Life history stage-dependent nuclear selection in chimeric fungi

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Abstract

A single hyphal compartment of the filamentous fungus Neurospora crassa may contain tens or hundreds of nuclei, sharing macromolecules with each other, and, via a continuous cytoplasm, with the nuclei in other compartments. Nuclear lineages acquire mutations with each mitosis, which, combined with the autonomous mitosis of nuclei, has fueled speculation that multilevel selection may occur, both upon the mycelium, and upon individual nuclear populations. Here, we combine experiments on fungal chimera formed from two auxotrophically and epitopically labeled nuclear populations, with specially created microscopy toolkit for extracting the proportions of the two nucleotypes to analyze the strength of nuclear-level selective forces at different stages in the fungal life history. We find strong nucleotype-selective forces during spore-germination and establishment of the mycelium, and no evidence of selection on nuclei inside a growing mycelium. The kinetics of mycelial initiation from individual spores therefore allow for the selection of nuclear compositions best adapted to the fungus’ environment, in accordance with the hypothesized function of unicellular life history stages for purging deleterious mutations.
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Abstract A single hyphal compartment of the filamentous fungus Neurospora crassa may contain tens or hundreds of nuclei, sharing macromolecules with each other, and, via a continuous cytoplasm, with the nuclei in other compartments. Nuclear lineages acquire mutations with each mitosis, which, combined with the autonomous mitosis of nuclei, has fueled speculation that multilevel selection may occur, both upon the mycelium, and upon individual nuclear populations. Here, we combine experiments on fungal chimera formed from two auxotrophically and epitopically labeled nuclear populations, with specially created microscopy toolkit for extracting the proportions of the two nucleotypes to analyze the strength of nuclear-level selective forces at different stages in the fungal life history. We find strong nucleotype-selective forces during spore-germination and establishment of the mycelium, and no evidence of selection on nuclei inside a growing mycelium. The kinetics of mycelial initiation from individual spores therefore allow for the selection of nuclear compositions best adapted to the fungus’ environment, in accordance with the hypothesized function of unicellular life history stages for purging deleterious mutations. Competing Interest Statement The authors have declared no competing interest. Footnotes ↵† mroper{at}math.ucla.edu

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License: CC-BY-NC-ND-4.0