Understanding the molecular evolutionary basis of social behavior is a major challenge in evolutionary biology. Social insects evolved a complex language of chemical signals to coordinate thousands of individuals. In the fire ant Solenopsis invicta, chemical signals are involved in the determination of a polymorphic social organization. Single-queen (monogyne) or multiqueen (polygyne) social structure is determined by the “social chromosome,” a nonrecombining region containing 504 genes with two distinct haplotypes, SB and Sb. Monogyne queens are always SBB, while polygyne queens are always SBb. Workers discriminate monogyne from polygyne queens based on olfactory cues. Here, we took an evolutionary ge-nomics approach to search for candidate genes in the social chromosome that could be responsible for this discrimination. We compared the SB and Sb haplotypes and analyzed the evolutionary rates since their divergence. Notably, we identified a cluster of 23 odorant receptors in the nonrecombining region of the social chromosome that stands out in terms of nonsynonymous changes in both haplotypes. The cluster includes twelve genes formed by recent Solenopsis-specific duplications. We found evidence for positive selection on several tree branches and significant differences between the SB and Sb haplotypes of these genes. The most dramatic difference is the complete deletion of two of these genes in Sb. These results suggest that the evolution of polygyne social organization involved adaptations in olfactory genes and opens the way for functional studies of the molecular mechanisms underlying social behavior.
Bibliographical noteFunding Information:
We thank three anonymous reviewers for their constructive criticism of this article. We thank Oksana Riba-Grognuz for assistance with the S. invicta reference genome and social chromosome map. We thank Christina Grozinger for her support to the experimental validation, including usage of lab equipment at Penn State University. We thank Mickey Kosloff for advice on the structural analyses. E.P. was supported by Marie Curie Career Integration Grant no. 631582 and Israel Science Foundation Grants no. 646/15, 2140/15, and 2155/15.
© The Author(s) 2018.
- Genome evolution
- Odorant receptors
- Social evolution
- Social insects
ASJC Scopus subject areas
- Ecology, Evolution, Behavior and Systematics