Radiation and hybridization underpin the spread of the fire ant social supergene

Abstract

Supergenes are clusters of tightly linked genes that jointly produce complex phenotypes. Although widespread in nature, how such genomic elements are formed and how they spread are in most cases unclear. In the fire ant Solenopsis invicta and closely related species, a "social supergene controls whether a colony maintains one or multiple queens. Here, we show that the three inversions constituting the Social b (Sb) supergene emerged sequentially during the separation of the ancestral lineages of S. invicta and Solenopsis richteri. The two first inversions arose in the ancestral population of both species, while the third one arose in the S. richteri lineage. Once completely assembled in the S. richteri lineage, the supergene first introgressed into S. invicta, and from there into the other species of the socially polymorphic group of South American fire ant species. Surprisingly, the introgression of this large and important genomic element occurred despite recent hybridization being uncommon between several of the species. These results highlight how supergenes can readily move across species boundaries, possibly because of fitness benefits they provide and/or expression of selfish properties favoring their transmission.

Keywords: fire ants; hybridization; introgression; social polymorphism; supergene.

Fig. 1.

Phylogenetic hypotheses for six socially polymorphic fire ant species and their three Sb supergene inversions. Rooted cladograms (Top) and unrooted phylogenies (Bottom) of chromosomes 1 to 15 (A) and of inversion In(16)3 (B), inversion In(16)2 (C), and inversion In(16)1 (D) based on complete genomes of 185 (haploid) males. For each inversion phylogeny, Sb haplotypes are circled with a thick black line. Sequences from the outgroup species are not circled. Bootstrap support values <100 on inner branches between species lineages are shown in red type.

Fig. 2.

D statistics analyses of the fire ant SB and Sb supergene haplotypes. (A) Schematic representation of the method. Only polymorphic sites with the ABBA and BABA combination of alleles in the focal species were analyzed. (B) Summary depiction of the D statistics for the In(16)3 inversion (Left), In(16)2 inversion (Middle), and In(16)1 inversion (Right) for all combinations of SB and Sb haplotypes across species (species tree, Far Left). Increasingly negative (blue) D values indicate that Sb haplotypes share increasingly more of the derived alleles with SB haplotypes from the same species than with SB haplotypes of other species. Increasingly positive (yellow) values indicate increasingly more alleles are shared with the other species than with conspecifics. Red boxes highlight comparisons for which the highest D values are predicted for each inversion based on the phylogenetic results.

Fig. 3.

Geographic distributions of the six socially polymorphic fire ant species and evidence of gene flow among them. (A) Estimated native species ranges. (B) Frequencies of the 12 most commonly recovered topologies inferred from topology weighting using windows of 1,000 SNPs in the nuclear genomes (chromosomes 1 to 15). (C) Heatmap summarizing the D statistics results for different combinations of socially polymorphic species using S. metallica and S. saevissima as outgroups (S. AdRX samples are included with S. invicta). Higher D values (warmer colors) indicate higher estimates of introgression (admixture). Error bars represent SD. (D) Admixture graphs representing the evolutionary history of the socially polymorphic species. The three graphs show all proposed admixture events (orange dashed lines) included in the six best-fitting admixture graphs (SI Appendix, Fig. S11).

Fig. 4.

Hypothesized evolutionary history of the Sb supergene haplotype. The green line represents the evolutionary history of Sb: dashed for the intermediate stages, and solid for the complete haplotype with the three inversions. Arrows illustrate introgression events between the socially polymorphic species inferred from Sb inversion phylogenies. The blue line represents the evolutionary history of the SB haplotype. The estimation of divergence time is from refs. and .