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Influence of early-life nutrition on mortality and reproductive success during a subsequent famine in a preindustrial population.

ABSTRACT: Individuals with insufficient nutrition during development often experience poorer later-life health and evolutionary fitness. The Predictive Adaptive Response (PAR) hypothesis proposes that poor early-life nutrition induces physiological changes that maximize fitness in similar environments in adulthood and that metabolic diseases result when individuals experiencing poor nutrition during development subsequently encounter good nutrition in adulthood. However, although cohort studies have shown that famine exposure in utero reduces health in favorable later-life conditions, no study on humans has demonstrated the predicted fitness benefit under low later-life nutrition, leaving the evolutionary origins of such plasticity unexplored. Taking advantage of a well-documented famine and unique datasets of individual life histories and crop yields from two preindustrial Finnish populations, we provide a test of key predictions of the PAR hypothesis. Known individuals from fifty cohorts were followed from birth until the famine, where we analyzed their survival and reproductive success in relation to the crop yields around birth. We were also able to test whether the long-term effects of early-life nutrition differed between individuals of varying socioeconomic status. We found that, contrary to predictions of the PAR hypothesis, individuals experiencing low early-life crop yields showed lower survival and fertility during the famine than individuals experiencing high early-life crop yields. These effects were more pronounced among young individuals and those of low socioeconomic status. Our results do not support the hypothesis that PARs should have been favored by natural selection and suggest that alternative models may need to be invoked to explain the epidemiology of metabolic diseases.

SUBMITTER: Hayward AD

PROVIDER: S-EPMC3752237 | biostudies-other | 2013 Aug

REPOSITORIES: biostudies-other

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Influence of early-life nutrition on mortality and reproductive success during a subsequent famine in a preindustrial population.

Hayward Adam D AD Rickard Ian J IJ Lummaa Virpi V

Proceedings of the National Academy of Sciences of the United States of America 20130805 34

Individuals with insufficient nutrition during development often experience poorer later-life health and evolutionary fitness. The Predictive Adaptive Response (PAR) hypothesis proposes that poor early-life nutrition induces physiological changes that maximize fitness in similar environments in adulthood and that metabolic diseases result when individuals experiencing poor nutrition during development subsequently encounter good nutrition in adulthood. However, although cohort studies have shown ...[more]

PMID: 23918366

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Project description: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.

Project description:Variation in fitness between individuals in populations may be attributed to differing environmental conditions experienced among birth (or hatch) years (i.e., between cohorts). In this study, we tested whether cohort fitness could also be explained by environmental conditions experienced in years post-hatch, using 736 lifelong resighting histories of Greenland white-fronted geese (Anser albifrons flavirostris) marked in their first winter. Specifically, we tested whether variation in age at first successful reproduction, the size of the first successful brood and the proportion of successful breeders by cohort was explained by environmental conditions experienced on breeding areas in west Greenland during hatch year, those in adulthood prior to successful reproduction and those in the year of successful reproduction, using North Atlantic Oscillation indices as proxies for environmental conditions during these periods. Fifty-nine (8%) of all marked birds reproduced successfully (i.e., were observed on wintering areas with young) only once in their lifetime and 15 (2%) reproduced successfully twice or thrice. Variation in age at first successful reproduction was explained by the environmental conditions experienced during adulthood in the years prior to successful reproduction. Birds bred earliest (mean age 4) when environmental conditions were 'good' prior to the year of successful reproduction. Conversely, birds successfully reproduced at older ages (mean age 7) if they experienced adverse conditions prior to the year of successful reproduction. Hatch year conditions and an interaction between those experienced prior to and during the year of successful reproduction explained less (marginally significant) variation in age at first successful reproduction. Environmental conditions did not explain variation in the size of the first successful brood or the proportion of successful breeders. These findings show that conditions during adulthood prior to the year of successful reproduction are most important in determining the age at first successful reproduction in Greenland white-fronted geese. Very few birds bred successfully at all (most only once), which suggests that May environmental conditions on breeding areas have cohort effects that influence lifetime (and not just annual) reproductive success.

Dataset Information

Influence of early-life nutrition on mortality and reproductive success during a subsequent famine in a preindustrial population.

Publications

Influence of early-life nutrition on mortality and reproductive success during a subsequent famine in a preindustrial population.

Similar Datasets

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