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The unique life form of plants promotes the accumulation of somatic mutations that can be passed to offspring in the next generation, because the same meristem cells responsible for vegetative growth also generate gametes for sexual reproduction. However, little is known about the consequences of somatic mutation accumulation for offspring fitness. We evaluate the fitness effects of somatic mutations in Mimulus guttatus by comparing progeny from self-pollinations made within the same flower (autogamy) to progeny from self-pollinations made between stems on the same plant (geitonogamy). The effects of somatic mutations are evident from this comparison, as autogamy leads to homozygosity of a proportion of somatic mutations, but progeny from geitonogamy remain heterozygous for mutations unique to each stem. In two different experiments, we find consistent fitness effects of somatic mutations from individual stems. Surprisingly, several progeny groups from autogamous crosses displayed increases in fitness compared to progeny from geitonogamy crosses, likely indicating that beneficial somatic mutations occurred in some stems. These results support the hypothesis that somatic mutations accumulate during vegetative growth, but they are filtered by different forms of selection that occur throughout development, resulting in the culling of expressed deleterious mutations and the retention of beneficial mutations.
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Inheritance of somatic mutations can affect fitness in monkeyflowers
Abstract Plants have the ability to transmit mutations to progeny that arise through both meiotic and mitotic (somatic) cell divisions. This is because the same meristem cells responsible for vegetative growth will also generate gametes for sexual reproduction. Despite the potential for somatic mutations to contribute to genetic variation and adaptation, their role in plant evolution remains largely unexplored. We conducted experiments with the bush monkeyflower (Mimulus aurantiacus) to assess the phenotypic effects of somatic mutations inherited across generations. By generating self-pollinations within a flower (autogamy) or between flowers on different stems of the same plant (geitonogamy), we tracked the effects of somatic mutations transmitted to progeny. Autogamy and geitonogamy lead to different segregation patterns of somatic mutations among stems, with only autogamy resulting in offspring that are homozygous for somatic mutations specific to that stem. This allowed us to compare average phenotypic differences between pollination treatments that could be attributed to the inheritance of somatic variants. While most experimental units showed no impacts on fitness, in some cases, we detected increased seed production, as well as significant increases in drought tolerance, even though M. aurantiacus is already well adapted to drought conditions. We also found increased variance in drought tolerance following autogamy, consistent with the hypothesis that somatic mutations transmitted between generations can impact fitness. These results highlight the potential role of inherited somatic mutations as a relevant source of genetic variation in plant evolution.
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- PAR ID:
- 10591943
- Publisher / Repository:
- Oxford University Press
- Date Published:
- Journal Name:
- Journal of Evolutionary Biology
- Volume:
- 38
- Issue:
- 5
- ISSN:
- 1420-9101
- Format(s):
- Medium: X Size: p. 630-638
- Size(s):
- p. 630-638
- Sponsoring Org:
- National Science Foundation
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