Drosophila embryogenesis scales uniformly across temperature in developmentally diverse species

TL;DR

This study shows that Drosophila embryogenesis duration varies with temperature but maintains a consistent relative timing of developmental events across multiple species, indicating a conserved developmental timer.

Contribution

It demonstrates that despite differences in total development time, the relative timing of embryonic events remains constant across temperatures and species, revealing a conserved developmental timing mechanism.

Findings

Embryogenesis duration varies twofold with temperature.

Relative timing of developmental events is conserved across temperatures.

Different Drosophila species exhibit similar relative developmental timing despite varied total durations.

Abstract

Temperature affects both the timing and outcome of animal development, but the detailed effects of temperature on the progress of early development have been poorly characterized. To determine the impact of temperature on the order and timing of events during Drosophila melanogaster embryogenesis, we used time-lapse imaging to track the progress of embryos from shortly after egg laying through hatching at seven precisely maintained temperatures between 17.5C and 32.5C. We employed a combination of automated and manual annotation to determine when 36 milestones occurred in each embryo. D. melanogaster embryogenesis takes ~33 hours at 17.5C, and accelerates with increasing temperature to 16 hours at 27.5C, above which embryogenesis slows slightly. Remarkably, while the total time of embryogenesis varies over two fold, the relative timing of events from cellularization through hatching is constant across temperatures. To further explore the relationship between temperature and embryogenesis, we expanded our analysis to cover ten additional Drosophila species of varying climatic origins. Six of these species, like D. melanogaster, are of tropical origin, and embryogenesis time at different temperatures was similar for them all. D. mojavensis, a sub-tropical fly, develops slower than the tropical species at lower temperatures, while D. virilis, a temperate fly, exhibits slower development at all temperatures. The alpine sister species D. persimilis and D. pseudoobscura develop as rapidly as tropical flies at cooler temperatures, but exhibit diminished acceleration above 22.5C and have drastically slowed development by 30C. Despite ranging from 13 hours for D. erecta at 30C to 46 hours for D. virilis at 17.5C, the relative timing of events from cellularization through hatching is constant across all species and temperatures, suggesting the existence of a timer controlling embryogenesis.