The basidiomycete Schizophyllum commune has the highest level of genetic polymorphism known among living organisms. In a previous study, it was also found to have a moderately high per-generation mutation rate of 2×10−8, likely contributing to its high polymorphism. However, this rate has been measured only in an experiment on Petri dishes, and it is unclear how it translates to natural populations. Here, we used an experimental design that measures the rate of accumulation of de novo mutations in a linearly growing mycelium. We show that S. commune accumulates mutations at a rate of 1.24×10−7 substitutions per nucleotide per meter of growth, or ∼2.04×10−11 per nucleotide per cell division. In contrast to what has been observed in a number of species with extensive vegetative growth, this rate does not decline in the course of propagation of a mycelium. As a result, even a moderate per-cell-division mutation rate in S. commune can translate into a very high per-generation mutation rate when the number of cell divisions between consecutive meiosis is large.

AbstractThe number of mutations that occur per nucleotide per generation varies between species by several orders of magnitude. In multicellular eukaryotes, the per generation mutation rate depends both on the per cell division mutation rate and on the number of germline cell divisions per generation. In a range of species, from fungi to humans, the number of germline cell divisions is lower than that of somatic cells, reducing the mutation burden on the offspring. The basidiomycete Schizophyllum commune has the highest level of genetic polymorphism known among eukaryotes. In a previous study, it was also found to have a high per generation mutation rate, probably contributing to its high polymorphism. However, this rate has been measured only in a breeding experiment on Petri dishes, and it is unclear how this result translates to natural populations. Here, we used an experimental design that measures the rate of accumulation of de novo mutations in a linearly growing mycelium. We show that S. commune accumulates mutations at a uniform rate of 1.4·10−7 substitutions per nucleotide per meter of growth, which is 3 orders of magnitude higher than the corresponding rates in the oak Quercus robur and the fungus Armillaria gallica. This figure is consistent with the estimate obtained before, and suggests the lack of a dedicated germline in this system. If so, even a low per cell division mutation rate can translate into a very high per generation mutation rate when the number of cell divisions between consecutive meioses is large.

BackgroundNatural selection is possible only because all species produce more offsprings than what is needed to maintain the population. Still, the lifetime number of offspring varies widely across species. One may expect natural selection to be stronger in high-fecundity species. Alternatively, natural selection could be stronger in species where a female invests more into an individual offspring. This issue needed to be addressed empirically.ResultsWe analyzed the prevalence of loss-of-function alleles in 35 metazoan species and have found that the strength of negative selection does not correlate with lifetime fecundity or other life-history traits.ConclusionsHigher random mortality in high-fecundity species may negate the effect of increased opportunity for selection. Perhaps, invariance of the strength of negative selection across a wide variety of species emerges because natural selection optimized the life history in each of them, leading to the strongest possible competition.ReviewersThis article was reviewed by Nicolas Galtier and I. King Jordan.Electronic supplementary materialThe online version of this article (10.1186/s13062-018-0206-9) contains supplementary material, which is available to authorized users.

Background: Natural selection is possible only because all species produce more offsprings than what is needed to maintain the population. Still, the lifetime number of offspring varies widely across species. One may expect natural selection to be stronger in high-fecundity species. Alternatively, natural selection could be stronger in species where a female invests more into an individual offspring. This issue needed to be addressed empirically.