Has gene expression neofunctionalization in the fire ant antennae contributed to queen discrimination behavior?
Viet-Dai Dang1,2,3,4, Amir B Cohanim5, Silvia Fontana1,2,3
1Biodiversity Research Center Academia Sinica Taipei Taiwan.
Ecology and Evolution
|December 3, 2019
Summary
Fire ant queen discrimination is genetically controlled. Differential gene expression in antennae, particularly odorant-binding protein SiOBP12b, likely drives distinct worker behaviors in monogyne and polygyne societies.
Area of Science:
- Evolutionary genetics
- Animal behavior
- Chemical ecology
Background:
- Queen discrimination behavior in fire ants (Solenopsis invicta) maintains distinct monogyne (single queen) and polygyne (multiple queens) social structures.
- This behavior is governed by a supergene with two alleles (SB and Sb) but the precise genetic mechanisms remain unclear.
- Worker genotypes (SB/SB, SB/Sb) influence queen acceptance or rejection, with polygyne workers accepting SB/Sb queens but rejecting SB/SB queens, while monogyne workers reject all additional queens.
Purpose of the Study:
- To investigate the role of differential gene expression in antennae, the primary sensory organ, in mediating queen discrimination behavior.
- To identify specific genes within the supergene responsible for the distinct sensory perception of queens by different worker genotypes.
Main Methods:
- RNA sequencing was performed on antennae from three worker classes: monogyne SB/SB, polygyne SB/SB, and polygyne SB/Sb.
- Differentially expressed genes were identified, with a focus on those involved in chemical metabolism and perception.
- Specific genes, including odorant receptor SiOR463 and odorant-binding protein SiOBP12, were analyzed for genetic variation and expression patterns.
Main Results:
- 81 differentially expressed protein-coding genes were identified, including 13 related to chemical perception.
- The odorant receptor SiOR463 was lost in the Sb genome, while the odorant-binding protein SiOBP12 showed an Sb-specific duplication (SiOBP12b') expressed in polygyne SB/Sb worker antennae.
- Antennal expression of SiOBP12b' is unique to S. invicta, suggesting a role in species-specific queen discrimination.
Conclusions:
- Differential gene expression in antennae, particularly the neofunctionalization of SiOBP12b', likely underlies the evolution of queen discrimination in fire ants.
- This study highlights the importance of sensory gene evolution in shaping complex social behaviors.
