Natural variation in the maternal and zygotic mRNA complements of the early embryo in Drosophila melanogaster.

Background: Maternal gene products supplied to the egg during oogenesis drive the earliest events of development in all metazoans. After the initial stages of embryogenesis, maternal transcripts are degraded as zygotic transcription is activated; this is known as the maternal to zygotic transition (MZT). Recently, it has been shown that the expression of maternal and zygotic transcripts have evolved in the Drosophila genus over the course of 50 million years.

The early embryonic transcriptome of a Hawaiian Drosophila picture-wing fly shows evidence of altered gene expression and novel gene evolution.

A massive adaptive radiation on the Hawaiian archipelago has produced approximately one-quarter of the fly species in the family Drosophilidae. The Hawaiian Drosophila clade has long been recognized as a model system for the study of both the ecology of island endemics and the evolution of developmental mechanisms, but relatively few genomic and transcriptomic datasets are available for this group. We present here a differential expression analysis of the transcriptional profiles of two highly conserved embryonic stages in the Hawaiian picture-wing fly Drosophila grimshawi.

Evolved Differences in and Regulation Between the Maternal and Zygotic mRNA Complements in the Embryo.

How gene expression can evolve depends on the mechanisms driving gene expression. Gene expression is controlled in different ways in different developmental stages; here we ask whether different developmental stages show different patterns of regulatory evolution. To explore the mode of regulatory evolution, we used the early stages of embryonic development controlled by two different genomes, that of the mother and that of the zygote.

The conserved regulatory basis of mRNA contributions to the early Drosophila embryo differs between the maternal and zygotic genomes.

The gene products that drive early development are critical for setting up developmental trajectories in all animals. The earliest stages of development are fueled by maternally provided mRNAs until the zygote can take over transcription of its own genome. In early development, both maternally deposited and zygotically transcribed gene products have been well characterized in model systems.

Evolution of larval segment position across 12 Drosophila species.

Many developmental traits that are critical to the survival of the organism are also robust. These robust traits are resistant to phenotypic change in the face of variation. This presents a challenge to evolution.

Evolution of maternal and zygotic mRNA complements in the early Drosophila embryo.

The earliest stages of animal development are controlled by maternally deposited mRNA transcripts and proteins. Once the zygote is able to transcribe its own genome, maternal transcripts are degraded, in a tightly regulated process known as the maternal to zygotic transition (MZT). While this process has been well-studied within model species, we have little knowledge of how the pools of maternal and zygotic transcripts evolve.

Effect of Larval Nutrition on Maternal mRNA Contribution to the Egg.

Embryonic development begins under the control of maternal gene products, mRNAs and proteins that the mother deposits into the egg; the zygotic genome is activated some time later. Maternal control of early development is conserved across metazoans. Gene products contributed by mothers are critical to many early developmental processes, and set up trajectories for the rest of development.

Sex Bias and Maternal Contribution to Gene Expression Divergence in Drosophila Blastoderm Embryos.

Early embryogenesis is a unique developmental stage where genetic control of development is handed off from mother to zygote. Yet the contribution of this transition to the evolution of gene expression is poorly understood. Here we study two aspects of gene expression specific to early embryogenesis in Drosophila: sex-biased gene expression prior to the onset of canonical X chromosomal dosage compensation, and the contribution of maternally supplied mRNAs.

Sex-specific embryonic gene expression in species with newly evolved sex chromosomes.

Sex chromosome dosage differences between females and males are a significant form of natural genetic variation in many species. Like many species with chromosomal sex determination, Drosophila females have two X chromosomes, while males have one X and one Y. Fusions of sex chromosomes with autosomes have occurred along the lineage leading to D.

Extensive divergence of transcription factor binding in Drosophila embryos with highly conserved gene expression.

To better characterize how variation in regulatory sequences drives divergence in gene expression, we undertook a systematic study of transcription factor binding and gene expression in blastoderm embryos of four species, which sample much of the diversity in the 40 million-year old genus Drosophila: D. melanogaster, D. yakuba, D.

An essential role for zygotic expression in the pre-cellular Drosophila embryo.

The Drosophila embryo proceeds through thirteen mitotic divisions as a syncytium. Its nuclei distribute in the embryo's interior during the first six divisions, dividing synchronously with a cycle time of less than ten minutes. After seven divisions (nuclear cycle 8), the syncytial blastoderm forms as the nuclei approach the embryo surface and slow their cycle time; subsequent divisions proceed in waves that initiate at the poles.

Noncanonical compensation of zygotic X transcription in early Drosophila melanogaster development revealed through single-embryo RNA-seq.

When Drosophila melanogaster embryos initiate zygotic transcription around mitotic cycle 10, the dose-sensitive expression of specialized genes on the X chromosome triggers a sex-determination cascade that, among other things, compensates for differences in sex chromosome dose by hypertranscribing the single X chromosome in males. However, there is an approximately 1 hour delay between the onset of zygotic transcription and the establishment of canonical dosage compensation near the end of mitotic cycle 14. During this time, zygotic transcription drives segmentation, cellularization, and other important developmental events.

Evolution and inheritance of early embryonic patterning in Drosophila simulans and D. sechellia.

Pattern formation in Drosophila is a widely studied example of a robust developmental system. Such robust systems pose a challenge to adaptive evolution, as they mask variation that selection may otherwise act upon. Yet we find variation in the localization of expression domains (henceforth "stripe allometry") in the pattern formation pathway.

Artificial selection on egg size perturbs early pattern formation in Drosophila melanogaster.

Pattern formation in Drosophila embryogenesis has been widely investigated as a developmental and evolutionary model of robustness. To ask whether genetic variation for pattern formation is suppressed in this system, artificial selection for divergent egg size was used to challenge the scaling of even-skipped (eve) pattern formation in mitotic cycle 14 (stage 5) embryos of Drosophila melanogaster. Three-dimensional confocal imaging revealed shifts in the allometry of eve pair-rule stripes along both anterior–posterior (A–P) and dorsoventral (D–V) axes as a correlated response to egg size selection, indicating the availability of genetic variation for this buffered trait.

Canalization of segmentation and its evolution in Drosophila.

Segmentation in Drosophila embryogenesis occurs through a hierarchical cascade of regulatory gene expression driven by the establishment of a diffusion-mediated morphogen gradient. Here, we investigate the response of this pattern formation process to genetic variation and evolution in egg size. Specifically, we ask whether spatial localization of gap genes Kruppel (Kr) and giant (gt) and the pair-rule gene even-skipped (eve) during cellularization is robust to genetic variation in embryo length in three Drosophila melanogaster isolines and two closely related species.