Conditions and properties of non-Mendelian transmission of recombinants in female meiosis
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In female meiosis, each of the four chromatids in a tetrad has a 25% chance to be selected for transmission through the pronucleus, realizing Mendel’s second law. Here, we characterize a cheating but unselfish behaviour that has documented cases across diverse animal taxa including humans and flies, whereby chromatids with crossovers (COs) have a transmission advantage, resulting in increased production of recombinant offspring. Taking advantage of Drosophila ovarian physiology, we show that this form of meiotic cheating which we call recombinant drive occurs on the autosomes when females are under nutrient stress, potentially as a mechanism for recombination plasticity, while curiously, the effect is suppressed on the X by the distributive system. We explored recombinant drive using simulations and identified unique quantitative signatures that are at odds with several intrinsic properties of linkage. One violation is the production of more offspring with recombinant versus parental allele combinations, which we empirically demonstrated to be possible. Further, we show that recombinant drive can appear to modify CO patterning effectively acting as assurance and interference mechanisms, even when it has no influence on and acts downstream of CO spacing. We discuss the potential benefits and consequences of having a conserved method that can rapidly increase recombination in response to stress, and speculate on a mechanism for the preferential transmission of COs at meiosis II. Overall, our study revealed distinct properties and behaviours of a poorly understood, but potentially widespread, conserved phenomenon and offers avenues for broad detection and mechanistic dissection.
SIGNIFICANCE
Meiotic drivers, typically described as selfish, violate Mendel’s law of segregation to gain a transmission and evolutionary advantage. Here, we explore a form of unselfish drive, whereby chromatids with crossovers are more likely to be transmitted in female meiosis, resulting in increased production of offspring with novel allelic combinations. This is a form of Mendelian cheating called recombinant drive, and has been documented in some animals, including humans and flies. Using classical genetics and computational simulations, we uncovered unique consequences of recombinant drive, some of which even violate fundamental properties of recombination and linkage. Overall, our study begins to illuminate an otherwise poorly characterized but potentially conserved mechanism that has implications on evolutionary and population dynamics.
