Veni, vidi, vici: the success of wtf meiotic drivers in fission yeast

Abstract

Meiotic drivers are selfish DNA loci that can bias their own transmission into gametes. Owing to their transmission advantages, meiotic drivers can spread in populations even if the drivers or linked variants decrease organismal fitness. Meiotic drive was first formally described in the 1950s and is thought to be a powerful force shaping eukaryotic genomes. Classic genetic analyses have detected the action of meiotic drivers in plants, filamentous fungi, insects and vertebrates. Several of these drive systems have limited experimental tractability and relatively little is known about the molecular mechanisms of meiotic drive. Recently, however, meiotic drivers were discovered in a yeast species. The Schizosaccharomyces pombe wtf gene family contains several active meiotic drive genes. This review summarizes what is known about the wtf family and highlights its potential as a highly tractable experimental model for molecular and evolutionary characterization of meiotic drive.

Keywords: Schizosaccharomyces; infertility; meiosis; meitoic drive; speciation.

Figure 1

Meiotic drive in fission yeast. (a) The driving Sk wtf4 gene makes two proteins: a trans‐acting poison that is first expressed prior to the meiotic divisions and a gamete‐specific antidote expressed after gamete (spore) individualization. The gametes that do not carry the wtf driver allele are destroyed. (b) The Sk wtf4 poison and antidote proteins are made using alternative transcripts. Other wtf genes appear to share the ability to make two transcripts (top). Verified drive genes are shown in bold. A second class of wtf genes (bottom) appears to encode only a long transcript that is similar to the antidote transcript of Sk wtf4. (c) Model describing the hypothesized mechanisms of how the Wtf^poison protein kills and how the Wtf^antidote proteins neutralize the poisons [Colour figure can be viewed at http://wileyonlinelibrary.com]

Figure 2

Hypothetical evolutionary history of wtf genes in a population over time (left to right). The ancestral population did not carry driving wtf genes. The first wtf drive gene entered the population by mutation of an existing non‐driving gene, de novo gene birth, or by horizontal gene transfer. The wtf drive gene can spread in the population and birth new wtf drive genes via gene duplication (drivers are shown in shades of blue). Owing to the fitness costs of drivers, suppressors (shown in shades of green) are expected to emerge, perhaps from amongst the wtf drive genes themselves, through loss of the poison transcriptional or translational start sites. Fixation of a driver or successful antagonism by a suppressor could each contribute to the pseudogenization of a wtf driver. Suppressors lacking targets could also decay. These events are dynamic and ongoing, leading to a mix of functional drivers, suppressors, and pseudogene remnants in the genome [Colour figure can be viewed at http://wileyonlinelibrary.com]