Meiotic Drive and the Survival Probability of Newly Inverted Chromosomes

Abstract

When a new gene arrangement is generated by spontaneous mutation its survival is uncertain and largely unaffected by associated fitness effects. However, if a new chromosomal inversion is introduced into a population already polymorphic for inversions, then its survival probability will be a function of the relative size, position, and linkage phase of the gene rearrangements. This dependence on structural features is due to the complex meiotic behavior of overlapping inversions generating asymmetric dyads, which in turn cause both underdominance and meiotic drive/drag. Therefore, survival probabilities of new inversions can be expressed in terms of the probability of forming an asymmetric dyad via crossing over in meiosis I and the probability of recovery from that asymmetric dyad during disjunction in meiosis II. This model of female meiotic drive was parameterized with data from published experiments on laboratory constructs in Drosophila melanogaster. Generalizing this analysis to all possible inversions predicts a bias towards larger, proximally located inversions having a shorter persistence time in populations. These population genetic predictions are consistent with cytological evidence from natural populations of D. melanogaster. This research mathematically formalizes a cytogenetic mechanism for female meiotic drive/drag as the major force governing behavior of new gene arrangements entering populations, and therefore determining the genomic distribution of segregating inversion polymorphism.