Temporal dynamics of gene expression during metamorphosis in two distant Drosophila species

Abstract Complete metamorphosis of holometabolous insects is a complex biological process characterized by profound morphological, physiological, and transcriptional changes. To reveal the temporal dynamics of gene expression during this critical developmental transition, we conducted a detailed analysis of the developmental transcriptomes of two Drosophila species,Drosophila melanogasterandDrosophila virilis. We confirmed partial recapitulation of the embryonic transcriptional program in pupae, but unlike the traditional hourglass model, suggesting maximal conservation at mid-embryonic stages, at different stages of pupae we observed a more complicated pattern of alternating low and high diversity, resembling an inverted hourglass, or “spindle”. This underscores the complexity of developmental processes during complete metamorphosis. Notably, recently formed genes (specific to insects) exhibit pronounced expression peaks during mid-pupal development, indicating their potential role in developmental transitions. Significance Statement This study describes the transcriptomic dynamics of complete metamorphosis in holometabolous insects. By analyzing developmental transcriptomes ofDrosophila melanogasterandDrosophila virilis, we characterize the spindle pattern of gene expression during pupal stages, contrasting with the classical hourglass model of embryogenesis. This alternating pattern of low and high transcriptional diversity highlights the unique complexity of the metamorphose processes.