Recurring adaptive introgression of a supergene variant that determines social organization

Abstract

Introgression has been proposed as an essential source of adaptive genetic variation. However, a key barrier to adaptive introgression is that recombination can break down combinations of alleles that underpin many traits. This barrier might be overcome in supergene regions, where suppressed recombination leads to joint inheritance across many loci. Here, we study the evolution of a large supergene region that determines a major social and ecological trait in Solenopsis fire ants: whether colonies have one queen or multiple queens. Using coalescent-based phylogenies built from the genomes of 365 haploid fire ant males, we show that the supergene variant responsible for multiple-queen colonies evolved in one species and repeatedly spread to other species through introgressive hybridization. This finding highlights how supergene architecture can enable a complex adaptive phenotype to recurrently permeate species boundaries.

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

“… 32 concluded that the supergene probably arose in S. richteri and introgressed into S. invicta , while ref. 29 concluded, from an analysis including more species, that the supergene evolved in S. invicta/S. macdonaghi (note that the authors incorrectly labeled samples of S. AdRX as S. macdonaghi in this paper).…”

“…For example, the vast majority of the genes (87 out of 97) analyzed by ref. 29 are localized on In(16)1 ( SI Appendix , Table S7 ). Thus, this study effectively reconstructed the evolutionary history of the largest inversion [ In(16)1 ], which our analyses indeed revealed to be a (moderately supported) sister group to the SB haplotypes of S. AdRX and S. invicta .…”

“…Reconstructing the evolutionary history of supergene evolution is essential to understanding how such remarkable genomic elements originate and, possibly, the sequence of incorporation of key phenotypic elements into complex traits. The socially polymorphic species are hypothesized to have diverged from the outgroup species S. saevissima and Solenopsis metallica , ∼0.75 to 1.75 million y ago and then radiated within the past ∼500,000 y ( 22 , 29 ). While a single origin of the Sb haplotype is robustly supported ( 30 , 31 ), it remains unclear whether this unique element originated in the ancestral population before the radiation, or whether it has invaded the known socially polymorphic species through introgression events ( 22 , 29 , 32 ).…”

“…The socially polymorphic species are hypothesized to have diverged from the outgroup species S. saevissima and Solenopsis metallica , ∼0.75 to 1.75 million y ago and then radiated within the past ∼500,000 y ( 22 , 29 ). While a single origin of the Sb haplotype is robustly supported ( 30 , 31 ), it remains unclear whether this unique element originated in the ancestral population before the radiation, or whether it has invaded the known socially polymorphic species through introgression events ( 22 , 29 , 32 ). Multiple studies have documented recent hybridization involving three of the socially polymorphic Solenopsis species in both the native and introduced ranges ( 33 – 37 ), highlighting a demographic context conducive to such genomic invasion in at least some cases.…”

A simple conceptual framework and nomenclature for studying repeated, parallel and convergent evolution

“…De novo mutation can happen repeatedly (Konečná et al, 2021;Fulgione et al, 2022), especially in hotspots of adaptive variation, as discussed above (Xie et al, 2019). Repeated events of gene flow have also been shown (Jones et al, 2018;Giska et al, 2019;Stolle et al, 2022), and there can be a repeated recruitment of standing genetic variation in di erent lineages (Lai et al, 2019;Konečná et al, 2021). This, once again, highlights the need of coherent language.…”