Ectopic expression of ovary expressed polo transcripts and duplicates in Drosophila melanogaster testis creates female-biased sex ratios



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Polo-like kinases (Plks) play vital roles in mitosis and meiosis. Drosophila melanogaster has a single Plk gene (polo) that is alternatively spliced into two transcripts that differ in their 5'- and 3'-UTR, but not in their coding sequence. Curiously, polo has also been duplicated multiple times within the evolution of the Drosophila genus. In D. pseudoobscura, the ancestral polo gene (Dpse-polo) is found on a neo-X chromosome, and there are two autosomal duplications (Dpse-polo-dup1 and Dpse-polo-dup2) that are predominately testis expressed. The precise roles of the polo transcripts and duplications in male meiosis are unknown. Here, we show that when the D. melanogaster ovary-derived polo mRNA or Dpse-polo mRNA is expressed in D. melanogaster testis, the number of female offspring is greater than the number of male offspring. In contrast, equal numbers of males and females are produced when testis-derived polo mRNA or Dpse-polo-dup1 are expressed in the D. melanogaster male germline. These results suggest that polo duplicates and transcripts are specialized for sex-specific meiotic functions, specifically related to equal inheritance of the X and Y sex chromosomes in the male germline. Consistent with such specialization, we find that Dpse-polo-dup1 has accumulated significantly more amino acid substitutions than Dpse-polo since the duplication event. We hypothesize that the sex-specific specialization of polo duplicates and transcripts may be related to repeated intragenomic conflicts involving segregation distorters that differentially affect spermatogenesis and oogenesis.