Atypical meiosis can be adaptive in outcrossedS. pombedue towtfmeiotic drivers

Abstract

Killer meiotic drivers are genetic parasites that destroy ‘sibling’ gametes lacking the driver allele. The fitness costs of drive can lead to selection of unlinked suppressors. This suppression could involve evolutionary tradeoffs that compromise gametogenesis and contribute to infertility. Schizosaccharomyces pombe, an organism containing numerous gamete-killing wtf drivers, offers a tractable system to test this hypothesis. Here, we demonstrate that in scenarios analogous to outcrossing, wtf drivers generate a fitness landscape in which atypical gametes, such as aneuploids and diploids, are advantageous. In this context, wtf drivers can decrease the fitness cost of mutations that disrupt meiotic fidelity and, in some circumstances, can even make such mutations beneficial. Moreover, we find that S. pombe isolates vary greatly in their ability to make haploid gametes, with some isolates generating more than 25% aneuploid or diploid gametes. This work empirically demonstrates the potential for meiotic drivers to shape the evolution of gametogenesis.

The wtf meiotic driver gene family has unexpectedly persisted for over 100 million years

“…We then introduced the plasmids into S. cerevisiae and analyzed the phenotypes of the resulting strains. We found that induction of each of the putative Wtf poison proteins, except S. In S. pombe, the Wtf antidote protein encoded by one wtf gene generally cannot neutralize the Wtf poison protein encoded by a different wtf gene (Bravo Núñez et al, 2020b, 2018aHu et al, 2017). Instead, a high level of sequence identity appears to be required for a Wtf antidote protein to co-assemble with and neutralize a Wtf poison protein (Nuckolls et al, 2020).…”

“…We first looked for similarities in overall gene structure between the S. pombe wtf genes and the candidate wtf genes in S. octosporus , S. osmophilus and S. cryophilus . The wtf genes of S. pombe have been classified into three broad categories: predicted meiotic drivers (4-14 per isolate), predicted suppressors of drive that encode only antidote proteins (9-17 per isolate) and genes of unknown function (4 in each isolate) (Bravo Núñez et al, 2020b, 2018a; Eickbush et al, 2019; Hu et al, 2017; Nuckolls et al, 2017). We found that the overall gene structure of the candidate wtf genes in all three species was similar to that of the 5-exon wtf drivers and 5-exon wtf suppressors in S. pombe (Figure 2A).…”

“…In S. pombe , the Wtf antidote protein encoded by one wtf gene generally cannot neutralize the Wtf poison protein encoded by a different wtf gene (Bravo Núñez et al, 2020b, 2018a; Hu et al, 2017). Instead, a high level of sequence identity appears to be required for a Wtf antidote protein to co-assemble with and neutralize a Wtf poison protein (Nuckolls et al, 2020).…”

“…pombe have been classified into three broad categories: predicted meiotic drivers (4-14 per isolate), predicted suppressors of drive that encode only antidote proteins (9-17 per isolate) and genes of unknown function (4 in each isolate) (Bravo Núñez et al, 2020b, 2018aEickbush et al, 2019;Hu et al, 2017;Nuckolls et al, 2017). We found that the overall gene structure of the candidate wtf genes in all three species was similar to that of the 5-exon wtf drivers and 5-exon wtf suppressors in S. pombe (Figure 2A).…”

“…To cause selective spore death, each wtf driver employs a poison protein and an antidote protein produced from two overlapping transcripts. All developing spores are exposed to the poison, while only spores that inherit the wtf drivers express the antidote and are rescued from destruction (Bravo Núñez et al, 2020a, 2020b, 2018aHu et al, 2017;Nuckolls et al, 2017).…”