Meiotic cohesin Rec8 imposes fitness costs on fission yeast gametes to drive evolution of parental bias in gene expression

Differences between partner gametes, which evolved repeatedly in unicellular and multicellular eukaryotes, are central to biological phenomena such as non-Mendelian inheritance and sexual selection1–4. How functional asymmetries first emerge between equivalent partners is poorly understood due to limited experimental evidence. Here, we report that in the isogamous fission yeast Schizosaccharomyces pombe, partner P- and M-gametes differentially invest into zygotic development by making unequal amounts of the conserved meiotic cohesin Rec85. Driven by asymmetric partner communication, P-gametes produce Rec8 before fertilization to promote meiotic fidelity and production of viable spores in zygotes. However, this early Rec8 expression also causes genomic instabilities6 and imposes a fitness cost on P-gametes, revealing a trade-off between sexual success and gamete survival. Using biologically parametrized model and experimental evolution, we show that the Rec8 costs and benefits drive selection for biased parental investment and evolution of mating populations. Our work dissects a molecular mechanism that selects for functional gamete asymmetries in an isogamous species, providing rare experimental evidence for an early step in the evolution of gamete dimorphism. Overall design: Heterothallic wild-type strains that produce only one gamete type and thus arrest as unmated cells (NMWT) or homothallic fus1? mutants, which arrested as mated pairs (F1), were grown exponentially in liquid MSL+N media and then diluted to density of O.D.600 = 1 and incubated at 30°C with 200 rpm agitation for 5 hours. The starved cells were collected by centrifugation, ~2·107 cells concentrated into 20 µL of media and spotted onto MSL-N solid media. After 10 hours of incubation at 25°C, mating efficiency reached approximately 80% and 6 mating spots (~1.2·108 cells) were harvested using inoculation loops, per biological replica (triplicates), for RNA extraction.