Social isolation and group size are associated with divergent gene expression in the brain of ant queens

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.

Larger, more connected societies of ants have a higher prevalence of viruses

“…We further downloaded the genome sequences of 231 newly identified insect viruses (Käfer et al, 2019) and added these to our kraken2 database. We used this combined database for taxonomic classification of the RNA-Seq reads obtained from whole body or brains of S. invicta queens from single-queen and multiple-queen colonies (Arsenault et al, 2020;Chandra et al, 2018;Manfredini et al, 2021;Martinez-Ruiz et al, 2020;Morandin et al, 2016;Wurm et al, 2011). Because our kraken2 database contained the S. invicta genome, kraken2 could classify any reads from endogenous viral elements to the genus Solenopsis and not as free infectious viruses.…”

“…For each of the 22 single-queen and 27 multiple-queen colonies, we used published RNA-Seq data from whole bodies (three single-queen and eight multiple-queen colonies; BioProject PRJDB4088 and PRJNA629802; Morandin et al, 2016;Wurm et al, 2011) or brains of queens (19 single-queen and 19 multiple-queen colonies; BioProject PRJNA525584, PRJNA472392, PRJNA542606 and PRJNA629802; Arsenault et al, 2020;Chandra et al, 2018;Manfredini et al, 2021;Martinez-Ruiz et al, 2020). All colonies were sampled in North America (see Supporting Information Data Set).…”

“…All colonies were sampled in North America (see Supporting Information Data Set). Total RNA was extracted from whole bodies or brains of queens, followed by Illumina library preparation from total RNA after ribodepletion (Manfredini et al, 2021) or from enriched mRNA (Arsenault et al, 2020;Chandra et al, 2018;Martinez-Ruiz et al, 2020;Morandin et al, 2016;Wurm et al, 2011).…”

“…We analysed 1.77 billion independent RNA-Seq reads from whole bodies and brains of queens with one sample from each of 22 singlequeen colonies and up to three samples from each of 27 multiplequeen colonies (i.e., on average 25 million independent reads from each sample; see Supporting Information Data Set for details; Arsenault et al, 2020;Chandra et al, 2018;Manfredini et al, 2021;Martinez-Ruiz et al, 2020;Morandin et al, 2016;Wurm et al, 2011).…”

Deepening the understanding of social bonding and dynamics of social interactions

“…Our next article departs from analysis of social bonding in mammals and birds to examine mechanisms of plasticity involved in formation of groups of individuals in a completely different taxon. Namely, Manfredini et al 10 examine molecular signatures of plasticity associated with differences in social environment in the fire ants ( Solenopsis invicta ). Queens of this species can found colonies in either solitary or group conditions 11 .…”