Multi-level analysis of reproduction in an Antarctic midge identifies female and male accessory gland products that are altered by larval stress and impact progeny viability
The Antarctic midge, Belgica antarctica, is a wingless, non-biting midge endemic to Antarctica. Larval development requires at least 2 years, but adults live only 2 weeks. The nonfeeding adults mate in swarms and females die shortly after oviposition. Eggs are suspended in a gel of unknown compositi...
Published in: | Scientific Reports |
---|---|
Main Authors: | , , , , , , , , , , , , , , , , , , |
Format: | Text |
Language: | English |
Published: |
Nature Publishing Group UK
2020
|
Subjects: | |
Online Access: | http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7666147/ http://www.ncbi.nlm.nih.gov/pubmed/33188214 https://doi.org/10.1038/s41598-020-76139-6 |
id |
ftpubmed:oai:pubmedcentral.nih.gov:7666147 |
---|---|
record_format |
openpolar |
spelling |
ftpubmed:oai:pubmedcentral.nih.gov:7666147 2023-05-15T13:44:48+02:00 Multi-level analysis of reproduction in an Antarctic midge identifies female and male accessory gland products that are altered by larval stress and impact progeny viability Finch, Geoffrey Nandyal, Sonya Perretta, Carlie Davies, Benjamin Rosendale, Andrew J. Holmes, Christopher J. Gantz, J. D. Spacht, Drew E. Bailey, Samuel T. Chen, Xiaoting Oyen, Kennan Didion, Elise M. Chakraborty, Souvik Lee, Richard E. Denlinger, David L. Matter, Stephen F. Attardo, Geoffrey M. Weirauch, Matthew T. Benoit, Joshua B. 2020-11-13 http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7666147/ http://www.ncbi.nlm.nih.gov/pubmed/33188214 https://doi.org/10.1038/s41598-020-76139-6 en eng Nature Publishing Group UK http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7666147/ http://www.ncbi.nlm.nih.gov/pubmed/33188214 http://dx.doi.org/10.1038/s41598-020-76139-6 © The Author(s) 2020 Open Access This 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/. CC-BY Sci Rep Article Text 2020 ftpubmed https://doi.org/10.1038/s41598-020-76139-6 2020-11-22T01:37:18Z The Antarctic midge, Belgica antarctica, is a wingless, non-biting midge endemic to Antarctica. Larval development requires at least 2 years, but adults live only 2 weeks. The nonfeeding adults mate in swarms and females die shortly after oviposition. Eggs are suspended in a gel of unknown composition that is expressed from the female accessory gland. This project characterizes molecular mechanisms underlying reproduction in this midge by examining differential gene expression in whole males, females, and larvae, as well as in male and female accessory glands. Functional studies were used to assess the role of the gel encasing the eggs, as well as the impact of stress on reproductive biology. RNA-seq analyses revealed sex- and development-specific gene sets along with those associated with the accessory glands. Proteomic analyses were used to define the composition of the egg-containing gel, which is generated during multiple developmental stages and derived from both the accessory gland and other female organs. Functional studies indicate the gel provides a larval food source as well as a buffer for thermal and dehydration stress. All of these function are critical to juvenile survival. Larval dehydration stress directly reduces production of storage proteins and key accessory gland components, a feature that impacts adult reproductive success. Modeling reveals that bouts of dehydration may have a significant impact on population growth. This work lays a foundation for further examination of reproduction in midges and provides new information related to general reproduction in dipterans. A key aspect of this work is that reproduction and stress dynamics, currently understudied in polar organisms, are likely to prove critical in determining how climate change will alter their survivability. Text Antarc* Antarctic Antarctic midge Antarctica Belgica antarctica PubMed Central (PMC) Antarctic The Antarctic Scientific Reports 10 1 |
institution |
Open Polar |
collection |
PubMed Central (PMC) |
op_collection_id |
ftpubmed |
language |
English |
topic |
Article |
spellingShingle |
Article Finch, Geoffrey Nandyal, Sonya Perretta, Carlie Davies, Benjamin Rosendale, Andrew J. Holmes, Christopher J. Gantz, J. D. Spacht, Drew E. Bailey, Samuel T. Chen, Xiaoting Oyen, Kennan Didion, Elise M. Chakraborty, Souvik Lee, Richard E. Denlinger, David L. Matter, Stephen F. Attardo, Geoffrey M. Weirauch, Matthew T. Benoit, Joshua B. Multi-level analysis of reproduction in an Antarctic midge identifies female and male accessory gland products that are altered by larval stress and impact progeny viability |
topic_facet |
Article |
description |
The Antarctic midge, Belgica antarctica, is a wingless, non-biting midge endemic to Antarctica. Larval development requires at least 2 years, but adults live only 2 weeks. The nonfeeding adults mate in swarms and females die shortly after oviposition. Eggs are suspended in a gel of unknown composition that is expressed from the female accessory gland. This project characterizes molecular mechanisms underlying reproduction in this midge by examining differential gene expression in whole males, females, and larvae, as well as in male and female accessory glands. Functional studies were used to assess the role of the gel encasing the eggs, as well as the impact of stress on reproductive biology. RNA-seq analyses revealed sex- and development-specific gene sets along with those associated with the accessory glands. Proteomic analyses were used to define the composition of the egg-containing gel, which is generated during multiple developmental stages and derived from both the accessory gland and other female organs. Functional studies indicate the gel provides a larval food source as well as a buffer for thermal and dehydration stress. All of these function are critical to juvenile survival. Larval dehydration stress directly reduces production of storage proteins and key accessory gland components, a feature that impacts adult reproductive success. Modeling reveals that bouts of dehydration may have a significant impact on population growth. This work lays a foundation for further examination of reproduction in midges and provides new information related to general reproduction in dipterans. A key aspect of this work is that reproduction and stress dynamics, currently understudied in polar organisms, are likely to prove critical in determining how climate change will alter their survivability. |
format |
Text |
author |
Finch, Geoffrey Nandyal, Sonya Perretta, Carlie Davies, Benjamin Rosendale, Andrew J. Holmes, Christopher J. Gantz, J. D. Spacht, Drew E. Bailey, Samuel T. Chen, Xiaoting Oyen, Kennan Didion, Elise M. Chakraborty, Souvik Lee, Richard E. Denlinger, David L. Matter, Stephen F. Attardo, Geoffrey M. Weirauch, Matthew T. Benoit, Joshua B. |
author_facet |
Finch, Geoffrey Nandyal, Sonya Perretta, Carlie Davies, Benjamin Rosendale, Andrew J. Holmes, Christopher J. Gantz, J. D. Spacht, Drew E. Bailey, Samuel T. Chen, Xiaoting Oyen, Kennan Didion, Elise M. Chakraborty, Souvik Lee, Richard E. Denlinger, David L. Matter, Stephen F. Attardo, Geoffrey M. Weirauch, Matthew T. Benoit, Joshua B. |
author_sort |
Finch, Geoffrey |
title |
Multi-level analysis of reproduction in an Antarctic midge identifies female and male accessory gland products that are altered by larval stress and impact progeny viability |
title_short |
Multi-level analysis of reproduction in an Antarctic midge identifies female and male accessory gland products that are altered by larval stress and impact progeny viability |
title_full |
Multi-level analysis of reproduction in an Antarctic midge identifies female and male accessory gland products that are altered by larval stress and impact progeny viability |
title_fullStr |
Multi-level analysis of reproduction in an Antarctic midge identifies female and male accessory gland products that are altered by larval stress and impact progeny viability |
title_full_unstemmed |
Multi-level analysis of reproduction in an Antarctic midge identifies female and male accessory gland products that are altered by larval stress and impact progeny viability |
title_sort |
multi-level analysis of reproduction in an antarctic midge identifies female and male accessory gland products that are altered by larval stress and impact progeny viability |
publisher |
Nature Publishing Group UK |
publishDate |
2020 |
url |
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7666147/ http://www.ncbi.nlm.nih.gov/pubmed/33188214 https://doi.org/10.1038/s41598-020-76139-6 |
geographic |
Antarctic The Antarctic |
geographic_facet |
Antarctic The Antarctic |
genre |
Antarc* Antarctic Antarctic midge Antarctica Belgica antarctica |
genre_facet |
Antarc* Antarctic Antarctic midge Antarctica Belgica antarctica |
op_source |
Sci Rep |
op_relation |
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7666147/ http://www.ncbi.nlm.nih.gov/pubmed/33188214 http://dx.doi.org/10.1038/s41598-020-76139-6 |
op_rights |
© The Author(s) 2020 Open Access This 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/. |
op_rightsnorm |
CC-BY |
op_doi |
https://doi.org/10.1038/s41598-020-76139-6 |
container_title |
Scientific Reports |
container_volume |
10 |
container_issue |
1 |
_version_ |
1766207136830849024 |