Conditions and properties of non-Mendelian transmission of recombinants in female meiosis

Abstract

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.