The social supergene dates back to the speciation time of two Solenopsis fire ant species

Pnina Cohen,Eyal Privman

doi:10.1038/s41598-020-67999-z

Abstract

Colony social organization of multiple Solenopsis fire ant species is determined by a supergene with two haplotypes SB and Sb, which are similar to X/Y sex chromosomes. The ancestral monogyne (single-queen) social form has been associated with homozygous SB/SB queens, while queens in colonies with the derived polygyne (multi-queen) social structure are heterozygous SB/Sb. By comparing 14 Solenopsis invicta genomes and the outgroup S. fugax, we dated the formation of the supergene to 1.1 (0.7–1.6) million years ago, much older than previous estimates, and close to the estimated time of speciation of the two socially polymorphic species S. invicta and S. richteri. We also used 12 S. invicta and S. richteri genomes to compare the evolutionary distances between these species and the distances between the social haplotypes, and found them to be similar. A phylogenetic analysis suggested that the monophyletic Sb clade is more closely related to S. richteri SB haplotypes than to S. invicta SB haplotypes. We conclude that the formation of the supergene occurred concomitantly with the process of speciation of the Solenopsis socially-polymorphic clade, and hypothesize that the Sb variant first arouse in one incipiently-speciating population and then introgressed into the other populations or species.

Highlights

Many ant species are socially polymorphic, displaying multiple alternative social structures
While it seems reasonable to assume that the divergence of the SB and Sb variants predates the divergence of the species in the Solenopsis socially-polymorphic clade, it is possible that historic admixture carried the polygyne variant across species boundaries
Aligning social chromosome haplotypes of RAD sequenced S. invicta and S. richteri. This analysis was based on Restriction site Associated DNA sequencing (RAD-seq) data of S. invicta and S. richteri populations samples from Argentina, which we described in Cohen and P rivman[25]

Summary

Introduction

Many ant species are socially polymorphic, displaying multiple alternative social structures. While it seems reasonable to assume that the divergence of the SB and Sb variants predates the divergence of the species in the Solenopsis socially-polymorphic clade, it is possible that historic admixture carried the polygyne variant across species boundaries. Such an event may have been driven by adaptive introgression as Scientific Reports | (2020) 10:11538. This observation is a stark contrast with the prevalent hybridization that is taking place in their introduced range of South-Eastern U SA26,27 At odds with this evidence, the divergence of the two social variants was dated to 390,000 (95% confidence level 350,000–420,000) years ago, much later than S. invicta and S. richteri ‘s estimated speciation time. This dating was calibrated by the divergence time of two species of leafcutter ants[17], which were the most closely related species to the Solenopsis clade for which genomic sequences were available at the time

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Discussion

Conclusion