Diverse mating phenotypes impact the spread of wtf meiotic drivers in Schizosaccharomyces pombe

Abstract

Meiotic drivers are genetic elements that break Mendel's law of segregation to be transmitted into more than half of the offspring produced by a heterozygote. The success of a driver relies on outcrossing (mating between individuals from distinct lineages) because drivers gain their advantage in heterozygotes. It is, therefore, curious that Schizosaccharomyces pombe, a species reported to rarely outcross, harbors many meiotic drivers. To address this paradox, we measured mating phenotypes in S. pombe natural isolates. We found that the propensity for cells from distinct clonal lineages to mate varies between natural isolates and can be affected both by cell density and by the available sexual partners. Additionally, we found that the observed levels of preferential mating between cells from the same clonal lineage can slow, but not prevent, the spread of a wtf meiotic driver in the absence of additional fitness costs linked to the driver. These analyses reveal parameters critical to understanding the evolution of S. pombe and help explain the success of meiotic drivers in this species.

S. pombe wtf drivers use dual transcriptional regulation and selective protein exclusion from spores to cause meiotic drive

“…Some S . pombe natural isolates preferentially inbreed and some isolates generate disomic (aneuploid or diploid) spores at high frequencies (up to 46% of spores; [ 41 , 78 ]). Although it is hard to say if the wtf genes promoted the evolution of these traits, it is possible, as both traits effectively suppress fitness costs of wtf drivers [ 41 , 78 ].…”

“…pombe natural isolates preferentially inbreed and some isolates generate disomic (aneuploid or diploid) spores at high frequencies (up to 46% of spores; [ 41 , 78 ]). Although it is hard to say if the wtf genes promoted the evolution of these traits, it is possible, as both traits effectively suppress fitness costs of wtf drivers [ 41 , 78 ]. If these traits were selected for based on their ability to suppress drive, suppression likely came at a steep price to fitness, given that inbreeding and meiotic disruption are generally not good for fitness.…”

Genome-wide quantification of contributions to sexual fitness identifies genes required for spore viability and health in fission yeast

“…To perform live imaging, we spread isolated spores onto a YEA+SUP plate using beads. Immediately after the plates dried, we removed the beads from the plate and removed a circular punch of agar from the plate using a 1271E Arch Punch as previously described [ 96 ]. We inverted the agar and placed it top side down into a 35 mm glass bottom dish (No.…”

The search for Schizosaccharomyces fission yeasts in environmental metatranscriptomes

“…Knowledge of the natural environment of fission yeast will inform us on the natural temperature of this environment and thus to which temperatures most physiological processes the species is adapted, a factor of relevance for enzymatic dynamics (Pluskal et al, 2009), but also, for example, meiotic crossover rates (Hyppa et al, 2014). From the growth medium, we can deduce the number of asexual cell cycles that are possible before resources run out, giving information about the number of asexual versus sexual cycles in nature which is mostly unknown (Farlow et al, 2015; Hernández et al, 2021). The density in such a habitat will inform us of intraspecific competition and the need for haploid selfing or the potential for outcrossing (Hernández et al, 2021; Leupold, 1949; Nieuwenhuis et al, 2018).…”

“…From the growth medium, we can deduce the number of asexual cell cycles that are possible before resources run out, giving information about the number of asexual versus sexual cycles in nature which is mostly unknown (Farlow et al, 2015;Hernández et al, 2021). The density in such a habitat will inform us of intraspecific competition and the need for haploid selfing or the potential for outcrossing (Hernández et al, 2021;Leupold, 1949;Nieuwenhuis et al, 2018). Therefore, to fully utilize S. pombe as a model organism, knowledge of its natural growth environment is needed.…”