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Insights into the queen discrimination behavior in the fire ant from worker antennal RNA profiling

Viet-Dai Dang, Viet-Dai DANG , John WANG
TIGP Biodiversity Program, Biodiversity Research Center, Academia Sinica, Taipei, Taiwan; TIGP Biodiversity Program, Biodiversity Research Center, Academia Sinica, Taipei, Taiwan ; Biodiversity Research Center, Academia Sinica, Taipei, Taiwan
The queen acceptance and rejection behavior in the red imported fire ant by workers is associated with the genotype composition of both workers and queens. This behavior is controlled by a supergene with two alleles: SB and Sb. The multi-queen colony (polygyne) workers, who have either the SB/SB or SB/Sb genotype, can sense and accept only additional SB/Sb queens into their colonies and will kill SB/SB queens. In contrast, the single-queen colony (monogyne) workers, all having the SB/SB genotype, accept only their own SB/SB mother and reject all additional queens, regardless of genotype. Although the supergene controls this behavior, which of the ~600 protein coding genes within it actually mediate this queen-worker interaction behavior is unknown. In this study we hypothesized that the alternate worker genotypes sense queens differently because they express different patterns of genes in their main sensory organ, the antennae. To identify such genes, we sequenced RNA extracted and amplified from four biological replicate pools of antennae of three groups of workers: monogyne SB/SB, polygyne SB/SB, and polygyne SB/Sb (M_BB, P_BB, and P_Bb, respectively). Analysis of the RNA-seq data revealed 80 differentially expressed genes with 47 genes being up-regulated in P_Bb compared to both P_BB and M_BB samples. Only six genes were up-regulated in polygyne (P_BB and P_Bb) compared to monogyne (M_BB) samples. This result indicated that antennal RNA expression is affected more by genotype than social organization. Only 35 of the 80 genes have predicted function. Of these, 11 encode potential odor metabolism or perception proteins have potential to function in queen discrimination behavior.