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Expression analysis of vitellogenins in the workers of the red imported fire ant (Solenopsis invicta)

Vitellogenin has been proposed to regulate division of labor and social organization in social insects. The red imported fire ant (Solenopsis invicta) harbors four distinct, adjacent vitellogenin genes (Vg1, Vg2, Vg3, and Vg4). Contrary to honey bees that have a single Vg ortholog as well as potenti...

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Autores principales: Hawkings, Chloe, Tamborindeguy, Cecilia
Formato: Online Artículo Texto
Lenguaje:English
Publicado: PeerJ Inc. 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5978388/
https://www.ncbi.nlm.nih.gov/pubmed/29868280
http://dx.doi.org/10.7717/peerj.4875
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author Hawkings, Chloe
Tamborindeguy, Cecilia
author_facet Hawkings, Chloe
Tamborindeguy, Cecilia
author_sort Hawkings, Chloe
collection PubMed
description Vitellogenin has been proposed to regulate division of labor and social organization in social insects. The red imported fire ant (Solenopsis invicta) harbors four distinct, adjacent vitellogenin genes (Vg1, Vg2, Vg3, and Vg4). Contrary to honey bees that have a single Vg ortholog as well as potentially fertile nurses, and to other ant species that lay trophic eggs, S. invicta workers completely lack ovaries or the ability to lay eggs. This provides a unique model to investigate whether Vg duplication in S. invicta was followed by subfunctionalization to acquire non-reproductive functions and whether Vg was co-opted to regulate behavior within the worker caste. To investigate these questions, we compared the expression patterns of S. invicta Vg genes among workers from different morphological subcastes or performing different tasks. RT-qPCRs revealed higher relative expression of Vg1 in major workers compared to both medium and minor workers, and of Vg2 in major workers when compared to minor workers. Relative expression of Vg1 was also higher in carbohydrate foragers when compared to nurses and protein foragers. By contrast, the level of expression of Vg2, Vg3, and Vg4 were not significantly different among the workers performing the specific tasks. Additionally, we analyzed the relationship between the expression of the Vg genes and S-hydroprene, a juvenile hormone analog. No changes in Vg expression were recorded in workers 12 h after application of the analog. Our results suggest that in S. invicta the Vg gene underwent subfunctionalization after duplication to new functions based on the expression bias observed in these data. This may suggest an alternative and still unknown function for Vg in the workers that needs to be investigated further.
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spelling pubmed-59783882018-06-04 Expression analysis of vitellogenins in the workers of the red imported fire ant (Solenopsis invicta) Hawkings, Chloe Tamborindeguy, Cecilia PeerJ Entomology Vitellogenin has been proposed to regulate division of labor and social organization in social insects. The red imported fire ant (Solenopsis invicta) harbors four distinct, adjacent vitellogenin genes (Vg1, Vg2, Vg3, and Vg4). Contrary to honey bees that have a single Vg ortholog as well as potentially fertile nurses, and to other ant species that lay trophic eggs, S. invicta workers completely lack ovaries or the ability to lay eggs. This provides a unique model to investigate whether Vg duplication in S. invicta was followed by subfunctionalization to acquire non-reproductive functions and whether Vg was co-opted to regulate behavior within the worker caste. To investigate these questions, we compared the expression patterns of S. invicta Vg genes among workers from different morphological subcastes or performing different tasks. RT-qPCRs revealed higher relative expression of Vg1 in major workers compared to both medium and minor workers, and of Vg2 in major workers when compared to minor workers. Relative expression of Vg1 was also higher in carbohydrate foragers when compared to nurses and protein foragers. By contrast, the level of expression of Vg2, Vg3, and Vg4 were not significantly different among the workers performing the specific tasks. Additionally, we analyzed the relationship between the expression of the Vg genes and S-hydroprene, a juvenile hormone analog. No changes in Vg expression were recorded in workers 12 h after application of the analog. Our results suggest that in S. invicta the Vg gene underwent subfunctionalization after duplication to new functions based on the expression bias observed in these data. This may suggest an alternative and still unknown function for Vg in the workers that needs to be investigated further. PeerJ Inc. 2018-05-28 /pmc/articles/PMC5978388/ /pubmed/29868280 http://dx.doi.org/10.7717/peerj.4875 Text en © 2018 Hawkings and Tamborindeguy http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, reproduction and adaptation in any medium and for any purpose provided that it is properly attributed. For attribution, the original author(s), title, publication source (PeerJ) and either DOI or URL of the article must be cited.
spellingShingle Entomology
Hawkings, Chloe
Tamborindeguy, Cecilia
Expression analysis of vitellogenins in the workers of the red imported fire ant (Solenopsis invicta)
title Expression analysis of vitellogenins in the workers of the red imported fire ant (Solenopsis invicta)
title_full Expression analysis of vitellogenins in the workers of the red imported fire ant (Solenopsis invicta)
title_fullStr Expression analysis of vitellogenins in the workers of the red imported fire ant (Solenopsis invicta)
title_full_unstemmed Expression analysis of vitellogenins in the workers of the red imported fire ant (Solenopsis invicta)
title_short Expression analysis of vitellogenins in the workers of the red imported fire ant (Solenopsis invicta)
title_sort expression analysis of vitellogenins in the workers of the red imported fire ant (solenopsis invicta)
topic Entomology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5978388/
https://www.ncbi.nlm.nih.gov/pubmed/29868280
http://dx.doi.org/10.7717/peerj.4875
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