Mots-Clés

Supergene, population genomics, evolutionary history

Description

Supergenes play a major role in the evolution of complex phenotypes as revealed by the increased use of population genomic studies in diverse taxa. By locking a set of genes determining complex adaptive phenotypes and by being inherited as a single block due to the (partial) suppression of recombination, they avoid the production of intermediate, less-fit, phenotypes. They are responsible for some spectacular polymorphisms such as male and female sexes, mimetic morphs in butterflies, mating-type in fungi or colony social organization in ants. The social polymorphism in ants consists in the occurrence of two very distinct morphs within a species/population linked with many colonial and individual traits, with colonies headed either by a single queen (monogynous) or by multiple queens (polygynous). This polymorphism occurs in around 15 % of ant species and to date it has been shown to be controlled by a supergene in five ant lineages (Chapuisat 2023), showing striking similarities with sexual chromosomes. In our group, we recently investigated the ant species M. graminicola, in which three types of colonies are known: polygynous colonies, always headed by more than one apterous reproductive queens, and monogynous colonies headed either by a single winged dealated (after her mating flight) reproductive queen or by an apterous queen. By whole genome sequencing 24 queens belonging to the three morphs, we found two supergenes controlling for the two traits (sociality and presence/absence of wings), which despite lying in two separated scaffolds of the reference genome, shows strong signature of linkage disequilibrium, supporting recent claim about the importance of social antagonistic selection in supergene evolution (Scarparo et al. 2023). However, we found another supergene (hereafter referred as the third supergene), not yet associated to any phenotypic traits, on the same scaffold of the supergene governing wings’ presence. Preliminary comparative genomic analyses suggests that this supergene is partially syntenic to both the supergene controlling sex-ratio (the ability of a colony to produce exclusively queens or males) and the queens’ size in the genus Formica. Interestingly, M. graminicola displays both the sex-ratio polymorphism and a queens’ size polymorphism but the genetic determinant of these traits needs yet to be proven.

RESEARCH PROPOSAL/OBJECTIVES:

The aim of this project is to investigate the evolutionary history of the third supergene. In parallel, we are setting up experiments to determine the association between individuals’ genotype at this supergene and both sex-ratio and queen size, but this will not be part of this internship. Here we will use genomic data to focus on three questions: 1) date the origin of the third supergene; 2) compare the gene tree at the third supergene against the species tree using genome wide data from M. graminicola and two sister species (M. nipponica and M. sicula); 3) investigate the presence of the third supergene in several ant species using genomic data available either from collaborators or from the literature. Investigating the evolutionary dynamics of this supergene will not only provide new clues on its function but it will also expand our knowledge concerning general models of supergenes’ evolution (antagonistic selection, recruitment or loss of new genes by time, dynamics of the nested inversions).

DESCRIPTION OF DATA if applicable (Data must be available before the start of the internship):

First, we have produced HiFi long reads and HiC data from a male of M. graminicola to assemble a new quality reference genome. The assembly is almost finished, we are at the manual curation step. We then recently sequenced 64 unrelated queens sampled in the Fontainebleau Forest, 7 workers (we have not yet found nests) of M. sicula, and 32 queens from M. nipponica. Before the starting of the internship (January 2025) we will most likely expand our datasets adding more nipponica and sicula individuals and produce RNAseq data for a better genome annotation (we already have one produced by the GAGA ant genome consortium) to characterize genes within the third supergene. Whenever new data production will take more time then expected, this will not compromise the internship. We have also already collected genome-wide population datasets of the following species: 365 males from 7 Solenopsis species, 22 queens from Monomorium pharensis, 16 from Themnothorax rugulatus, in addition to individuals from Vollenhovia emeryi and 2 species of Messor.

METHODOLOGIES:

• Task 1: dating the origin of the supergene is traditionally challenging. We will be using coalescent based methods such as the PSMC (Li and Durbin 2011) and explicit modelling of divergence between individuals homozygous for both alleles (for example, using the fastsimcoal framework, Excoffier et al. 2021)
• Task2: we will compare species tree vs gene tree at the third supergene. This will be realised either with clustering methods (sNMF, PCA, etc) and phylogenetic reconstruction (for example, tree-based analyses on BUSCO genes, and merging of these genes using approaches such as ASTRAL, Mirabab et al. 2014). These analyses will be used to compare graminicola, nipponica, and sicula.
• Task3: the third supergene will be aligned to target species (i.e., Solenopsis etc.) to identify candidate syntenic regions. Then, population samples will be used to detect the presence of a supergene (PCA, LD based analyses etc). These analyses will allow to determine the evolutionary dynamics of the third supergene and eventually provide new hints on his function. We will finally analyse the gene/other functional elements shared between these species.

REFERENCES (max. 5):

• Chapuisat, M. (2023). Supergenes as drivers of ant evolution. Myrmecological News 33.
• Li, H., and Durbin, R. (2011). Inference of human population history from individual whole-genome sequences. Nature 475, 493–496. 10.1038/nature10231.
• Scarparo, G., Palanchon, M., Brelsford, A., and Purcell, J. (2023). Social antagonism facilitates supergene expansion in ants. Current Biology, S0960982223014501. 10.1016/j.cub.2023.10.049.
• L. Excoffier, N. Marchi, D. A. Marques, R. Matthey-Doret, A. Gouy, V. C. Sousa, Fastsimcoal2: Demographic inference under complex evolutionary scenarios. Bioinformatics 37, 4882–4885 (2021).
• S. Mirarab, R. Reaz, Md. S. Bayzid, T. Zimmermann, M. S. Swenson and T. Warnow (2014) ASTRAL: genome-scale coalescent-based species tree estimation. Bioinformatics, 30:i541–i548.