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.

Fig. 1. Hypothetical and empirical species and supergene phylogenetic trees.

a–d A simplified species tree (a), and hypothetical scenarios for the evolutionary history of the supergene (b–d). b SB and Sb supergene variants diverged (star) in the common ancestor of S. invicta and S. richteri; the supergene is thus a trans-species polymorphism. c Sb evolved twice from SB, representing independent origins (stars) after the separation of the two species. d Sb diverged in S. invicta and spread to S. richteri through introgression (arrows). e Empirical coalescent-based trees of 368 Solenopsis samples based on 1631 single-gene trees from chromosomes 1–15 (left; species tree) and 97 single-gene trees from the supergene region of chromosome 16 (right; supergene tree). Branches shorter than 0.05 were collapsed into polytomies. A tanglegram (middle) indicates the relative positions of each sample in both trees. Circled numbers highlight patterns consistent with introgression of Sb from S. invicta/macdonaghi into other species. On either side of the tanglegram black bars indicate where samples with the Sb genotype can be found in the two trees. Support values (ASTRAL bootstrap support | local posterior probability) are provided for key nodes of speciation and supergene differentiation.