Social organization and dispersal: the dual role of a supergene in ants – SOGENANT

A difficulty in understanding the maintenance of supergenes lies in obtaining a picture as complete as possible of the selective forces at play. In most model systems, behavioural experiments are barely feasible, preventing researchers from getting crucial parameters of the system. Moreover, behavioural and ecological approaches are often performed separately from genomic analyses by different research teams, being not necessarily conducted on the same populations and preventing a proper integration of all results. Our project will overcome these difficulties by (i) focusing on a manipulable small ant species with small colonies for which mating can be obtained in the laboratory and (ii) proposing an integrative approach combining expertise in genomics, population genetics, chemical ecology, behavioural ecology and spatial ecology.

Our first paper published in Current Biology (https://doi.org/10.1016/j.cub.2025.10.065) described our discovery of a new ‘‘social supergene’’ of ∼20 Mb with three haplotypes. Supergene genotypes determine the three queen phenotypes observed in nature: monogyne winged, monogyne apterous, and polygyne apterous. The two haplotypes associated with aptery carry a ∼116 kb insertion containing an additional copy of a gene probably involved in wing development. Interestingly, the presence/absence of this insertion predated the origin of the social supergene (∼20 vs. ∼1 mya). Syntenic analyses showcased an independent evolution of the social supergene. The screening of workers’ genotypes within colonies of a population in Fontainebleau suggested that assortative mating and segregation distortion may play a role in preserving supergene polymorphism. This unique supergene system illustrates the theoretically expected genetic link between social polymorphism and dispersal in ants. Its modular evolution mirrors the role of sexually antagonistic selection in the origin of sex chromosomes.

We are currently generating high-quality genome assemblies for each haplotype of the social supergene in M. graminicola, as well as for closely related species. This will allow us to reconstruct the deeper evolutionary history of the supergene and characterize the origin and evolutionary dynamics of the insertion associated with it.

In parallel, we are conducting an ecological survey of supergene haplotypes across natural populations to assess the extent of spatially varying selection. We are also investigating patterns of transmission ratio distortion to determine whether deviations from Mendelian inheritance contribute to the maintenance and spread of the supergene.

Finally, we are performing behavioral assays and chemical analysis to test whether social genotype influences worker behavior thereby linking genomic variation to social behaviors.

Supergenes are groups of neighbouring genes inherited as a single Mendelian element. They play a central role in the evolution of complex phenotypes. New case studies are essential to understand their evolution and maintenance in the face of rapid human-induced environmental changes. In six ant genera, a supergene determines the number of queens, a fascinating social polymorphism also affecting dispersal abilities. This social polymorphism is associated to chemical, morphological and behavioural variation both at the individual and colony levels. In the two genera in which it has been well studied, the supergene shows a different evolutionary trajectory and various mechanisms maintaining its polymorphism. Recently, our team has discovered a novel social supergene in the ant species Myrmecina graminicola accompanied by another (smaller) supergene determining wing polymorphism (presence or absence of wings in the queen). This unique and original system of supergenes offers a great opportunity to shed light on the intricated multilevel effects of supergenes combining selfish and cooperative effects and on the powerful role of supergenes as drivers of adaptation, especially through their effects on dispersal. The aim of our project is therefore to combine genomics, ecological, behavioural and chemical approaches to better characterize the evolutionary history of these supergenes and the maintenance of their associated polymorphisms in the ant genus Myrmecina. Our project addresses two main questions: (i) How do these supergenes evolve at a deep evolutionary scale? and (ii) Which mechanisms act on the maintenance of the supergene polymorphism?
To answer to these questions, our project is structured into 4 work-packages (WP). WP1 aims to unravel the evolution of the supergenes by (i) shedding light on their genomic architecture and (ii) assessing their demographic history in M. graminicola; (iii) searching for the supergenes in closely related species to infer their deep evolutionary history. WP2 aims at investigating the phenotypic effects of the supergenes on (i) the sociogenetic organisation of the colonies; (ii) the differential effect of supergene haplotypes on offspring survival at different developmental stages leading to distortion to Mendelian segregation (TRD); (iii) the relative success of the morphs by indirect morphological measurements correlated with queen fecundity and colony foundation success and (iv) the effect of the social environment (supergene haplotype frequencies in workers) on colony success and TRD. WP3 will investigate the importance of spatially heterogeneous selection and of mating patterns on the maintenance of supergene polymorphisms. To do so, we will (i) test the hypothesis that habitat fragmentation (size and distance between patches of favourable habitat) drives the maintenance of supergenes polymorphism; (ii) characterize the fine scale population genetic structure to test the effect of habitat fragmentation on dispersal and evaluate the differential dispersal abilities of the queen morphs and (iii) assess the pattern of non-random mating. Finally, WP4 will integrate our results into an eco-evolutionary model mimicking the genetic determinism of the supergenes. This model will extend a previous model by our team which tested the effect of fragmentation on the evolution of dispersal.
By studying a new supergene system, our project will provide insights into the generality and specificity of the mechanisms underlying supergene evolution and maintenance. By focusing on a manipulable small ant species and proposing an integrative approach combining the expertise in genomic and population genetics, chemical, ecology and behavioural ecology of three Parisian partners having a long-lasting experience in working together (ISYEB; iEES-Paris; LEEC), we believe that our project will generate fundamental advances on supergenes as drivers of complex adaptation.