Recurring adaptive introgression of a supergene variant that determines social organization

Eckart Stolle,Rodrigo Pracana,Claudia Castillo-Carrillo,Federico López-Osorio,Yannick Wurm,Gabriel Luis Hernández,Martin Bollazzi,Carolina Ivon Paris,Maria Cristina Arias,Anurag Priyam,Marian K Priebe

doi:10.1038/s41467-022-28806-7

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.

Highlights

Introgression has been proposed as an essential source of adaptive genetic variation
Our findings contradict previous suggestions that the Sb supergene variant evolved in a common ancestor of S. invicta and S. richteri[18] or within S. richteri[20]
We focused on singlecopy genes, which allowed us to avoid complex genealogies and potential genotyping artifacts caused by read mis-mapping of copy-number variants of genes and repetitive elements; such variation is common in the degenerating Sb variant of the social chromosome[14,17,21,26]

Summary

Introduction

Introgression has been proposed as an essential source of adaptive genetic variation. 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. Close relatives of S. invicta are socially dimorphic and carry the same social supergene system[17–19] This supergene system could be a trans-species polymorphism that evolved in the common ancestor of these species[17–19], or even a set of polymorphisms that originated independently in each species, it is possible that its spread[17,18,20] was instead mediated by introgressive hybridization. Using coalescent-based phylogenies, we show that the supergene system originated in S. invicta and spread to different species through the introgression of the Sb variant of the supergene

Methods

Results

Conclusion