Antagonistically pleiotropic allele increases lifespan and late-life reproduction at the cost of early-life reproduction and individual fitness

Alexei A. Maklakov, Hanne Carlsson, Philip Denbaum, Martin I. Lind, Brian Mautz, Andrea Hinas, Simone Immler

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Abstract

Evolutionary theory of ageing maintains that increased allocation to early-life reproduction results in reduced somatic maintenance, which is predicted to compromise longevity and late-life reproduction. This prediction has been challenged by the discovery of long-lived mutants with no loss of fecundity. The first such long-lived mutant was found in the nematode worm Caenorhabditis elegans. Specifically, partial-loss-of-function mutation in the age-1 gene, involved in the nutrient-sensing insulin/insulin-like growth factor (IIS) signalling pathway, confers longevity, as well as increased resistance to pathogens and to temperature stress without appreciable fitness detriment. Here we show that the long-lived age-1(hx546) mutant has reduced fecundity and offspring production in early-life but increased fecundity, hatching success and offspring production in late-life compared to wild-type worms under standard conditions. However, reduced early-life performance of long-lived mutant animals was not fully compensated by improved performance in late-life and resulted in reduced individual fitness. These results suggest that the age-1(hx546) allele has opposing effects on early-life versus late-life fitness in accordance with antagonistic pleiotropy and disposable soma theories of ageing. These findings support the theoretical conjecture that experimental studies based on standing genetic variation underestimate the importance of antagonistic pleiotropy in the evolution of ageing.
Original languageEnglish
JournalProceedings of the Royal Society B: Biological Sciences
Volume284
Issue number1856
DOIs
Publication statusPublished - 14 Jun 2017

Keywords

  • Ageing
  • senescence
  • evolutionary genetics
  • life-history trade-off

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