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Drosophila Embryogenesis Scales Uniformly across Temperature in Developmentally Diverse Species

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, w...

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Autores principales: Kuntz, Steven G., Eisen, Michael B.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2014
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3998915/
https://www.ncbi.nlm.nih.gov/pubmed/24762628
http://dx.doi.org/10.1371/journal.pgen.1004293
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author Kuntz, Steven G.
Eisen, Michael B.
author_facet Kuntz, Steven G.
Eisen, Michael B.
author_sort Kuntz, Steven G.
collection PubMed
description 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 17.5°C and 32.5°C. We employed a combination of automated and manual annotation to determine when 36 milestones occurred in each embryo. D. melanogaster embryogenesis takes [Image: see text]33 hours at 17.5°C, and accelerates with increasing temperature to a low of 16 hours at 27.5°C, 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 22.5°C and have drastically slowed development by 30°C. Despite ranging from 13 hours for D. erecta at 30°C to 46 hours for D. virilis at 17.5°C, the relative timing of events from cellularization through hatching is constant across all species and temperatures examined here, suggesting the existence of a previously unrecognized timer controlling the progress of embryogenesis that has been tuned by natural selection as each species diverges.
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spelling pubmed-39989152014-04-29 Drosophila Embryogenesis Scales Uniformly across Temperature in Developmentally Diverse Species Kuntz, Steven G. Eisen, Michael B. PLoS Genet Research Article 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 17.5°C and 32.5°C. We employed a combination of automated and manual annotation to determine when 36 milestones occurred in each embryo. D. melanogaster embryogenesis takes [Image: see text]33 hours at 17.5°C, and accelerates with increasing temperature to a low of 16 hours at 27.5°C, 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 22.5°C and have drastically slowed development by 30°C. Despite ranging from 13 hours for D. erecta at 30°C to 46 hours for D. virilis at 17.5°C, the relative timing of events from cellularization through hatching is constant across all species and temperatures examined here, suggesting the existence of a previously unrecognized timer controlling the progress of embryogenesis that has been tuned by natural selection as each species diverges. Public Library of Science 2014-04-24 /pmc/articles/PMC3998915/ /pubmed/24762628 http://dx.doi.org/10.1371/journal.pgen.1004293 Text en © 2014 Kuntz, Eisen http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited.
spellingShingle Research Article
Kuntz, Steven G.
Eisen, Michael B.
Drosophila Embryogenesis Scales Uniformly across Temperature in Developmentally Diverse Species
title Drosophila Embryogenesis Scales Uniformly across Temperature in Developmentally Diverse Species
title_full Drosophila Embryogenesis Scales Uniformly across Temperature in Developmentally Diverse Species
title_fullStr Drosophila Embryogenesis Scales Uniformly across Temperature in Developmentally Diverse Species
title_full_unstemmed Drosophila Embryogenesis Scales Uniformly across Temperature in Developmentally Diverse Species
title_short Drosophila Embryogenesis Scales Uniformly across Temperature in Developmentally Diverse Species
title_sort drosophila embryogenesis scales uniformly across temperature in developmentally diverse species
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3998915/
https://www.ncbi.nlm.nih.gov/pubmed/24762628
http://dx.doi.org/10.1371/journal.pgen.1004293
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