Inheritance of somatic mutations can affect fitness in monkeyflowers

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.