Rapid evolution driven by translocation-associated selection during meiosis

The evolution of allele frequencies in a population is often ascribed to differential fitness among organisms carrying different alleles. However, selection during meiosis can substantially influence this process. Here, we studied the evolution of a hybrid yeast population over six meiotic generations and observed rapid allele frequency dynamics at many genomic loci. By tracking the whole population and analyzing single gametes we discovered that biased segregation pattern during meiosis can drive rapid evolutionary changes at translocation-linked loci. The inter-chromosomal translocation present in one parental strain creates quadrivalent structures that promote adjacent-1 segregation coupled with crossover formation over alternate segregation during meiosis. This ultimately increases the proportion of unbalanced gametes, and consequently alters allele frequencies in the population. These findings demonstrate that meiotic selection operates more broadly than previously recognized and constitutes a significant evolutionary force affecting population allele frequencies. Given the prevalence of inter-chromosomal translocations, biased segregation pattern may complement the established role of translocations in shaping evolutionary outcomes.