Queen discrimination behavior in the fire ant Solenopsis invicta maintains its two types of societies: colonies with one (monogyne) or many (polygyne) queens, yet the underlying genetic mechanism is poorly understood. This behavior is controlled by two supergene alleles, SB and Sb, encompassing ~600 genes. Polygyne workers, having either the SB/SB or SB/Sb genotype, accept additional SB/Sb queens into their colonies but kill SB/SB queens. In contrast, monogyne workers, all having the SB/SB genotype, reject all additional queens regardless of genotypes.
Our main question is: How do polygyne workers recognize the queen’s genotype? To address this question, we dissected it into three parts: the social chromosome investigation, signal perception and making decision in the worker, and signal production in the queen.
In the social chromosome investigation, we questioned how the supergene evolved and shaped the social polymorphism in the fire ant. To address this question, we tried to super-scaffold the social chromosome and identified the supergene boundaries. We super-scaffolded seven scaffolds and five contigs, and identified the outer most breakpoint of the supergene. Additionally, we found that the supergene formation likely changed the cis-regulation of breakpoint adjacent genes.
From the worker side, we hypothesized that the evolution of differential expression of key genes in their antennae and brains affects the difference in sensing queens and making queen acceptance/rejection decision, respectively, by the alternate worker genotypes. We sequenced RNA of pooled antennae, and pooled brains from three groups of workers: monogyne SB/SB, polygyne SB/SB, and polygyne SB/Sb. We identified 81 and 98 differentially expressed genes in the antennae and brains, respectively. Detailed analysis on odorant binding protein SiOBP12 revealed SiOBP12 has an Sb-specific duplication, SiOBP12b’, which may have evolved, in part, through expression neofunctionalization. From brain RNA-seq analysis, we highlighted two putative signaling transmission genes.
From the queen side, we aimed to find the source of the supergene chemical cues. We hypothesized the body part which habors the source of the cues will elicit the queen discrimination behavior consistently between two closed rubbing times. To test this, we used rubbing experiments on different body parts of matured virgin queens. Our results suggested the abdomen likely contains the source of the cues.

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