Larval crowding accelerates C. elegans development and reduces lifespan.

Environmental conditions experienced during animal development are thought to have sustained impact on maturation and adult lifespan. Here we show that in the model organism C. elegans developmental rate and adult lifespan depend on larval population density, and that this effect is mediated by excr...

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Main Authors: Andreas H Ludewig, Clotilde Gimond, Joshua C Judkins, Staci Thornton, Dania C Pulido, Robert J Micikas, Frank Döring, Adam Antebi, Christian Braendle, Frank C Schroeder
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2017-04-01
Series:PLoS Genetics
Online Access:http://europepmc.org/articles/PMC5402976?pdf=render
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spelling doaj-ae12795da473417daaad597e7fbe26652020-11-24T21:51:08ZengPublic Library of Science (PLoS)PLoS Genetics1553-73901553-74042017-04-01134e100671710.1371/journal.pgen.1006717Larval crowding accelerates C. elegans development and reduces lifespan.Andreas H LudewigClotilde GimondJoshua C JudkinsStaci ThorntonDania C PulidoRobert J MicikasFrank DöringAdam AntebiChristian BraendleFrank C SchroederEnvironmental conditions experienced during animal development are thought to have sustained impact on maturation and adult lifespan. Here we show that in the model organism C. elegans developmental rate and adult lifespan depend on larval population density, and that this effect is mediated by excreted small molecules. By using the time point of first egg laying as a marker for full maturity, we found that wildtype hermaphrodites raised under high density conditions developed significantly faster than animals raised in isolation. Population density-dependent acceleration of development (Pdda) was dramatically enhanced in fatty acid β-oxidation mutants that are defective in the biosynthesis of ascarosides, small-molecule signals that induce developmental diapause. In contrast, Pdda is abolished by synthetic ascarosides and steroidal ligands of the nuclear hormone receptor DAF-12. We show that neither ascarosides nor any known steroid hormones are required for Pdda and that another chemical signal mediates this phenotype, in part via the nuclear hormone receptor NHR-8. Our results demonstrate that C. elegans development is regulated by a push-pull mechanism, based on two antagonistic chemical signals: chemosensation of ascarosides slows down development, whereas population-density dependent accumulation of a different chemical signal accelerates development. We further show that the effects of high larval population density persist through adulthood, as C. elegans larvae raised at high densities exhibit significantly reduced adult lifespan and respond differently to exogenous chemical signals compared to larvae raised at low densities, independent of density during adulthood. Our results demonstrate how inter-organismal signaling during development regulates reproductive maturation and longevity.http://europepmc.org/articles/PMC5402976?pdf=render
collection DOAJ
language English
format Article
sources DOAJ
author Andreas H Ludewig
Clotilde Gimond
Joshua C Judkins
Staci Thornton
Dania C Pulido
Robert J Micikas
Frank Döring
Adam Antebi
Christian Braendle
Frank C Schroeder
spellingShingle Andreas H Ludewig
Clotilde Gimond
Joshua C Judkins
Staci Thornton
Dania C Pulido
Robert J Micikas
Frank Döring
Adam Antebi
Christian Braendle
Frank C Schroeder
Larval crowding accelerates C. elegans development and reduces lifespan.
PLoS Genetics
author_facet Andreas H Ludewig
Clotilde Gimond
Joshua C Judkins
Staci Thornton
Dania C Pulido
Robert J Micikas
Frank Döring
Adam Antebi
Christian Braendle
Frank C Schroeder
author_sort Andreas H Ludewig
title Larval crowding accelerates C. elegans development and reduces lifespan.
title_short Larval crowding accelerates C. elegans development and reduces lifespan.
title_full Larval crowding accelerates C. elegans development and reduces lifespan.
title_fullStr Larval crowding accelerates C. elegans development and reduces lifespan.
title_full_unstemmed Larval crowding accelerates C. elegans development and reduces lifespan.
title_sort larval crowding accelerates c. elegans development and reduces lifespan.
publisher Public Library of Science (PLoS)
series PLoS Genetics
issn 1553-7390
1553-7404
publishDate 2017-04-01
description Environmental conditions experienced during animal development are thought to have sustained impact on maturation and adult lifespan. Here we show that in the model organism C. elegans developmental rate and adult lifespan depend on larval population density, and that this effect is mediated by excreted small molecules. By using the time point of first egg laying as a marker for full maturity, we found that wildtype hermaphrodites raised under high density conditions developed significantly faster than animals raised in isolation. Population density-dependent acceleration of development (Pdda) was dramatically enhanced in fatty acid β-oxidation mutants that are defective in the biosynthesis of ascarosides, small-molecule signals that induce developmental diapause. In contrast, Pdda is abolished by synthetic ascarosides and steroidal ligands of the nuclear hormone receptor DAF-12. We show that neither ascarosides nor any known steroid hormones are required for Pdda and that another chemical signal mediates this phenotype, in part via the nuclear hormone receptor NHR-8. Our results demonstrate that C. elegans development is regulated by a push-pull mechanism, based on two antagonistic chemical signals: chemosensation of ascarosides slows down development, whereas population-density dependent accumulation of a different chemical signal accelerates development. We further show that the effects of high larval population density persist through adulthood, as C. elegans larvae raised at high densities exhibit significantly reduced adult lifespan and respond differently to exogenous chemical signals compared to larvae raised at low densities, independent of density during adulthood. Our results demonstrate how inter-organismal signaling during development regulates reproductive maturation and longevity.
url http://europepmc.org/articles/PMC5402976?pdf=render
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