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

ABSTRACT: 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.

SUBMITTER: Pigeon G

PROVIDER: S-EPMC5413925 | biostudies-literature | 2017 Apr

REPOSITORIES: biostudies-literature

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

Pigeon Gabriel G Festa-Bianchet Marco M Pelletier Fanie F

Proceedings. Biological sciences 20170401 1853

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 conditi ...[more]

PMID: 28424347

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Project description:Despite intensive antibiotic treatment, Pseudomonas aeruginosa often persists in the airways of cystic fibrosis (CF) patients for decades, and can do so without antibiotic resistance development. Using high-throughput screening assays of bacterial survival after treatment with high concentrations of ciprofloxacin, we have determined the prevalence of persisters in a large patient cohort using 460 longitudinal isolates of P. aeruginosa from 39 CF patients. Isolates were classed as high persister variants (Hip) if they regrew following antibiotic treatment in at least 75% of the experimental replicates. Strain genomic data, isolate phenotyping, and patient treatment records were integrated in a lineage-based analysis of persister formation and clinical impact. In total, 19% of the isolates were classified as Hip and Hip emergence increased over lineage colonization time within 22 Hip+ patients. Most Hip+ lineages produced multiple Hip isolates, but few Hip+ lineages were dominated by Hip. While we observed no strong signal of adaptive genetic convergence within Hip isolates, they generally emerged in parallel or following the development of ciprofloxacin resistance and slowed growth. Transient lineages were majority Hip-, while strains that persisted over a clinically diagnosed 'eradication' period were majority Hip+. Patients received indistinguishable treatment regimens before Hip emergence, but Hip+ patients overall were treated significantly more than Hip- patients, signaling repeated treatment failure. When subjected to in vivo-similar antibiotic dosing, a Hip isolate survived better than a non-Hip in a structured biofilm environment. In sum, the Hip phenotype appears to substantially contribute to long-term establishment of a lineage in the CF lung environment. Our results argue against the existence of a single dominant molecular mechanism underlying bacterial antibiotic persistence. We instead show that many routes, both phenotypic and genetic, are available for persister formation and consequent increases in strain fitness and treatment failure in CF airways.

Dataset Information

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

Publications

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

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