Fire ant social chromosomes: Differences in number, sequence and expression of odorant binding proteins.

Abstract

Variation in social behavior is common yet our knowledge of the mechanisms underpinning its evolution is limited. The fire ant Solenopsis invicta provides a textbook example of a Mendelian element controlling social organization: alternate alleles of a genetic element first identified as encoding an odorant binding protein (OBP) named Gp-9 determine whether a colony accepts one or multiple queens. The potential roles of such a protein in perceiving olfactory cues and evidence of positive selection on its amino acid sequence made it an appealing candidate gene. However, we recently showed that recombination is suppressed between Gp-9 and hundreds of other genes as part of a >19 Mb supergene-like region carried by a pair of social chromosomes. This finding raises the need to reassess the potential role of Gp-9. We identify 23 OBPs in the fire ant genome assembly, including nine located in the region of suppressed recombination with Gp-9. For six of these, the alleles carried by the two variants of the supergene-like region differ in protein-coding sequence and thus likely in function, with Gp-9 showing the strongest evidence of positive selection. We identify an additional OBP specific to the Sb variant of the region. Finally, we find that 14 OBPs are differentially expressed between single- and multiple-queen colonies. These results are consistent with multiple OBPs playing a role in determining social structure.