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.

Keywords: Green beard; Solenopsis invicta; olfaction; pheromone; social behavior; social chromosome; supergene.

Figure 1

Phylogenetic tree based on a codon‐level alignment of revised gene predictions for previously described OBPs (SiOBP1–17) and novel OBPs (SiOBPZ2–Z6). Branches are colored by gene cluster and linkage group (lg). SiOBPZ1 was removed from this analysis because the high divergence of its sequence led to unreliable alignments and positioning in the phylogeny. All OBPs on linkage group 16 (lg16) are within the supergene‐like region of the social chromosomes (Fig. 2).

Figure 2

Relative positions on the social chromosome (i.e., linkage group 16) of 10 OBP loci, highlighting intron–exon structures and differences between the supergene region of Sb (blue) and SB (red). SiOBPZ5 is specific to Sb but we do not know its exact location; SiOBP15 is missing a 3‐exon region in Sb; SiOBP9 is in an unmapped scaffold that likely belongs to the supergene region based on high levels of SB‐Sb differentiation (Pracana et al. 2017).

Figure 3

Expression patterns for all analyzed RNAseq datasets. Each tile represents the logarithm base 2 of DESeq normalized transcript counts. The rows with asterisks (*) correspond to those OBPs with significant differential expression between social forms within castes in dataset A (Morandin et al. 2016). Information about each dataset is available in Table S2 (A: PRJDB4088, B and C: PRJNA49629, D: PRJNA266847). ^† The exons of SiOBP5 and SiOBP7 are split across three unmapped scaffolds; we do not know whether these genes are within or outside the supergene region.