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Fertility costs of cryptic viral infections in a model social insect

Declining insect populations emphasize the importance of understanding the drivers underlying reductions in insect fitness. Here, we investigated viruses as a threat to social insect reproduction, using honey bees as a model species. We report that in two independent surveys (N = 93 and N = 54, resp...

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Autores principales: Chapman, Abigail, Amiri, Esmaeil, Han, Bin, McDermott, Erin, Rueppell, Olav, Tarpy, David R., Foster, Leonard J., McAfee, Alison
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9508145/
https://www.ncbi.nlm.nih.gov/pubmed/36151143
http://dx.doi.org/10.1038/s41598-022-20330-4
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author Chapman, Abigail
Amiri, Esmaeil
Han, Bin
McDermott, Erin
Rueppell, Olav
Tarpy, David R.
Foster, Leonard J.
McAfee, Alison
author_facet Chapman, Abigail
Amiri, Esmaeil
Han, Bin
McDermott, Erin
Rueppell, Olav
Tarpy, David R.
Foster, Leonard J.
McAfee, Alison
author_sort Chapman, Abigail
collection PubMed
description Declining insect populations emphasize the importance of understanding the drivers underlying reductions in insect fitness. Here, we investigated viruses as a threat to social insect reproduction, using honey bees as a model species. We report that in two independent surveys (N = 93 and N = 54, respectively) of honey bee (Apis mellifera) queens taken from a total of ten beekeeping operations across British Columbia, high levels of natural viral infection are associated with decreased ovary mass. Failed (poor quality) queens displayed higher levels of viral infection, reduced sperm viability, smaller ovaries, and altered ovary protein composition compared to healthy queens. We experimentally infected queens with Israeli acute paralysis virus (IAPV) and found that the ovary masses of IAPV-injected queens were significantly smaller than control queens, demonstrating a causal relationship between viral infection and ovary size. Queens injected with IAPV also had significantly lower expression of vitellogenin, the main source of nutrition deposited into developing oocytes, and higher levels of heat-shock proteins, which are part of the honey bee’s antiviral response. This work together shows that viral infections occurring naturally in the field are compromising queen reproductive success.
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spelling pubmed-95081452022-09-25 Fertility costs of cryptic viral infections in a model social insect Chapman, Abigail Amiri, Esmaeil Han, Bin McDermott, Erin Rueppell, Olav Tarpy, David R. Foster, Leonard J. McAfee, Alison Sci Rep Article Declining insect populations emphasize the importance of understanding the drivers underlying reductions in insect fitness. Here, we investigated viruses as a threat to social insect reproduction, using honey bees as a model species. We report that in two independent surveys (N = 93 and N = 54, respectively) of honey bee (Apis mellifera) queens taken from a total of ten beekeeping operations across British Columbia, high levels of natural viral infection are associated with decreased ovary mass. Failed (poor quality) queens displayed higher levels of viral infection, reduced sperm viability, smaller ovaries, and altered ovary protein composition compared to healthy queens. We experimentally infected queens with Israeli acute paralysis virus (IAPV) and found that the ovary masses of IAPV-injected queens were significantly smaller than control queens, demonstrating a causal relationship between viral infection and ovary size. Queens injected with IAPV also had significantly lower expression of vitellogenin, the main source of nutrition deposited into developing oocytes, and higher levels of heat-shock proteins, which are part of the honey bee’s antiviral response. This work together shows that viral infections occurring naturally in the field are compromising queen reproductive success. Nature Publishing Group UK 2022-09-23 /pmc/articles/PMC9508145/ /pubmed/36151143 http://dx.doi.org/10.1038/s41598-022-20330-4 Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/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/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Chapman, Abigail
Amiri, Esmaeil
Han, Bin
McDermott, Erin
Rueppell, Olav
Tarpy, David R.
Foster, Leonard J.
McAfee, Alison
Fertility costs of cryptic viral infections in a model social insect
title Fertility costs of cryptic viral infections in a model social insect
title_full Fertility costs of cryptic viral infections in a model social insect
title_fullStr Fertility costs of cryptic viral infections in a model social insect
title_full_unstemmed Fertility costs of cryptic viral infections in a model social insect
title_short Fertility costs of cryptic viral infections in a model social insect
title_sort fertility costs of cryptic viral infections in a model social insect
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9508145/
https://www.ncbi.nlm.nih.gov/pubmed/36151143
http://dx.doi.org/10.1038/s41598-022-20330-4
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