title: Functional divergence of the miRNA transcriptome at the onset of Drosophila metamorphosis.
abstract: MicroRNAs (miRNAs) are endogenous RNA molecules that regulate gene expression posttranscriptionally. To date, the emergence of miRNAs and their patterns of sequence evolution have been analyzed in great detail. However, the extent to which miRNA expression levels have evolved over time, the role different evolutionary forces play in shaping these changes, and whether this variation in miRNA expression can reveal the interplay between miRNAs and mRNAs remain poorly understood. This is especially true for miRNA expressed during key developmental transitions. Here, we assayed miRNA expression levels immediately before (≥18BPF [18 h before puparium formation]) and after (PF) the increase in the hormone ecdysone responsible for triggering metamorphosis. We did so in four strains of Drosophila melanogaster and two closely related species. In contrast to their sequence conservation, approximately 25% of miRNAs analyzed showed significant within-species variation in male expression levels at ≥18BPF and/or PF. Additionally, approximately 33% showed modifications in their pattern of expression bias between developmental timepoints. A separate analysis of the ≥18BPF and PF stages revealed that changes in miRNA abundance accumulate linearly over evolutionary time at PF but not at ≥18BPF. Importantly, ≥18BPF-enriched miRNAs showed the greatest variation in expression levels both within and between species, so are the less likely to evolve under stabilizing selection. Functional attributes, such as expression ubiquity, appeared more tightly associated with lower levels of miRNA expression polymorphism at PF than at ≥18BPF. Furthermore, ≥18BPF- and PF-enriched miRNAs showed opposite patterns of covariation in expression with mRNAs, which denoted the type of regulatory relationship between miRNAs and mRNAs. Collectively, our results show contrasting patterns of functional divergence associated with miRNA expression levels during Drosophila ontogeny.
authors.affiliation: Department of Ecology and Evolutionary Biology, University of California, Irvine.
authors.forename: Shu-Dan
authors.initials: SD
authors.lastname: Yeh
authors.affiliation: Department of Ecology and Evolutionary Biology, University of California, Irvine jranz@uci.edu.
authors.forename: Marcin
authors.initials: M
authors.lastname: von Grotthuss
authors.affiliation: Department of Ecology and Evolutionary Biology, University of California, Irvine.
authors.forename: Kania A
authors.initials: KA
authors.lastname: Gandasetiawan
authors.affiliation: Department of Ecology and Evolutionary Biology, University of California, Irvine.
authors.forename: Suvini
authors.initials: S
authors.lastname: Jayasekera
authors.affiliation: Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan, China.
authors.forename: Xiao-Qin
authors.initials: XQ
authors.lastname: Xia
authors.affiliation: Department of Ecology and Evolutionary Biology, University of California, Irvine.
authors.forename: Carolus
authors.initials: C
authors.lastname: Chan
authors.affiliation: School of Mathematics and Statistics, The University of Sydney, Sydney, NSW, Australia.
authors.forename: Vivek
authors.initials: V
authors.lastname: Jayaswal
authors.affiliation: Department of Ecology and Evolutionary Biology, University of California, Irvine jranz@uci.edu.
authors.forename: José M
authors.initials: JM
authors.lastname: Ranz
mesh_terms: D000818:Animals; D017124:Conserved Sequence; D004331:Drosophila melanogaster / Q000145:classification / Q000235:genetics / Q000254:growth & development*; D019143:Evolution, Molecular; D005260:Female; D020869:Gene Expression Profiling; D018507:Gene Expression Regulation, Developmental; D014644:Genetic Variation; D008297:Male; D008675:Metamorphosis, Biological; D035683:MicroRNAs / Q000235:genetics*; D008969:Molecular Sequence Data; D010802:Phylogeny; D012727:Sex Characteristics
chemical_list: D035683:MicroRNAs
keywords: Drosophila; evolution of expression profiles; metamorphosis; miRNAs; miRNA–mRNA associations