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Germline mutation rate is elevated in young and old parents in Caenorhabditis remanei

The effect of parental age on germline mutation rate across generations is not fully understood. While some studies report a positive linear relationship of mutation rate with increasing age, others suggest that mutation rate varies with age but not in a linear fashion. We investigated the effect of...

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Autores principales: Chen, Hwei-yen, Krieg, Therese, Mautz, Brian, Jolly, Cécile, Scofield, Douglas, Maklakov, Alexei A, Immler, Simone
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10692996/
https://www.ncbi.nlm.nih.gov/pubmed/38045724
http://dx.doi.org/10.1093/evlett/qrad052
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author Chen, Hwei-yen
Krieg, Therese
Mautz, Brian
Jolly, Cécile
Scofield, Douglas
Maklakov, Alexei A
Immler, Simone
author_facet Chen, Hwei-yen
Krieg, Therese
Mautz, Brian
Jolly, Cécile
Scofield, Douglas
Maklakov, Alexei A
Immler, Simone
author_sort Chen, Hwei-yen
collection PubMed
description The effect of parental age on germline mutation rate across generations is not fully understood. While some studies report a positive linear relationship of mutation rate with increasing age, others suggest that mutation rate varies with age but not in a linear fashion. We investigated the effect of parental age on germline mutations by generating replicated mutation accumulation lines in Caenorhabditis remanei at three parental ages (“Young T1” [Day 1], “Peak T2” [Day 2], and “Old T5” [Day 5] parents). We conducted whole-genome resequencing and variant calling to compare differences in mutation rates after three generations of mutation accumulation. We found that Peak T2 lines had an overall reduced mutation rate compared to Young T1 and Old T5 lines, but this pattern of the effect varied depending on the variant impact. Specifically, we found no high-impact variants in Peak T2 lines, and modifiers and up- and downstream gene variants were less frequent in these lines. These results suggest that animals at the peak of reproduction have better DNA maintenance and repair compared to young and old animals. We propose that C. remanei start to reproduce before they optimize their DNA maintenance and repair, trading the benefits of earlier onset of reproduction against offspring mutation load. The increase in offspring mutation load with age likely represents germline senescence.
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spelling pubmed-106929962023-12-03 Germline mutation rate is elevated in young and old parents in Caenorhabditis remanei Chen, Hwei-yen Krieg, Therese Mautz, Brian Jolly, Cécile Scofield, Douglas Maklakov, Alexei A Immler, Simone Evol Lett Letters The effect of parental age on germline mutation rate across generations is not fully understood. While some studies report a positive linear relationship of mutation rate with increasing age, others suggest that mutation rate varies with age but not in a linear fashion. We investigated the effect of parental age on germline mutations by generating replicated mutation accumulation lines in Caenorhabditis remanei at three parental ages (“Young T1” [Day 1], “Peak T2” [Day 2], and “Old T5” [Day 5] parents). We conducted whole-genome resequencing and variant calling to compare differences in mutation rates after three generations of mutation accumulation. We found that Peak T2 lines had an overall reduced mutation rate compared to Young T1 and Old T5 lines, but this pattern of the effect varied depending on the variant impact. Specifically, we found no high-impact variants in Peak T2 lines, and modifiers and up- and downstream gene variants were less frequent in these lines. These results suggest that animals at the peak of reproduction have better DNA maintenance and repair compared to young and old animals. We propose that C. remanei start to reproduce before they optimize their DNA maintenance and repair, trading the benefits of earlier onset of reproduction against offspring mutation load. The increase in offspring mutation load with age likely represents germline senescence. Oxford University Press 2023-10-17 /pmc/articles/PMC10692996/ /pubmed/38045724 http://dx.doi.org/10.1093/evlett/qrad052 Text en © The Author(s) 2023. Published by Oxford University Press on behalf of The Society for the Study of Evolution (SSE) and European Society for Evolutionary Biology (ESEN). https://creativecommons.org/licenses/by/4.0/This is an Open Access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle Letters
Chen, Hwei-yen
Krieg, Therese
Mautz, Brian
Jolly, Cécile
Scofield, Douglas
Maklakov, Alexei A
Immler, Simone
Germline mutation rate is elevated in young and old parents in Caenorhabditis remanei
title Germline mutation rate is elevated in young and old parents in Caenorhabditis remanei
title_full Germline mutation rate is elevated in young and old parents in Caenorhabditis remanei
title_fullStr Germline mutation rate is elevated in young and old parents in Caenorhabditis remanei
title_full_unstemmed Germline mutation rate is elevated in young and old parents in Caenorhabditis remanei
title_short Germline mutation rate is elevated in young and old parents in Caenorhabditis remanei
title_sort germline mutation rate is elevated in young and old parents in caenorhabditis remanei
topic Letters
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10692996/
https://www.ncbi.nlm.nih.gov/pubmed/38045724
http://dx.doi.org/10.1093/evlett/qrad052
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