Analysis of the Drosophila melanogaster testes transcriptome reveals coordinate regulation of paralogous genes

Gene duplications have been broadly implicated in the generation of testis-specific genes. To perform a comprehensive analysis of paralogous testis-biased genes, we characterized the testes transcriptome of Drosophila melanogaster by comparing gene expression in testes vs. ovaries, heads, and gonadectomized males. A number of the identified 399 testis-biased genes code for the known components of mature sperm. Among the detected 69 genes downregulated in testes, a large fraction is required for viability. By analyzing paralogs of testis-biased genes, we identified "co-regulated" paralogous pairs in which both genes are testis biased, "anti-regulated" pairs in which one paralog is testis biased and the other downregulated in testes, and "neutral" pairs in which one paralog is testis biased and the other constitutively expressed. The numbers of identified co-regulated and anti-regulated pairs were higher than expected by chance. Testis-biased genes included in these pairs show decreased frequency of lethal mutations, suggesting their specific role in male reproduction. These genes also show exceptionally high interspecific variability of expression in comparison between D. melanogaster and the closely related D. simulans. Further, interspecific changes in testis bias of expression are generally correlated within the co-regulated pairs and are anti-correlated within the anti-regulated pairs, suggesting coordinated regulation within both types of paralogous gene pairs.