GSE136646
Evolved differences in cis and trans regulation between the maternal and zygotic mRNA complements in the Drosophila embryo
During embryogenesis in animals, initial developmental processes are driven entirely by maternally provided gene products that are deposited into the oocyte. The zygotic genome is transcriptionally activated later, when developmental control is handed off from maternal gene products to the zygote during the maternal to zygotic transition (MZT). The MZT is highly regulated and conserved across all animals, and while some details change across model systems where it has been studied, most are too evolutionarily diverged to make comparisons as to how this process evolves. There are differences in maternal gene products and their zygotic complements across Drosophila species, so here we used hybrid crosses between sister species of Drosophila (D. simulans, D. sechellia, and D. mauritiana) and transcriptomics to determine how gene regulation changes in early embryogenesis across species. We find that regulation of maternal transcript deposition and zygotic transcription evolve through different mechanisms. Changes in transcript levels occur predominantly through differences in trans regulation for maternal genes, while changes in zygotic transcription occur through a combination of regulatory changes in cis, trans, and both cis and trans. We find that patterns of transcript level inheritance in hybrids relative to parental species differs between maternal and zygotic transcripts; maternal transcript levels are more likely to be conserved but both stages have a large proportion of transcripts showing dominance of one parental species. Differences in the underlying regulatory landscape in the mother and the zygote are likely the primary determinants for how maternal and zygotic transcripts evolve species. Overall design: Crosses between D. simulans, D. sechellia, and D. mauritiana, reciprocally where possible, were performed, for 5 total crosses. Embryos were collected from two developmental stages, stage 2 where all transcripts present are maternal in origin, and late stage 5, after zygotic genome activation. Stage 2 embryos were collected from F1 hybrid mothers, late stage 5 embryos were F1 hybrids themselves (collected from a between-species cross). mRNA-Seq was performed on RNA extracted from single staged embryos, 3 replicates per cross for stage 2, and 6 replicates per cross for stage 5 (3 female and 3 male embryos), for a total of 45 hybrid embryo samples.