Rapid and repeatable genome evolution across three hybrid ant populations

Abstract

Hybridization is frequent in the wild but it is unclear whether admixture events lead to predictable outcomes and if so, at what timescale. We show that selection led to correlated sorting of genetic variation in less than 50 generations in three hybrid Formica aquilonia × F. polyctena ant populations. Removal of ancestry from the species with the lowest effective population size happened repeatedly in all populations, consistent with purging of deleterious load. This process was modulated by recombination rate variation and the density of functional sites. Moreover, haplotypes with signatures of positive selection in either species were more likely to fix in hybrids. These mechanisms led to mosaic genomes with comparable ancestry proportions. Our work demonstrates predictable evolution over short timescales after admixture in nature.

Extensive hybridisation between multiple differently adapted species may aid persistence in a changing climate

“…Hybridisation patterns are consistent with the mating strategies of the different species While hybridisation has been characterised previously in wood ants (Nouhaud et al, 2022;Purcell et al, 2016;Seifert, 2021;Seifert et al, 2010), our study is the first one to report genomic evidence of three-way hybridisation. The parental species have been reported to hybridise only in pairs of F. aquilonia × F. polyctena and F. polyctena × F. rufa.…”

“…In addition, morphological and allozyme data suggests several other hybrid findings between F. aquilonia and F. polyctena, mainly in southern Finland (Pamilo & Kulmuni, 2022; Seifert, 2021; Sorvari, 2022), and indications of F. aquilonia and F. lugubris hybridisation in northern Finland (Pamilo & Kulmuni, 2022). However, outside of F. aquilonia and F. polyctena (Nouhaud et al, 2022; Portinha et al, 2022) no genomic studies on the F. rufa group exist, and consequently no information on the congruence between morphological and genomic data is available.…”

Assembly of a Hybrid Formica aquilonia × F. polyctena Ant Genome From a Haploid Male

“…The genome and its annotation are both of sufficient quality for studies aiming to reconstruct speciation histories (e.g., Portinha et al 2022 ) and identify barrier loci or regions of adaptive introgression (e.g., Heliconius Genome Consortium 2012 ). It will also enable new approaches on the genomics of hybridization in this fascinating system ( Nouhaud et al 2020 , 2022 ). Finally, it also demonstrates that high-quality arthropod genomes can be assembled from single individuals using standard, cost-effective protocols.…”

“…In our case, using data from different individuals, short-read polishing could be impacted by samples having different ancestries at a given locus. However, the same hybrid population (Långholmen) was sampled both for assembly and polishing purposes, and local ancestries are correlated across individuals within a hybrid population ( Nouhaud et al 2022 ): it is then unlikely that 2 ancestries still segregate at the same locus in the population.…”

“…Two hybrid lineages coexist in a single population ( Kulmuni et al 2010 ), where introgression between lineages is sex specific but could be modulated by external factors ( Kulmuni et al 2020 ). This hybrid population is relatively young (estimated age <50 generations) and has evolved without any significant gene flow from either species since admixture ( Nouhaud et al 2022 ).…”