lifetime fitness of bighorn ewes.

Cohort effects, when a common environment affects long-term performance, can have a major impact on population dynamics. Very few studies of wild animals have obtained the necessary data to study the mechanisms leading to cohort effects. We exploited 42 years of individual-based data on bighorn sheep to test for causal links between birth density, body mass, age at first reproduction (AFR), longevity and lifetime reproductive success (LRS) using path analysis. Specifically, we investigated whether the effect of early-life environment on lifetime fitness was the result of indirect effects through body mass or direct effects of early-life environment on fitness. Additionally, we evaluated whether the effects of early-life environment were dependant on the environment experienced during adulthood. Contrary to expectation, the effect on LRS mediated through body mass was weak compared to the effects found via a delay in AFR, reduced longevity and the direct effect of birth density. Birth density also had an important indirect effect on LRS through reduced longevity, but only when adult density was high. Our results show that the potential long-term consequences of a harsh early-life environment on fitness are likely to be underestimated if investigations are limited to body mass instead of fitness at several life stages, or if the interactions between past and present environment are ignored.

Relating past and present diet to phenotypic and transcriptomic variation in the fruit fly.

BACKGROUND: Sub-optimal developmental diets often have adverse effects on long-term fitness and health. One hypothesis is that such effects are caused by mismatches between the developmental and adult environment, and may be mediated by persistent changes in gene expression. However, there are few experimental tests of this hypothesis. Here we address this using the fruit fly, Drosophila melanogaster. We vary diet during development and adulthood in a fully factorial design and assess the consequences for both adult life history traits and gene expression at middle and old age. RESULTS: We find no evidence that mismatches between developmental and adult diet are detrimental to either lifespan or fecundity. Rather, developmental and adult diet exert largely independent effects on both lifespan and gene expression, with adult diet having considerably more influence on both traits. Furthermore, we find effects of developmental diet on the transcriptome that persist into middle and old-age. Most of the genes affected show no correlation with the observed phenotypic effects of larval diet on lifespan. However, in each sex we identify a cluster of ribosome, transcription, and translation-related genes whose expression is altered across the lifespan and negatively correlated with lifespan. CONCLUSIONS: As several recent studies have linked decreased expression of ribosomal and transcription related proteins to increased lifespan, these provide promising candidates for mediating the effects of larval diet on lifespan. We place our findings in the context of theories linking developmental conditions to late-life phenotypes and discuss the likelihood that gene expression differences caused by developmental exposure causally relate to adult ageing phenotypes.

Childhood and adult socioeconomic position interact to predict health in mid life in a cohort of British women.

BACKGROUND: Low childhood socioeconomic position (cSEP) is associated with poorer adult health, even after adult socioeconomic position (aSEP) is adjusted for. However, whether cSEP and aSEP combine additively or non-additively in predicting adult health is less well studied. Some evidence suggests that the combination of low cSEP and low aSEP is associated with worse health than would be predicted from the sum of their individual effects. METHODS: Using data from female members of the British National Child Development Study cohort, we developed continuous quantitative measures of aSEP and cSEP, and used these to predict self-rated health at ages 23, 33, and 42. RESULTS: Lower aSEP predicted poorer heath at all ages. Lower cSEP predicted poorer health at all ages, even after adjustment for aSEP, but the direct effects of cSEP were substantially weaker than those of aSEP. At age 23, the effects of cSEP and aSEP were additive. At ages 33 and 42, cSEP and aSEP interacted, such that the effects of low aSEP on health were more negative if cSEP had also been low. CONCLUSIONS: As women age, aSEP and cSEP may affect their health interactively. High cSEP, by providing a good start in life, may be partially protective against later negative impacts of low aSEP. We relate this to the extended 'silver spoon' principle recently documented in a non-human species.

Long-term fitness consequences of early environment in a long-lived ungulate.

Cohort effects can be a major source of heterogeneity and play an important role in population dynamics. Silver-spoon effects, when environmental quality at birth improves future performance regardless of the adult environment, can induce strong lagged responses on population growth. Alternatively, the external predictive adaptive response (PAR) hypothesis predicts that organisms will adjust their developmental trajectory and physiology during early life in anticipation of expected adult conditions but has rarely been assessed in wild species. We used over 40 years of detailed individual monitoring of bighorn ewes (Ovis canadensis) to quantify long-term cohort effects on survival and reproduction. We then tested both the silver-spoon and the PAR hypotheses. Cohort effects involved a strong interaction between birth and current environments: reproduction and survival were lowest for ewes that were born and lived at high population densities. This interaction, however, does not support the PAR hypothesis because individuals with matching high-density birth and adult environments had reduced fitness. Instead, individuals born at high density had overall lower lifetime fitness suggesting a silver-spoon effect. Early-life conditions can induce long-term changes in fitness components, and their effects on cohort fitness vary according to adult environment.

Food availability affects adult survival trajectories depending on early developmental conditions.

Food availability modulates survival in interaction with (for example) competition, disease and predators, but to what extent food availability in natural populations affects survival independent of these factors is not well known. We tested the effect of food availability on lifespan and actuarial senescence in a large population of captive zebra finches by increasing the effort required to obtain food, reflecting natural contrasts in food availability. Food availability may not affect all individuals equally and we therefore created heterogeneity in phenotypic quality by raising birds with different numbers of siblings. Low food availability had no effect on lifespan for individuals from benign developmental conditions (raised in small broods), but shortened lifespan for individuals from harsh developmental conditions. The lifespan difference arose through higher baseline mortality rate of individuals from harsh developmental conditions, despite a decrease in the rate of actuarial senescence. We found no evidence for sex-specific environmental sensitivity, but females lived shorter than males due to increased actuarial senescence. Thus, low food availability by itself shortens lifespan, but only in individuals from harsh developmental conditions. Our food availability manipulation resembles dietary restriction as applied to invertebrates, where it extends lifespan in model organisms and we discuss possible reasons for the contrasting results.