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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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 [Formula: 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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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. 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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 credited: Kuntz SG, Eisen MB (2014) Drosophila Embryogenesis Scales Uniformly across Temperature in Developmentally Diverse Species. 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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 [Formula: 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.</description><subject>Animals</subject><subject>Biology and Life Sciences</subject><subject>Cold Temperature</subject><subject>Drosophila</subject><subject>Drosophila melanogaster - genetics</subject><subject>Ecology and Environmental Sciences</subject><subject>Embryonic development</subject><subject>Embryonic Development - genetics</subject><subject>Experiments</subject><subject>Gene expression</subject><subject>Genetic aspects</subject><subject>Genetic research</subject><subject>Genetic Variation - genetics</subject><subject>Heat</subject><subject>Insects</subject><subject>Phylogeny</subject><subject>Research and Analysis Methods</subject><subject>Selection, Genetic - genetics</subject><subject>Species Specificity</subject><subject>Temperature</subject><subject>Time-Lapse Imaging - methods</subject><subject>Transcription factors</subject><subject>Trends</subject><subject>Zoological research</subject><issn>1553-7404</issn><issn>1553-7390</issn><issn>1553-7404</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2014</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>DOA</sourceid><recordid>eNqVk0tr3DAQx01padK036C0hkJpD7vVy7J1KYSkj4XQQF9XIcujXS2y5Uj2kv321WY3YQ09tOggMfrNf2Y0mix7idEc0xJ_WPsxdMrN-yV0c4wQI4I-yk5xUdBZyRB7fHQ-yZ7FuEaIFpUon2YnhJWccFKdZvIy-Oj7lXUqh7YOW5_kINqYR60cxHzsrPGhddtc6YTGfIC2h6CGMUBuu7yBDTjft9ANyiWqsRsIEfLYg7YQn2dPjHIRXhz2s-zX508_L77Orq6_LC7Or2aai2qYQc0IUbSoFTUmlcK50BXlQBEnpSBQAyaNEZgjzqCulEK40oYWDTbAm6qiZ9nrvW7vfJSHt4kSF6SgiJYcJ2KxJxqv1rIPtlVhK72y8s7gw1KqMFjtQCpjWIoGVBvMmOIVIVRjXhYaC8M0SlofD9HGuoVGp-KDchPR6U1nV3LpN5IKUQlcJIF3B4Hgb0aIg2xt1OCc6sCPu7yxIJwW5S7Wmz26TP2QtjM-KeodLs9pSq1ihIpEzf9CpdVAa7XvwNhknzi8nzgkZoDbYanGGOXix_f_YL_9O3v9e8q-PWJXoNywit6Ng_VdnIJsD959wQDm4akxkrtpuO-43E2DPExDcnt13KYHp_vvT_8AqRsGtg</recordid><startdate>20140401</startdate><enddate>20140401</enddate><creator>Kuntz, Steven G</creator><creator>Eisen, Michael B</creator><general>Public Library of Science</general><general>Public Library of Science (PLoS)</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>IOV</scope><scope>ISN</scope><scope>ISR</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope></search><sort><creationdate>20140401</creationdate><title>Drosophila embryogenesis scales uniformly across temperature in developmentally diverse species</title><author>Kuntz, Steven G ; Eisen, Michael B</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c698t-eb422a35ba3ff042669c836e3062792ebe12df916064eb8aa018cf35d1fe6d883</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2014</creationdate><topic>Animals</topic><topic>Biology and Life Sciences</topic><topic>Cold Temperature</topic><topic>Drosophila</topic><topic>Drosophila melanogaster - genetics</topic><topic>Ecology and Environmental Sciences</topic><topic>Embryonic development</topic><topic>Embryonic Development - genetics</topic><topic>Experiments</topic><topic>Gene expression</topic><topic>Genetic aspects</topic><topic>Genetic research</topic><topic>Genetic Variation - genetics</topic><topic>Heat</topic><topic>Insects</topic><topic>Phylogeny</topic><topic>Research and Analysis Methods</topic><topic>Selection, Genetic - genetics</topic><topic>Species Specificity</topic><topic>Temperature</topic><topic>Time-Lapse Imaging - methods</topic><topic>Transcription factors</topic><topic>Trends</topic><topic>Zoological research</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Kuntz, Steven G</creatorcontrib><creatorcontrib>Eisen, Michael B</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Gale In Context: Opposing Viewpoints</collection><collection>Gale In Context: Canada</collection><collection>Gale In Context: Science</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PLoS genetics</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Kuntz, Steven G</au><au>Eisen, Michael B</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Drosophila embryogenesis scales uniformly across temperature in developmentally diverse species</atitle><jtitle>PLoS genetics</jtitle><addtitle>PLoS Genet</addtitle><date>2014-04-01</date><risdate>2014</risdate><volume>10</volume><issue>4</issue><spage>e1004293</spage><epage>e1004293</epage><pages>e1004293-e1004293</pages><issn>1553-7404</issn><issn>1553-7390</issn><eissn>1553-7404</eissn><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 17.5 °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 [Formula: 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.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>24762628</pmid><doi>10.1371/journal.pgen.1004293</doi><oa>free_for_read</oa></addata></record> |
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subjects | Animals Biology and Life Sciences Cold Temperature Drosophila Drosophila melanogaster - genetics Ecology and Environmental Sciences Embryonic development Embryonic Development - genetics Experiments Gene expression Genetic aspects Genetic research Genetic Variation - genetics Heat Insects Phylogeny Research and Analysis Methods Selection, Genetic - genetics Species Specificity Temperature Time-Lapse Imaging - methods Transcription factors Trends Zoological research |
title | Drosophila embryogenesis scales uniformly across temperature in developmentally diverse species |
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