Social isolation and group size are associated with divergent gene expression in the brain of ant queens
Social life and isolation pose a complex suite of challenges to organisms prompting significant changes in neural state. However, plasticity in how brains respond to social challenges remains largely unexplored. The fire ants Solenopsis invicta provide an ideal scenario for examining this. Fire ant...
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Published in | Genes, brain and behavior Vol. 21; no. 3; pp. e12758 - n/a |
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Main Authors | , , , , |
Format | Journal Article |
Language | English |
Published |
Oxford, UK
Blackwell Publishing Ltd
01.03.2022
John Wiley & Sons, Inc |
Subjects | |
Online Access | Get full text |
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Abstract | Social life and isolation pose a complex suite of challenges to organisms prompting significant changes in neural state. However, plasticity in how brains respond to social challenges remains largely unexplored. The fire ants Solenopsis invicta provide an ideal scenario for examining this. Fire ant queens may found colonies individually or in groups of up to 30 queens, depending on key factors such as density of newly mated queens and availability of nesting sites. We artificially manipulated availability of nesting sites to test how the brain responds to social versus solitary colony founding at two key timepoints (early vs. late colony founding) and to group size (large vs. small groups). We adopted a powerful neurogenomic approach to identify even subtle differences of gene expression between treatment groups, and we built a global gene co‐expression network of the fire ant brain to identify gene modules specifically associated with the different components of the social environment. The difference between group and single founding queens involves only one gene when founding behavior is still plastic and queens can switch from one modality to another, while hundreds of genes are involved later in the process, when behaviors have lost the initial plasticity and are more canalized. Furthermore, we find that large groups are associated with greater changes in gene expression than small groups, showing that even potentially subtle differences in the social environment can be linked to different neurogenomic states.
Exposure to social isolation and varying group size are associated with significant changes in the levels of expression of genes in the brain of fire ant queens. |
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AbstractList | Abstract
Social life and isolation pose a complex suite of challenges to organisms prompting significant changes in neural state. However, plasticity in how brains respond to social challenges remains largely unexplored. The fire ants
Solenopsis invicta
provide an ideal scenario for examining this. Fire ant queens may found colonies individually or in groups of up to 30 queens, depending on key factors such as density of newly mated queens and availability of nesting sites. We artificially manipulated availability of nesting sites to test how the brain responds to social versus solitary colony founding at two key timepoints (early vs. late colony founding) and to group size (large vs. small groups). We adopted a powerful neurogenomic approach to identify even subtle differences of gene expression between treatment groups, and we built a global gene co‐expression network of the fire ant brain to identify gene modules specifically associated with the different components of the social environment. The difference between group and single founding queens involves only one gene when founding behavior is still plastic and queens can switch from one modality to another, while hundreds of genes are involved later in the process, when behaviors have lost the initial plasticity and are more canalized. Furthermore, we find that large groups are associated with greater changes in gene expression than small groups, showing that even potentially subtle differences in the social environment can be linked to different neurogenomic states. Social life and isolation pose a complex suite of challenges to organisms prompting significant changes in neural state. However, plasticity in how brains respond to social challenges remains largely unexplored. The fire ants Solenopsis invicta provide an ideal scenario for examining this. Fire ant queens may found colonies individually or in groups of up to 30 queens, depending on key factors such as density of newly mated queens and availability of nesting sites. We artificially manipulated availability of nesting sites to test how the brain responds to social versus solitary colony founding at two key timepoints (early vs. late colony founding) and to group size (large vs. small groups). We adopted a powerful neurogenomic approach to identify even subtle differences of gene expression between treatment groups, and we built a global gene co‐expression network of the fire ant brain to identify gene modules specifically associated with the different components of the social environment. The difference between group and single founding queens involves only one gene when founding behavior is still plastic and queens can switch from one modality to another, while hundreds of genes are involved later in the process, when behaviors have lost the initial plasticity and are more canalized. Furthermore, we find that large groups are associated with greater changes in gene expression than small groups, showing that even potentially subtle differences in the social environment can be linked to different neurogenomic states. Exposure to social isolation and varying group size are associated with significant changes in the levels of expression of genes in the brain of fire ant queens. Social life and isolation pose a complex suite of challenges to organisms prompting significant changes in neural state. However, plasticity in how brains respond to social challenges remains largely unexplored. The fire ants Solenopsis invicta provide an ideal scenario for examining this. Fire ant queens may found colonies individually or in groups of up to 30 queens, depending on key factors such as density of newly mated queens and availability of nesting sites. We artificially manipulated availability of nesting sites to test how the brain responds to social versus solitary colony founding at two key timepoints (early vs. late colony founding) and to group size (large vs. small groups). We adopted a powerful neurogenomic approach to identify even subtle differences of gene expression between treatment groups, and we built a global gene co‐expression network of the fire ant brain to identify gene modules specifically associated with the different components of the social environment. The difference between group and single founding queens involves only one gene when founding behavior is still plastic and queens can switch from one modality to another, while hundreds of genes are involved later in the process, when behaviors have lost the initial plasticity and are more canalized. Furthermore, we find that large groups are associated with greater changes in gene expression than small groups, showing that even potentially subtle differences in the social environment can be linked to different neurogenomic states. Social life and isolation pose a complex suite of challenges to organisms prompting significant changes in neural state. However, plasticity in how brains respond to social challenges remains largely unexplored. The fire ants Solenopsis invicta provide an ideal scenario for examining this. Fire ant queens may found colonies individually or in groups of up to 30 queens, depending on key factors such as density of newly mated queens and availability of nesting sites. We artificially manipulated availability of nesting sites to test how the brain responds to social versus solitary colony founding at two key timepoints (early vs. late colony founding) and to group size (large vs. small groups). We adopted a powerful neurogenomic approach to identify even subtle differences of gene expression between treatment groups, and we built a global gene co‐expression network of the fire ant brain to identify gene modules specifically associated with the different components of the social environment. The difference between group and single founding queens involves only one gene when founding behavior is still plastic and queens can switch from one modality to another, while hundreds of genes are involved later in the process, when behaviors have lost the initial plasticity and are more canalized. Furthermore, we find that large groups are associated with greater changes in gene expression than small groups, showing that even potentially subtle differences in the social environment can be linked to different neurogenomic states. Exposure to social isolation and varying group size are associated with significant changes in the levels of expression of genes in the brain of fire ant queens. |
Author | Wurm, Yannick Brown, Mark J. F. Martinez‐Ruiz, Carlos Manfredini, Fabio Shoemaker, De Wayne |
AuthorAffiliation | 3 School of Biological and Chemical Sciences Queen Mary University of London London UK 1 School of Biological Sciences University of Aberdeen Aberdeen UK 2 School of Biological Sciences Royal Holloway University of London Egham UK 4 Department of Entomology and Plant Pathology The University of Tennessee Institute of Agriculture Knoxville Tennessee USA |
AuthorAffiliation_xml | – name: 4 Department of Entomology and Plant Pathology The University of Tennessee Institute of Agriculture Knoxville Tennessee USA – name: 1 School of Biological Sciences University of Aberdeen Aberdeen UK – name: 2 School of Biological Sciences Royal Holloway University of London Egham UK – name: 3 School of Biological and Chemical Sciences Queen Mary University of London London UK |
Author_xml | – sequence: 1 givenname: Fabio orcidid: 0000-0002-9134-3994 surname: Manfredini fullname: Manfredini, Fabio email: fabio.manfredini@abdn.ac.uk organization: Royal Holloway University of London – sequence: 2 givenname: Carlos surname: Martinez‐Ruiz fullname: Martinez‐Ruiz, Carlos organization: Queen Mary University of London – sequence: 3 givenname: Yannick surname: Wurm fullname: Wurm, Yannick organization: Queen Mary University of London – sequence: 4 givenname: De Wayne surname: Shoemaker fullname: Shoemaker, De Wayne organization: The University of Tennessee Institute of Agriculture – sequence: 5 givenname: Mark J. F. surname: Brown fullname: Brown, Mark J. F. organization: Royal Holloway University of London |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/34101985$$D View this record in MEDLINE/PubMed |
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Keywords | fire ants social behavior isolation group size colony founding Solenopsis invicta gene expression |
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SubjectTerms | Animals Ants - genetics Brain Colonies colony founding fire ants Gene Expression Group size isolation Neural plasticity Original Queens Reproduction Social Behavior Social environment Social interactions Social Isolation Solenopsis invicta |
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Title | Social isolation and group size are associated with divergent gene expression in the brain of ant queens |
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