The spore killers, fungal meiotic driver elements

During meiosis, both alleles of any given gene should have equal chances of being inherited by the progeny. There are a number of reasons why, however, this is not the case, with one of the most intriguing instances presenting itself as the phenomenon of meiotic drive. Genes that are capable of driving can manipulate the ratio of alleles among viable meiotic products so that they are inherited in more than half of them. In many cases, this effect is achieved by direct antagonistic interactions, where the driving allele inhibits or otherwise eliminates the alternative allele. In ascomycete fungi, meiotic products are packaged directly into ascospores; thus, the effect of meiotic drive has been given the nefarious moniker, spore killing. In recent years, many of the known spore killers have been elevated from mysterious phenotypes to well-described systems at genetic, genomic, and molecular levels. In this review, we describe the known diversity of spore killers and synthesize the varied pieces of data from each system into broader trends regarding genome architecture, mechanisms of resistance, the role of transposable elements, their effect on population dynamics, speciation and gene flow, and finally how they may be developed as synthetic drivers. We propose that spore killing is common, but that it is under-observed because of a lack of studies on natural populations. We encourage researchers to seek new spore killers to build on the knowledge that these remarkable genetic elements can teach us about meiotic drive, genomic conflict, and evolution more broadly.

Automated summary

During meiosis, the phenomenon of meiotic drive allows certain genes to manipulate the inheritance of alleles, resulting in a higher frequency of one allele over the other. In ascomycete fungi, meiotic drive is known as spore killing and has recently been studied extensively at the genetic, genomic, and molecular levels. This review summarizes the known diversity of spore killers and explores their impacts on genome architecture, resistance mechanisms, population dynamics, speciation, and gene flow. The authors suggest that spore killing is common but under-observed in natural populations, and they encourage further research on this remarkable genetic phenomenon.