Female meiotic drive preferentially segregates derived metacentric chromosomes in Drosophila

Abstract

A vast diversity of karyotypes exists within and between species, yet the mechanisms that shape this diversity are poorly understood. Here we investigate the role of biased meiotic segregation--i.e., meiotic drive--in karyotype evolution. The closely related species, Drosophila americana and D. novamexicana, provide an ideal system to investigate mechanisms of karyotypic diversification. Since their recent divergence, D. americana has evolved two centromeric fusions: one between the 2nd and 3rd chromosomes, and another between the X and 4th chromosomes. The 2-3 fusion is fixed in D. americana, but the X-4 fusion is polymorphic and varies in frequency along a latitudinal cline. Here we evaluate the hypothesis that these derived metacentric chromosomes segregate preferentially to the egg nucleus during female meiosis in D. americana. Using two different methods, we show that the fused X-4 chromosome is transmitted at an average frequency of ~57%, exceeding expectations of 50:50 Mendelian segregation. Three paracentric inversions are found in the vicinity of the X-4 fusion and could potentially influence chromosome segregation. Using crosses between lines with differing inversion arrangements, we show that the transmission bias persists regardless of inversion status. Transmission rates are also biased in D. americana/D. novamexicana hybrid females, favoring both the X-4 and 2-3 fused arrangements over their unfused homologs. Our results show that meiotic drive influences chromosome segregation in D. americana favoring derived arrangements in its reorganized karyotype. Moreover, the fused centromeres are the facilitators of biased segregation rather than associated chromosomal inversions.