Genetic Villains: Killer Meiotic Drivers

Abstract

Unbiased allele transmission into progeny is a fundamental genetic concept canonized as Mendel's Law of Segregation. Not all alleles, however, abide by the law. Killer meiotic drivers are ultra-selfish DNA sequences that are transmitted into more than half (sometimes all) of the meiotic products generated by a heterozygote. As their name implies, these loci gain a transmission advantage in heterozygotes by destroying otherwise viable meiotic products that do not inherit the driver. We review and classify killer meiotic drive genes across a wide spectrum of eukaryotes. We discuss how analyses of these ultra-selfish genes can lead to greater insight into the mechanisms of gametogenesis and the causes of infertility.

Keywords: killer meiotic drivers; meiosis; meiotic drive; segregation distortion; selfish genes.

Figure 1. Hypothetical evolution of meiotic drivers

i) A meiotic drive locus (A) has the ability to generate drive when heterozygous. Homozygotes fail to exhibit drive. ii) If a drive allele becomes fixed in a population, drive will not be observed because all individuals will be homozygous. iii) Another possible path is that the driver (A) could duplicate, creating a drive locus (b) that is free to diverge. The original drive locus could accumulate mutations and be lost in the population. iv) As drivers are generally deleterious for fitness, unlinked suppressors (c) are likely to evolve. v) Over time, populations (represented in ii and iv) evolve distinct landscapes of meiotic drivers and suppressors. If these two populations were to merge (v), the phenotypes of cryptic drivers could emerge in hybrid individuals. In this way, meiotic drivers can contribute to hybrid infertility and speciation.

Figure 2 (Key Figure). General mechanisms of meiotic drivers

(A) Killer-target meiotic drivers create a killer element that acts only on the meiotic products that inherit the target. The target can be a DNA locus, or a gene product encoded by the locus. (B) Poison-antidote meiotic drivers create a transacting poison that acts indiscriminately on all meiotic products. Only meiotic products that inherit the meiotic drive locus, and thus the antidote, live. A clear way to distinguish the two types is to consider the phenotypes of mutants in which the gamete (or spore)-specific component is absent. In killer-target systems, individuals containing at least one copy of the killer allele, but no target, exhibit no killing of meiotic products. In contrast, in poison-antidote systems, all the meiotic products are destroyed in individuals that encode the poison but lack the antidote.