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, with ~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 SB/SB, reject all additional queens regardless of genotype. Because the SB and Sb alleles have suppressed recombination, determining which genes within the supergene mediate this differential worker behavior is difficult. We hypothesized that the alternate worker genotypes sense queens differently because of the evolution of differential expression of key genes in their main sensory organ, the antennae. To identify such genes, we sequenced RNA from four replicates of pooled antennae from three classes of workers: monogyne SB/SB, polygyne SB/SB, and polygyne SB/Sb. We identified 81 differentially expressed protein-coding genes with 13 encoding potential chemical metabolism or perception proteins. We focused on the two odorant perception genes: an odorant receptor SiOR463 and an odorant-binding protein SiOBP12. We found that SiOR463 has been lost in the Sb genome. In contrast, SiOBP12 has an Sb-specific duplication, SiOBP12b′, which is expressed in the SB/Sb worker antennae, while both paralogs are expressed in the body. Comparisons with another fire ant species revealed that SiOBP12b′ antennal expression is specific to S. invicta and suggests that queen discrimination may have evolved, in part, through expression neofunctionalization.
Bibliographical noteFunding Information:
We thank three anonymous reviewers and Scotty C.C Yang for comments on the manuscript, and Meiyeh Lu and the High Throughput Sequencing Core (Biodiversity Research Center, Academia Sinica, Taiwan) for sequencing, advice, and support. We acknowledge two students Ivy Yen and Winnie Ho for their help in RNA sample preparation. Research was funded by the Biodiversity Research Center, Academia Sinica, grants from MOST (103‐2311‐B‐001‐018‐MY3 and 104‐2314‐B‐001‐009‐MY5), and an Academia Sinica Career Development Grant to J.W.
© 2019 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd.
- Solenopsis invicta
- fire ant
- odorant-binding protein
- worker antennae
ASJC Scopus subject areas
- Ecology, Evolution, Behavior and Systematics
- Nature and Landscape Conservation