Enrichment of mRNA-like Noncoding RNAs in the Divergence of Drosophila Males

With the advent of transcriptome data, it has become clear that mRNA-like noncoding RNAs (mlncRNAs) are widespread in eukaryotes. Although their functions are poorly understood, these transcripts may play an important role in development and could thus be involved in determining developmental complexity and phenotypic diversification. However, few studies have assessed their potential roles in the divergence of closely related species. Here, we identify and study patterns of sequence and expression divergence in ten novel candidate mlncRNAs from Drosophila pseudoobscura and its close relative D. persimilis. The candidate mlncRNAs were identified by randomly sequencing a group of 734 cDNA clones from a microarray that showed either no difference in expression (187 clones) or differential expression (547 clones) in comparisons between D. pseudoobscura and D. persimilis and between these two species and their F-1 hybrids. Candidate mlncRNAs are overrepresented among differentially expressed transcripts between males of D. pseudoobscura and D. persimilis, and although they have high sequence conservation between these two species, seven of them have no putative homologs in any of the other ten Drosophila species whose genomes have been sequenced. Expression of eight of the ten candidate mlncRNAs was detected either in whole bodies (adults) or testes using a custom-designed oligonucleotide microarray. Three of the ten candidate mlncRNAs are highly expressed (in the top 4% of the male transcriptome), differentially expressed between species, and show extreme levels of sex-bias, with one transcript having the highest level of male bias in the whole transcriptome. Proteomic data from testes show no traces of any predicted peptides from the candidate mlncRNAs. Our results suggest that these mlncRNAs may be important in male-specific processes related to sexual dimorphism and species divergence in this species group.