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A novel method for quantifying the rate of embryogenesis uncovers considerable genetic variation for the duration of embryonic development in Drosophila melanogaster
BACKGROUND: Embryogenesis is a highly conserved, canalized process, and variation in the duration of embryogenesis (DOE), i.e., time from egg lay to hatching, has a potentially profound effect on the outcome of within- and between-species competition. There is both intra- and inter-specific variatio...
Autores principales: | , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
BioMed Central
2016
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5054588/ https://www.ncbi.nlm.nih.gov/pubmed/27717305 http://dx.doi.org/10.1186/s12862-016-0776-z |
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author | Horváth, Barbara Betancourt, Andrea J. Kalinka, Alex T. |
author_facet | Horváth, Barbara Betancourt, Andrea J. Kalinka, Alex T. |
author_sort | Horváth, Barbara |
collection | PubMed |
description | BACKGROUND: Embryogenesis is a highly conserved, canalized process, and variation in the duration of embryogenesis (DOE), i.e., time from egg lay to hatching, has a potentially profound effect on the outcome of within- and between-species competition. There is both intra- and inter-specific variation in this trait, which may provide important fuel for evolutionary processes, particularly adaptation. However, while genetic variation underlying simpler morphological traits, or with large phenotypic effects is well described in the literature, less is known about the underlying genetics of traits, such as DOE, partly due to a lack of tools with which to study them. RESULTS: Here, we establish a novel microscope-based assay to survey genetic variation for the duration of embryogenesis (DOE). First, to establish the potential importance of DOE in competitive fitness, we performed a set of experiments where we experimentally manipulated the time until hatching, and show that short hatching times result in priority effect in the form of improved larval competitive ability. We then use our assay to measure DOE for 43 strains from the Drosophila Genetic Reference Panel (DGRP). Our assay greatly simplifies the measurement of DOE, making it possible to precisely quantify this trait for 59,295 individual embryos (mean ± S.D. of 1103 ± 293 per DGRP strain, and 1002 ± 203 per control). We find extensive genetic variation in DOE, with a 15 % difference in rate between the slowest and fastest strains measured, and 89 % of phenotypic variation due to DGRP strain. Using sequence information from the DGRP, we perform a genome-wide association study, which suggests that some well-known developmental genes affect the speed of embryonic development. CONCLUSIONS: We showed that the duration of embryogenesis (DOE) can be efficiently and precisely measured in Drosophila, and that the DGRP strains show remarkable variation in DOE. A genome-wide analysis suggests that some well-known developmental genes are potentially associated with DOE. Further functional assays, or transcriptomic analysis of embryos from the DGRP, can validate the role of our candidates in early developmental processes. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12862-016-0776-z) contains supplementary material, which is available to authorized users. |
format | Online Article Text |
id | pubmed-5054588 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2016 |
publisher | BioMed Central |
record_format | MEDLINE/PubMed |
spelling | pubmed-50545882016-10-19 A novel method for quantifying the rate of embryogenesis uncovers considerable genetic variation for the duration of embryonic development in Drosophila melanogaster Horváth, Barbara Betancourt, Andrea J. Kalinka, Alex T. BMC Evol Biol Research Article BACKGROUND: Embryogenesis is a highly conserved, canalized process, and variation in the duration of embryogenesis (DOE), i.e., time from egg lay to hatching, has a potentially profound effect on the outcome of within- and between-species competition. There is both intra- and inter-specific variation in this trait, which may provide important fuel for evolutionary processes, particularly adaptation. However, while genetic variation underlying simpler morphological traits, or with large phenotypic effects is well described in the literature, less is known about the underlying genetics of traits, such as DOE, partly due to a lack of tools with which to study them. RESULTS: Here, we establish a novel microscope-based assay to survey genetic variation for the duration of embryogenesis (DOE). First, to establish the potential importance of DOE in competitive fitness, we performed a set of experiments where we experimentally manipulated the time until hatching, and show that short hatching times result in priority effect in the form of improved larval competitive ability. We then use our assay to measure DOE for 43 strains from the Drosophila Genetic Reference Panel (DGRP). Our assay greatly simplifies the measurement of DOE, making it possible to precisely quantify this trait for 59,295 individual embryos (mean ± S.D. of 1103 ± 293 per DGRP strain, and 1002 ± 203 per control). We find extensive genetic variation in DOE, with a 15 % difference in rate between the slowest and fastest strains measured, and 89 % of phenotypic variation due to DGRP strain. Using sequence information from the DGRP, we perform a genome-wide association study, which suggests that some well-known developmental genes affect the speed of embryonic development. CONCLUSIONS: We showed that the duration of embryogenesis (DOE) can be efficiently and precisely measured in Drosophila, and that the DGRP strains show remarkable variation in DOE. A genome-wide analysis suggests that some well-known developmental genes are potentially associated with DOE. Further functional assays, or transcriptomic analysis of embryos from the DGRP, can validate the role of our candidates in early developmental processes. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12862-016-0776-z) contains supplementary material, which is available to authorized users. BioMed Central 2016-10-07 /pmc/articles/PMC5054588/ /pubmed/27717305 http://dx.doi.org/10.1186/s12862-016-0776-z Text en © The Author(s). 2016 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. |
spellingShingle | Research Article Horváth, Barbara Betancourt, Andrea J. Kalinka, Alex T. A novel method for quantifying the rate of embryogenesis uncovers considerable genetic variation for the duration of embryonic development in Drosophila melanogaster |
title | A novel method for quantifying the rate of embryogenesis uncovers considerable genetic variation for the duration of embryonic development in Drosophila melanogaster |
title_full | A novel method for quantifying the rate of embryogenesis uncovers considerable genetic variation for the duration of embryonic development in Drosophila melanogaster |
title_fullStr | A novel method for quantifying the rate of embryogenesis uncovers considerable genetic variation for the duration of embryonic development in Drosophila melanogaster |
title_full_unstemmed | A novel method for quantifying the rate of embryogenesis uncovers considerable genetic variation for the duration of embryonic development in Drosophila melanogaster |
title_short | A novel method for quantifying the rate of embryogenesis uncovers considerable genetic variation for the duration of embryonic development in Drosophila melanogaster |
title_sort | novel method for quantifying the rate of embryogenesis uncovers considerable genetic variation for the duration of embryonic development in drosophila melanogaster |
topic | Research Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5054588/ https://www.ncbi.nlm.nih.gov/pubmed/27717305 http://dx.doi.org/10.1186/s12862-016-0776-z |
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