Simple inheritance, complex regulation: Supergene‐mediated fire ant queen polymorphism

Abstract

The fire ant Solenopsis invicta exists in two alternate social forms: monogyne nests contain a single reproductive queen and polygyne nests contain multiple reproductive queens. This colony-level social polymorphism corresponds with individual differences in queen physiology, queen dispersal patterns and worker discrimination behaviours, all evidently regulated by an inversion-based supergene that spans more than 13 Mb of a "social chromosome," contains over 400 protein-coding genes and rarely undergoes recombination. The specific mechanisms by which this supergene influences expression of the many distinctive features that characterize the alternate forms remain almost wholly unknown. To advance our understanding of these mechanisms, we explore the effects of social chromosome genotype and natal colony social form on gene expression in queens sampled as they embarked on nuptial flights, using RNA-sequencing of brains and ovaries. We observe a large effect of natal social form, that is, of the social/developmental environment, on gene expression profiles, with similarly substantial effects of genotype, including: (a) supergene-associated gene upregulation, (b) allele-specific expression and (c) pronounced extra-supergene trans-regulatory effects. These findings, along with observed spatial variation in differential and allele-specific expression within the supergene region, highlight the complex gene regulatory landscape that emerged following divergence of the inversion-mediated Sb haplotype from its homologue, which presumably largely retained the ancestral gene order. The distinctive supergene-associated gene expression trajectories we document at the onset of a queen's reproductive life expand the known record of relevant molecular correlates of a complex social polymorphism and point to putative genetic factors underpinning the alternate social syndromes.

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

“…We used published RNA-sequencing (RNA-Seq) data from six data sets containing 22 single-queen and 27 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).…”

“…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).…”

“…The first part of the analysis was done using the six data sets with 22 single-queen and 27 multiple-queen colonies. Two of these data sets involved RNA-Seq from whole bodies (Morandin et al, 2016;Wurm et al, 2011) of S. invicta queens, while the other four data sets involved RNA-Seq from brains of S. invicta queens (Arsenault et al, 2020;Chandra et al, 2018;Manfredini et al, 2021;Martinez-Ruiz et al, 2020). For a second analysis, we focused on one of the data sets (BioProject PRJNA629802) containing RNA-Seq from brains of eight queens from eight single-queen colonies and three queens per colony from each of eight multiple-queen colonies (Arsenault et al, 2020).…”

Non-kin Cooperation in Ants

“…However, we know surprisingly little about the proximate mechanisms leading to polygyne colonies and variation in polygyny within and among species. An exception is fire ants in the genus Solenopsis, where genetic variation at a large supergene plays a decisive role in the formation of polygyne nests (Krieger and Ross, 2005;Gotzek, 2007;Arsenault et al, 2020;Yan et al, 2020). In this case, workers behave differently toward queens of distinct supergene genotypes; this behavioral variation ultimately only leads to the acceptance of queens possessing heterozygous genotypes in polygyne colonies.…”

Distinct colony boundaries and larval discrimination in polygyne red imported fire ants (Solenopsis invicta)

“…Interestingly, the fire ant supergene (and all the complex traits associated with it) exhibits two haplotypes (SB and Sb), which are passed on via Mendelian inheritance (Arsenault et al, 2020;Ross & Shoemaker, 2018;Wang et al, 2013). Colonies bearing the Sb supergene haplotype express the polygyne phenotype (i.e., colonies accept multiple SB/Sb queens and reject any SB/SB queens), whereas colonies bearing exclusively the SB haplotype express the monogyne phenotype (i.e., colonies accept only one SB/SB queen and reject all SB/Sb queens; Arsenault et al, 2020;Gotzek & Ross, 2008Ross & Keller, 2002). Moreover, supergene control appears to be complete, as social organization is independent of genetic diversity within the colony (Gotzek & Ross, 2008), as well as nongenetic factors such as environmental odours, queen reproductive status, and prior social experience of the workers Ross & Keller, 2002).…”