Evolutionary persistence and divergence of the  tdk  killer meiotic driver family.
Killer meiotic drivers (KMDs) are selfish genetic elements that achieve super-Mendelian inheritance by selectively eliminating gametes lacking the driver. Although predicted to arise recurrently, KMDs are generally considered evolutionarily ephemeral-going extinct after fixation or host suppression. The identification of  tdk1  , a single-gene KMD in the fission yeast  Schizosaccharomyces pombe  , provides a model for studying KMD evolution. Here, we identify two divergent  tdk1  homologs (  tdk210  and  tdk203  ) from  S. cryophilus  , a fission yeast species that diverged ∼100 million years ago from  S. pombe  , as active KMDs. These three KMDs all act via post-germination killing, disrupting chromosome segregation in noncarrier progeny. Notably, they also exhibit striking functional divergences:  tdk1  ,  tdk210  , and  tdk203  are mutually incompatible (showing no cross-resistance), and the latter two act independently of Bdf1/Bdf2-host chromatin proteins required for  tdk1  killing. Phylogenetic analyses of the dozens of  tdk  family genes in  Schizosaccharomyces  support long-term persistence and rapid evolutionary dynamics of this gene family. Remarkably, homologs in distantly related fungal phyla display genomic and structural similarities to  Schizosaccharomyces tdk  genes, suggesting a deeply rooted origin of this KMD family in fungi. Our findings reveal that a single KMD family can undergo repeated functional innovation-generating mutually incompatible variants and rewiring host dependencies-while maintaining a conserved killing mode over deep evolutionary time.
Zhang FY, Jia GS, Ren JY, Suo F, Du TY, Zhang WC, Li W, Wang QM, Du LL, Hua Y