Long-Term Maintenance of Complex Chromosomal Inversion Polymorphism in Drosophila mediopunctata

Abstract

Natural selection is known to favor specific gene combinations, thereby shaping the evolution of recombination rates, often through epistatic interactions. However, the dynamics of these interacting factors within natural populations remain poorly understood. In this study, we investigate the long-term maintenance of a complex polymorphism involving linked, nonoverlapping chromosomal inversions in a natural population of Drosophila mediopunctata. Remarkably, even after 30 years—equivalent to roughly 340 generations—two major features have remained unexpectedly stable: the linkage disequilibrium (LD) between inversions, which deviates significantly from the theoretical prediction of decay, and a consistent seasonal cycle pattern of heterozygous excess and homozygous deficiencies. We explored the roles of recombination suppression, epistatic selection, and overdominance in maintaining this stability, examining their alignment with previously described patterns. Our findings reveal that moderate selection coefficients, such as s = 0.0407, are sufficient to maintain the observed LD for the most common haplotypes, albeit leading to an unstable equilibrium. Simulations further reveal that the introduction of overdominance stabilizes the system, enabling the long-term persistence of this complex inversion polymorphism across various frequency scenarios. The stability of this system appears to hinge on a delicate balance between LD, recombination rates, and selective pressures, with overdominance playing a critical role. Our findings highlight the significance of epistatic interactions and selective pressures in shaping evolutionary pathways in natural populations and offer a compelling example of natural selection acting on a complex inversion polymorphism, providing valuable insights into the evolutionary dynamics governing inversion systems.