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.

Adaptive introgression of a visual preference gene

“…Hybridization has been suggested to be an important source of genetic variation on which selection can act, including during behavioral evolution ( 36 , 37 ), but direct links between specific causal genes and behavioral phenotypes are lacking. Our results strongly suggest that H. timareta acquired a regucalcin1 allele by hybridizing with its closely related comimic H. melpomene , increasing attraction toward red females and presumably reproductive success.…”

An old inversion polymorphism involving giant mobile elements in an invasive fungal pathogen

“…In conclusion, we provide strong evidence for the existence of a non-recombining region partially linked to the mating-type locus and maintained by selection in the chestnut blight fungus C. parasitica . Such supergenes are increasingly reported in a variety of organisms thanks to new sequencing technologies ( 2 , 10 , 56 , 57 , 64 ). This study therefore contributes to our understanding of how selection for recombination suppression promotes the maintenance of two divergent haplotypes despite degeneration.…”

“…in Europe could also have resulted from introgression from a closely related species. The evolution of supergenes by introgression has been reported for example in ants and butterflies (56)(57)(58). However, we found little evidence for an introgression: i) the two haplotypes are present in the CL2 cluster of invasive European populations directly originating from Asia, ii) the MAT-Prox1 haplotype in the CL1 cluster more differentiated from the MAT-Prox2 haplotype than in the CL2 cluster is genetically close to an Asian haplotype, iii) footprints of recombination suppression are present in the native range in terms of degeneration and particular genomic structure in the MAT-Proximal region, and iv) we found no signatures of introgression from closely related species in gene genealogies.…”

Greenbeards in plants?

“…The multiplication of supergene discoveries in recent years suggests that such strong association between co‐segregating loci might not be as uncommon as previously thought, including in plants (e.g. Joron et al ., 2011; Li et al ., 2016; Helleu et al ., 2022). In many cases, co‐segregation results from chromosomal rearrangements that suppress recombination between the different genes (Gutiérrez‐Valencia et al ., 2021).…”