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Stagewise resolution of temperature-dependent embryonic and postembryonic development in the cowpea seed beetle Callosobruchus maculatus (F.)

BACKGROUND: The thermal plasticity of life-history traits receives wide attention in the recent biological literature. Of all the temperature-dependent traits studied, developmental rates of ectotherms are especially often addressed, and yet surprisingly little is known about embryonic responses to...

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Autor principal: Kutcherov, Dmitry
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7488527/
https://www.ncbi.nlm.nih.gov/pubmed/32917176
http://dx.doi.org/10.1186/s12898-020-00318-2
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author Kutcherov, Dmitry
author_facet Kutcherov, Dmitry
author_sort Kutcherov, Dmitry
collection PubMed
description BACKGROUND: The thermal plasticity of life-history traits receives wide attention in the recent biological literature. Of all the temperature-dependent traits studied, developmental rates of ectotherms are especially often addressed, and yet surprisingly little is known about embryonic responses to temperature, including changes in the thermal thresholds and thermal sensitivity during early development. Even postembryonic development of many cryptically living species is understood superficially at best. RESULTS: This study is the first to estimate the exact durations of developmental stages in the cowpea seed beetle C. maculatus from oviposition to adult emergence at five permissive constant temperatures from 20 to 32 °C. Early embryonic development was tracked and documented by means of destructive sampling and subsequent confocal imaging of fluorescently stained specimens. Late embryonic and early larval development was studied with the use of destructive sampling and light microscopy. Well-resolved temporal series based on thousands of embryos allowed precise timing of the following developmental events: formation of the blastoderm; formation, elongation, and retraction of the germ band; dorsal closure; the onset and completion of sclerotization of the cuticle; hatching, and penetration of the first-instar larva into the cowpea seed. Pupation and adult eclosion were observed directly through an incision in the seed coat. The thermal phenotype of C. maculatus was found to vary in the course of ontogeny and different stages scaled disproportionately with temperature, but pitfalls and caveats associated with analyses of relative durations of individual stages are also briefly discussed. CONCLUSION: Disproportionate changes in developmental durations with temperature may have important implications when study design requires a high degree of synchronization among experimental embryos or when the occurrence of particular stages in the field is of interest, as well as in any other cases when development times need to be estimated with precision. This work provides one of the first examples of integration of embryological techniques with ecophysiological concepts and will hopefully motivate similar projects in the future. While experiments with Drosophila continue to be the main source of information on animal development, knowledge on other model species is instrumental to building a broader picture of developmental phenomena.
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spelling pubmed-74885272020-09-16 Stagewise resolution of temperature-dependent embryonic and postembryonic development in the cowpea seed beetle Callosobruchus maculatus (F.) Kutcherov, Dmitry BMC Ecol Research Article BACKGROUND: The thermal plasticity of life-history traits receives wide attention in the recent biological literature. Of all the temperature-dependent traits studied, developmental rates of ectotherms are especially often addressed, and yet surprisingly little is known about embryonic responses to temperature, including changes in the thermal thresholds and thermal sensitivity during early development. Even postembryonic development of many cryptically living species is understood superficially at best. RESULTS: This study is the first to estimate the exact durations of developmental stages in the cowpea seed beetle C. maculatus from oviposition to adult emergence at five permissive constant temperatures from 20 to 32 °C. Early embryonic development was tracked and documented by means of destructive sampling and subsequent confocal imaging of fluorescently stained specimens. Late embryonic and early larval development was studied with the use of destructive sampling and light microscopy. Well-resolved temporal series based on thousands of embryos allowed precise timing of the following developmental events: formation of the blastoderm; formation, elongation, and retraction of the germ band; dorsal closure; the onset and completion of sclerotization of the cuticle; hatching, and penetration of the first-instar larva into the cowpea seed. Pupation and adult eclosion were observed directly through an incision in the seed coat. The thermal phenotype of C. maculatus was found to vary in the course of ontogeny and different stages scaled disproportionately with temperature, but pitfalls and caveats associated with analyses of relative durations of individual stages are also briefly discussed. CONCLUSION: Disproportionate changes in developmental durations with temperature may have important implications when study design requires a high degree of synchronization among experimental embryos or when the occurrence of particular stages in the field is of interest, as well as in any other cases when development times need to be estimated with precision. This work provides one of the first examples of integration of embryological techniques with ecophysiological concepts and will hopefully motivate similar projects in the future. While experiments with Drosophila continue to be the main source of information on animal development, knowledge on other model species is instrumental to building a broader picture of developmental phenomena. BioMed Central 2020-09-11 /pmc/articles/PMC7488527/ /pubmed/32917176 http://dx.doi.org/10.1186/s12898-020-00318-2 Text en © The Author(s) 2020 Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. 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 in a credit line to the data.
spellingShingle Research Article
Kutcherov, Dmitry
Stagewise resolution of temperature-dependent embryonic and postembryonic development in the cowpea seed beetle Callosobruchus maculatus (F.)
title Stagewise resolution of temperature-dependent embryonic and postembryonic development in the cowpea seed beetle Callosobruchus maculatus (F.)
title_full Stagewise resolution of temperature-dependent embryonic and postembryonic development in the cowpea seed beetle Callosobruchus maculatus (F.)
title_fullStr Stagewise resolution of temperature-dependent embryonic and postembryonic development in the cowpea seed beetle Callosobruchus maculatus (F.)
title_full_unstemmed Stagewise resolution of temperature-dependent embryonic and postembryonic development in the cowpea seed beetle Callosobruchus maculatus (F.)
title_short Stagewise resolution of temperature-dependent embryonic and postembryonic development in the cowpea seed beetle Callosobruchus maculatus (F.)
title_sort stagewise resolution of temperature-dependent embryonic and postembryonic development in the cowpea seed beetle callosobruchus maculatus (f.)
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7488527/
https://www.ncbi.nlm.nih.gov/pubmed/32917176
http://dx.doi.org/10.1186/s12898-020-00318-2
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