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Fire ant social chromosomes: Differences in number, sequence and expression of odorant binding proteins

Variation in social behavior is common yet our knowledge of the mechanisms underpinning its evolution is limited. The fire ant Solenopsis invicta provides a textbook example of a Mendelian element controlling social organization: alternate alleles of a genetic element first identified as encoding an...

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Autores principales: Pracana, Rodrigo, Levantis, Ilya, Martínez‐Ruiz, Carlos, Stolle, Eckart, Priyam, Anurag, Wurm, Yannick
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley and Sons Inc. 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6121795/
https://www.ncbi.nlm.nih.gov/pubmed/30283649
http://dx.doi.org/10.1002/evl3.22
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author Pracana, Rodrigo
Levantis, Ilya
Martínez‐Ruiz, Carlos
Stolle, Eckart
Priyam, Anurag
Wurm, Yannick
author_facet Pracana, Rodrigo
Levantis, Ilya
Martínez‐Ruiz, Carlos
Stolle, Eckart
Priyam, Anurag
Wurm, Yannick
author_sort Pracana, Rodrigo
collection PubMed
description Variation in social behavior is common yet our knowledge of the mechanisms underpinning its evolution is limited. The fire ant Solenopsis invicta provides a textbook example of a Mendelian element controlling social organization: alternate alleles of a genetic element first identified as encoding an odorant binding protein (OBP) named Gp‐9 determine whether a colony accepts one or multiple queens. The potential roles of such a protein in perceiving olfactory cues and evidence of positive selection on its amino acid sequence made it an appealing candidate gene. However, we recently showed that recombination is suppressed between Gp‐9 and hundreds of other genes as part of a >19 Mb supergene‐like region carried by a pair of social chromosomes. This finding raises the need to reassess the potential role of Gp‐9. We identify 23 OBPs in the fire ant genome assembly, including nine located in the region of suppressed recombination with Gp‐9. For six of these, the alleles carried by the two variants of the supergene‐like region differ in protein‐coding sequence and thus likely in function, with Gp‐9 showing the strongest evidence of positive selection. We identify an additional OBP specific to the Sb variant of the region. Finally, we find that 14 OBPs are differentially expressed between single‐ and multiple‐queen colonies. These results are consistent with multiple OBPs playing a role in determining social structure.
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spelling pubmed-61217952018-10-03 Fire ant social chromosomes: Differences in number, sequence and expression of odorant binding proteins Pracana, Rodrigo Levantis, Ilya Martínez‐Ruiz, Carlos Stolle, Eckart Priyam, Anurag Wurm, Yannick Evol Lett Letters Variation in social behavior is common yet our knowledge of the mechanisms underpinning its evolution is limited. The fire ant Solenopsis invicta provides a textbook example of a Mendelian element controlling social organization: alternate alleles of a genetic element first identified as encoding an odorant binding protein (OBP) named Gp‐9 determine whether a colony accepts one or multiple queens. The potential roles of such a protein in perceiving olfactory cues and evidence of positive selection on its amino acid sequence made it an appealing candidate gene. However, we recently showed that recombination is suppressed between Gp‐9 and hundreds of other genes as part of a >19 Mb supergene‐like region carried by a pair of social chromosomes. This finding raises the need to reassess the potential role of Gp‐9. We identify 23 OBPs in the fire ant genome assembly, including nine located in the region of suppressed recombination with Gp‐9. For six of these, the alleles carried by the two variants of the supergene‐like region differ in protein‐coding sequence and thus likely in function, with Gp‐9 showing the strongest evidence of positive selection. We identify an additional OBP specific to the Sb variant of the region. Finally, we find that 14 OBPs are differentially expressed between single‐ and multiple‐queen colonies. These results are consistent with multiple OBPs playing a role in determining social structure. John Wiley and Sons Inc. 2017-08-23 /pmc/articles/PMC6121795/ /pubmed/30283649 http://dx.doi.org/10.1002/evl3.22 Text en © 2017 The Author(s). Evolution Letters published by Wiley Periodicals, Inc. on behalf of Society for the Study of Evolution (SSE) and European Society for Evolutionary Biology (ESEB). This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
spellingShingle Letters
Pracana, Rodrigo
Levantis, Ilya
Martínez‐Ruiz, Carlos
Stolle, Eckart
Priyam, Anurag
Wurm, Yannick
Fire ant social chromosomes: Differences in number, sequence and expression of odorant binding proteins
title Fire ant social chromosomes: Differences in number, sequence and expression of odorant binding proteins
title_full Fire ant social chromosomes: Differences in number, sequence and expression of odorant binding proteins
title_fullStr Fire ant social chromosomes: Differences in number, sequence and expression of odorant binding proteins
title_full_unstemmed Fire ant social chromosomes: Differences in number, sequence and expression of odorant binding proteins
title_short Fire ant social chromosomes: Differences in number, sequence and expression of odorant binding proteins
title_sort fire ant social chromosomes: differences in number, sequence and expression of odorant binding proteins
topic Letters
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6121795/
https://www.ncbi.nlm.nih.gov/pubmed/30283649
http://dx.doi.org/10.1002/evl3.22
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