Highlights d Multi-queen colonies of a fire ant produce queens asexually but workers sexually d Single-queen colonies produce both queens and workers sexually d Queens in multi-queen colonies require sperm from singlequeen colony males to produce workers d Distinct asexual/multi-queen lineages may stem from a sexual/single-queen population
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 behaviors, all evidently regulated by an inversion-based supergene that spans more than 13Mb 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 effects of social chromosome genotype and natal colony social form on gene expression in virgin queens sampled as they embarked on nuptial flights, using RNA-sequencing of two important tissues. We observe relatively minor effects of natal social form, that is, of the social/developmental environment, on gene expression profiles, but substantial effects of genotype, including i) supergene-associated gene upregulation, ii) allele-specific expression, and iii) 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 evolutionary divergence of the inversion-mediated Sb haplotype from its homolog that largely retained the ancestral gene order.The distinctive social chromosome-linked 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 underpinnings of the alternate social syndromes.
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.
Ants communicate via large arrays of pheromones and possess expanded, highly complex olfactory systems, with antennal lobes in the brain comprising ~500 glomeruli. This expansion implies that odors could activate hundreds of glomeruli, which would pose challenges for higher order processing. To study this problem, we generated the first transgenic ants, expressing the genetically encoded calcium indicator GCaMP6s in olfactory sensory neurons. Using two-photon imaging, we mapped complete glomerular responses to four ant alarm pheromones. Alarm pheromones robustly activated ≤6 glomeruli, and activity maps for the three pheromones inducing panic-alarm in our study species converged on a single glomerulus. These results demonstrate that, rather than using broadly tuned combinatorial encoding, ants employ precise, narrowly tuned, and stereotyped representation of alarm pheromone cues. The identification of a central sensory hub glomerulus for alarm behavior suggests that a simple neural architecture is sufficient to translate pheromone perception into behavioral outputs.
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