Natural variation in life history and aging phenotypes is associated with mitochondrial DNA deletion frequency in <it>Caenorhabditis briggsae</it>

<p>Abstract</p> <p>Background</p> <p>Mutations that impair mitochondrial functioning are associated with a variety of metabolic and age-related disorders. A barrier to rigorous tests of the role of mitochondrial dysfunction in aging processes has been the lack of model...

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Main Authors: Smith Samson W, Knapp Jeremiah B, Martha Sarah R, de Haan Gene, Hicks Kiley A, Coleman-Hulbert Anna L, Estes Suzanne, Stein Kevin C, Denver Dee R
Format: Article
Language:English
Published: BMC 2011-01-01
Series:BMC Evolutionary Biology
Online Access:http://www.biomedcentral.com/1471-2148/11/11
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spelling doaj-26ecb34b2fa548b48597a4ed1fa688d22021-09-02T10:14:54ZengBMCBMC Evolutionary Biology1471-21482011-01-011111110.1186/1471-2148-11-11Natural variation in life history and aging phenotypes is associated with mitochondrial DNA deletion frequency in <it>Caenorhabditis briggsae</it>Smith Samson WKnapp Jeremiah BMartha Sarah Rde Haan GeneHicks Kiley AColeman-Hulbert Anna LEstes SuzanneStein Kevin CDenver Dee R<p>Abstract</p> <p>Background</p> <p>Mutations that impair mitochondrial functioning are associated with a variety of metabolic and age-related disorders. A barrier to rigorous tests of the role of mitochondrial dysfunction in aging processes has been the lack of model systems with relevant, naturally occurring mitochondrial genetic variation. Toward the goal of developing such a model system, we studied natural variation in life history, metabolic, and aging phenotypes as it relates to levels of a naturally-occurring heteroplasmic mitochondrial <it>ND5 </it>deletion recently discovered to segregate among wild populations of the soil nematode, <it>Caenorhabditis briggsae</it>. The normal product of <it>ND5 </it>is a central component of the mitochondrial electron transport chain and integral to cellular energy metabolism.</p> <p>Results</p> <p>We quantified significant variation among <it>C. briggsae </it>isolates for all phenotypes measured, only some of which was statistically associated with isolate-specific <it>ND5 </it>deletion frequency. We found that fecundity-related traits and pharyngeal pumping rate were strongly inversely related to <it>ND5 </it>deletion level and that <it>C. briggsae </it>isolates with high <it>ND5 </it>deletion levels experienced a tradeoff between early fecundity and lifespan. Conversely, oxidative stress resistance was only weakly associated with <it>ND5 </it>deletion level while ATP content was unrelated to deletion level. Finally, mean levels of reactive oxygen species measured <it>in vivo </it>showed a significant non-linear relationship with <it>ND5 </it>deletion level, a pattern that may be driven by among-isolate variation in antioxidant or other compensatory mechanisms.</p> <p>Conclusions</p> <p>Our findings suggest that the <it>ND5 </it>deletion may adversely affect fitness and mitochondrial functioning while promoting aging in natural populations, and help to further establish this species as a useful model for explicit tests of hypotheses in aging biology and mitochondrial genetics.</p> http://www.biomedcentral.com/1471-2148/11/11
collection DOAJ
language English
format Article
sources DOAJ
author Smith Samson W
Knapp Jeremiah B
Martha Sarah R
de Haan Gene
Hicks Kiley A
Coleman-Hulbert Anna L
Estes Suzanne
Stein Kevin C
Denver Dee R
spellingShingle Smith Samson W
Knapp Jeremiah B
Martha Sarah R
de Haan Gene
Hicks Kiley A
Coleman-Hulbert Anna L
Estes Suzanne
Stein Kevin C
Denver Dee R
Natural variation in life history and aging phenotypes is associated with mitochondrial DNA deletion frequency in <it>Caenorhabditis briggsae</it>
BMC Evolutionary Biology
author_facet Smith Samson W
Knapp Jeremiah B
Martha Sarah R
de Haan Gene
Hicks Kiley A
Coleman-Hulbert Anna L
Estes Suzanne
Stein Kevin C
Denver Dee R
author_sort Smith Samson W
title Natural variation in life history and aging phenotypes is associated with mitochondrial DNA deletion frequency in <it>Caenorhabditis briggsae</it>
title_short Natural variation in life history and aging phenotypes is associated with mitochondrial DNA deletion frequency in <it>Caenorhabditis briggsae</it>
title_full Natural variation in life history and aging phenotypes is associated with mitochondrial DNA deletion frequency in <it>Caenorhabditis briggsae</it>
title_fullStr Natural variation in life history and aging phenotypes is associated with mitochondrial DNA deletion frequency in <it>Caenorhabditis briggsae</it>
title_full_unstemmed Natural variation in life history and aging phenotypes is associated with mitochondrial DNA deletion frequency in <it>Caenorhabditis briggsae</it>
title_sort natural variation in life history and aging phenotypes is associated with mitochondrial dna deletion frequency in <it>caenorhabditis briggsae</it>
publisher BMC
series BMC Evolutionary Biology
issn 1471-2148
publishDate 2011-01-01
description <p>Abstract</p> <p>Background</p> <p>Mutations that impair mitochondrial functioning are associated with a variety of metabolic and age-related disorders. A barrier to rigorous tests of the role of mitochondrial dysfunction in aging processes has been the lack of model systems with relevant, naturally occurring mitochondrial genetic variation. Toward the goal of developing such a model system, we studied natural variation in life history, metabolic, and aging phenotypes as it relates to levels of a naturally-occurring heteroplasmic mitochondrial <it>ND5 </it>deletion recently discovered to segregate among wild populations of the soil nematode, <it>Caenorhabditis briggsae</it>. The normal product of <it>ND5 </it>is a central component of the mitochondrial electron transport chain and integral to cellular energy metabolism.</p> <p>Results</p> <p>We quantified significant variation among <it>C. briggsae </it>isolates for all phenotypes measured, only some of which was statistically associated with isolate-specific <it>ND5 </it>deletion frequency. We found that fecundity-related traits and pharyngeal pumping rate were strongly inversely related to <it>ND5 </it>deletion level and that <it>C. briggsae </it>isolates with high <it>ND5 </it>deletion levels experienced a tradeoff between early fecundity and lifespan. Conversely, oxidative stress resistance was only weakly associated with <it>ND5 </it>deletion level while ATP content was unrelated to deletion level. Finally, mean levels of reactive oxygen species measured <it>in vivo </it>showed a significant non-linear relationship with <it>ND5 </it>deletion level, a pattern that may be driven by among-isolate variation in antioxidant or other compensatory mechanisms.</p> <p>Conclusions</p> <p>Our findings suggest that the <it>ND5 </it>deletion may adversely affect fitness and mitochondrial functioning while promoting aging in natural populations, and help to further establish this species as a useful model for explicit tests of hypotheses in aging biology and mitochondrial genetics.</p>
url http://www.biomedcentral.com/1471-2148/11/11
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