If you are an INDONESIAN STUDENT, we proposed the following research project, please contact stefano.mona@ephe.psl.eu for more information

More information on the lpdp program 2026 (Panggilan Pendaftaran Beasiswa LPDP-France Program Doktor 2026 | Campus France)

To apply : send a CV, motivation letter, a copy of the Master Diplôma and a recommandation letter to stefano.mona@ephe.psl.eu before the 15th of June. 

The project will be conducted at the MNHN in Paris with field workd in Indonesia in collaboration with Purnama Hidayat, Professor of Entomology, Department of plant protection, IPB University (Bogor Agricultural University) in Indonesia (http://ipb.link/phidayat)

RESEARCH PROJECT

Abstract: Dispersal is a crucial trait of major importance for species survival. We recently identified a supergene system in the ant Myrmecina gramnicola guiding two traits related to dispersal: social (the number of queens in a colony) and wing (presence/absence) polymorphism. Using micro and macro-evolutionary analyses on a large dataset of whole genome sequences, we will dissect the genetic architecture of the two polymorphisms, gauging new evidence on the origin and maintenance of complex phenotypes.

Research unit hosting the doctoral student: Institut de Systématique, Evolution, Biodiversité (ISYEB), MNHN, 16 rue Buffon, Paris, France.

Laboratory description:

The ISYEB lab is a joint research center (UMR 7205) of CNRS, Muséum national d’Histoire naturelle, Sorbonne Université, Ecole Pratique des Hautes Etudes and Université des Antilles hosted in the prestigious Museum National d'Histoire Naturelle in Paris. 

The research center is a major hub of European systematics, making significant contributions to the fields of taxonomy and evolutionary biology using cutting-edge approaches in genomics and systematics. The laboratory has molecular biology facilities and technical help, which combined with advanced computational resources, provides an ideal framework for a PhD student. The laboratory offers a rich intellectual ecosystem where evolutionary questions are addressed across multiple scales—from genes to ecosystems.

Financial resources for sequencing are available thanks to funding from the ANR project SOGENANT. Supplementary funding can also be obtained from the MNHN.

Doctoral School: ED 472 de l’École Pratique des Hautes Études-PSL

Supergenes evolution: dissecting the origin of complex adaptive traits

Context and problematic:

Supergenes play an important role in the evolution of complex phenotypes, locking specific combinations of alleles (Schwander et al. 2014). Understanding the evolution of supergenes is essential for elucidating the mechanisms underlying adaptation, especially under variable environmental conditions, as these genomic architectures can promote the rapid emergence of complex and co-adapted phenotypes. Dispersal is a crucial and complex phenotypic trait of major importance for species survival (Clobert et al. 2012). While dispersal is inherently risky, failing to disperse can be equally detrimental especially under rapid environmental changes. Recent evidence suggests that some traits affecting dispersal may be controlled by supergenes (Matschiner et al. 2022). In ants, the female dispersal ability is associated with the social organization of colonies (the presence of single (monogyne) or multiple (polygyne) reproductive queens within colonies), a trait underpinned by a supergene in at least six lineages exhibiting this polymorphism (Chapuisat et al. 2013). These social supergenes show striking similarities with sex chromosomes. Both represent remarkable cases of convergent evolution (Kay et al. 2022) and antagonistic selection is thought to have played a major role in their origin (Scarparo et al. 2023). Indeed, in ants, when founding a new colony alone, the young queen generally disperse by flight and relies on its energetic reserves to raise the first workers (Peeters & Ito 2001). Conversely, the queens need less energetic reserves if they are adopted by an existing colony or if they found new colonies with the help of workers or other queens (Peeters & Ito 2001). In these cases, female dispersal is severely limited to the ant walking distance and costly traits associated with dispersal (e.g., wings or increased energy reserves) will be selected against. Producing queens with low energetic reserves for independent colony foundation would be very risky while producing large, winged queens would be wasteful if queens are readopted or found new colonies with the help of workers. Thus, in species harbouring both social and dispersal polymorphisms, antagonistic selection may promote the evolution of a genetic architecture linking these two traits. To investigate the evolution of the two traits, we recently conducted a population genomics analysis of the ant Myrmecina graminicola, in which a social polymorphism is coupled with the presence/absence of wings in queens (Mona et al. 2025). We discovered a new instance of a social supergene on chromosome 1 of the reference genome, characterized by three haplotypes (Mo, Ma, and Pa). Queen phenotypes observed in nature depends on the genotype at the social supergene: monogyne winged are MoMo, monogyne apterous MoMa, and polygyne apterous either MoPa or MaPa. The two haplotypes associated with aptery, namely Ma and Pa, carry an additional copy of the gene Awing probably involved in wing development as part of a ~116 kb insertion predating the origin of the social supergene (~20Mya vs. ~1Mya). The ancestral version of Awing is located in chromosome 4 at a short physical distance from another supergene (hereafter, FIGARO) coding for a yet unknown trait in M. graminicola. However, FIGARO is also present in the sister species M. nipponica, where it has captured the Awing genes. An association studies revealed that FIGARO indeed control wing polymorphism in M. nipponica, where conversely the social polymorphism is absent. These findings strongly suggest that despite the genetic architecture governing the wing polymorphism is different between the two species, there is a shared common basis and a deep evolutionary link with the social polymorphism.

Objectives and hypotheses

The aim of the PhD project is to understand the evolutionary history of the social and wing polymorphism and of their underlying genetic architecture in the genus Myrmecina using both micro and macro evolutionary approaches. This genus originated in Island South-East Asia (Steiner et al. 2006), with Indonesia representing its cradle. The variable occurrence of the two polymorphisms along the phylogeny of Myrmecina represent an excellent case study to investigate how complex traits evolved under supergenes control. Here we will start with five  species of the genus combining different states of the two traits: M. gopa, inhabiting the island of Java, with queens strictly polygynes and apterous (Ito 1996); M. graminicola, a palearctic species in which queens harbour both polymorphism but with spatial heterogeneity; M. sicula, the closest species to graminicola, but restricted to Sicily (Italy), in which preliminary analyses suggest that queens are all monogyne and apterous; M. nipponica, inhabiting Japan, and M. americana, restricted to the United States, where queens are monogynes but display the wing polymorphism. The species set could be extended by studying more Indonesian species thanks to the collaboration with Prof Purnama Hidayat, Bogor Agricultural University.  

The objectives of the project will be to:

i) Assess when and how polygyny and aptery, representing the derived states in ants, originated in the studied set of species. We will uncover the evolutionary relationships within the genus to determine a temporal framework of polymorphism’ evolution. We hypothesised that polygyny evolved independently in graminicola and gopa, while aptery is an ancestral polymorphism sharing similar genomic features.

ii) Characterise the genetic architecture underlying the two traits in the five species. To this end, we will investigate the synteny of both the social supergene and FIGARO in the studied lineages and contrast their evolutionary history with the species tree. Finally, we will look for signature of gene expansion of Awing and other candidate genes related to wing polymorphism recently identified in a RNA-seq experiment in graminicola. Our working hypothesis is that: a) social supergene is not highly syntenic between graminicola and gopa, but few genomic variants may be shared between the two species (similarly to Formica); b) FIGARO will have the opposite pattern, i.e., characterized by a large shared block, with few species-specific rearrangements; c) gene expansion of Awing (and possibly the other candidate genes) took different direction as the key feature determining the wing polymorphism is likely the number of copies, which could be variable even if coding the same phenotype.

 iii) Investigate how the two polymorphisms are maintained through time. Preliminary analysis of phenotypic and genotypic variation in both graminicola and nipponica suggest a spatial heterogeneity in the frequency distribution of the two polymorphisms. Here we will combine these observations with population level sequencing data recently obtained to test if the observed distribution is driven by neutrality of by specific environmental factors. Our hypothesis is that spatially heterogeneous selection is playing a key role in shaping the maintenance of the two polymorphisms. Pending funding acquisition, the same strategy will be adopted also in the other species available.

 Methodology

To meet our objectives, we will:

i)                         Build reference genomes for sicula, nipponica, americana, and gopa using a combination of long reads (PacBio Hi-fi or ONT Prometheon, depending on DNA quality) and Hi-C sequencing. Our team have now achieved strong experience in genome assembly, using a variety of assembler and scaffolding algorithm to achieve chromosome lever reference genomes.

ii)                       Resolve the phylogenetic species tree using phylogenomics pipeline (for example ASTRAL, Mirarab et al. 2014) which aim to reconstruct species trees from gene trees. This will be achieved focusing on BUSCO genes (Tegenfeldt et al. 2025). Constraining the molecular clock will also provide a temporal framework to the genus evolution.

iii)                    Social supergene and FIGARO of M. graminicola will be mapped on the new reference genome. Population genetics approaches will confirm the presence of the supergenes using a combination of population structure and linkage dis-equilibrium analysis (as in Mona et al. 2025). The same analyses conducted for genome wide BUSCO genes will be performed on BUSCO genes eventually present in the two supergenes, or in other orthologous genes (if not enough BUSCO will be found). These analyses will allow to contrast the species versus supergene tree, shading light on the mechanism leading to supergene formation and dynamics (expansion through strata, multiple inversions). Furthermore, degeneration will be investigated by computing the genomic load specific to each supergene haplotypes, which is expected to be higher in the derived ones. Finally, Awing copies will be searched in the different assembly using two strategies: 1)BLAST; 2) investigating the variation of depth of coverage (which should be higher if more copies of a gene are present but not integrated in the assembly). Phylogenetic and dating analyses will be performed on the orthologous copy. Topology weighting (Martin and Van Belleghem, 2017) will be also implemented to search for introgression (see for example the social supergene of Solenopsis invicta) or retention of ancestral polymorphisms (as in the social supergene of the genus Formica). The results within the two supergenes will be compared to genome-wide variation.

iv)                    Expand our current sampling of M. graminicola, which spans Italy and Northern Europe, to test for the presence of a latitudinal gradient in the distribution of both the social and the wing polymorphism (and so the social supergene haplotypes). Preliminary phenotypical observations suggest a strong difference in the distribution of the two polymorphisms between Italy and Northern Europe. The new samples will be analysed using a whole-genome resequencing approach (we currently have 160 individuals, which will be expanded to 250) Climatic variables will be obtained from freely available databases (e.g., WorldClim and CHELSA) and they will be correlated to the polymorphism distribution. Finally, historical demographic analyses, routinely implemented in our team, will be applied to determine whether the observed pattern at the social supergene is related to neutral (for example, post-glacial expansion) or selective processes (spatially variable selection).

Expected results

Three major general scientific advances are expected from this PhD project:

(i)                      Through the macro-evolutionary approach, we hope to demonstrate that supergenes have the remarkable ability to evolve independently and to “capture” additional genes during their evolution, thereby building new phenotypic combination. While the importance of supergenes in adaptation is now widely recognized, how they emerge and expand over times remain poorly understood. We hope our project will bring essential results revealing how genomic changes, especially genes coaptation, affect the expansion of supergenes. Finally, we expect to shed light on the mechanisms leading to evolutionary convergence of specific traits (typically, apterism).

(ii)                    Through the micro-evolutionary approach, we hope to reveal the importance of two main environmental variables of the Anthropocene (temperature and habitat isolation) on the evolution of key life-history traits linked to dispersal and social organisation. We expect that the difference in the distribution of social and wing polymorphism in graminicola is driven by selective rather than neutral processes, which will explain why they can be maintained over deep evolutionary times.

(iii)                 Finally, we will possibly resolve an old debate concerning ants’ evolution. The prevailing view is that changes in social behaviour precede the loss of dispersal traits, such as the presence of wings. Leveraging the geographical variation of the two polymorphisms in M. graminicola, as well as the coexistence of winged and apterous monogyne queens, we expect our results to challenge this paradigm and pinpoint the evolution of dispersal polymorphism as a first step for the evolution of social tolerance (polygyny). Macro-evolutionary results will also contribute with molecular dating to distinguish between the two hypotheses. Indeed, using macro and micro-evolutionary approaches, will strengthen our conclusion on when and how the social polymorphism evolved and whether its evolution led to the loss of wing polymorphism.

Provisional timetable

 Year 1:  Producing reference genomes and samples acquisition for micro-evolutionary inferences. Bioinformatics on short read sequencing (intra-specific samples). Manuscript on the new genomes (a genomic note).

Year 2:  Phylogenomics analyses, mapping, topology weighting. Manuscript preparation on the comparative genomics.

Year 3: Micro-evolutionary studies (historical demography and correlation with climatic variables). Manuscript preparation on intra-specific analysis and synthesis. Preparation of the phd manuscript.

Desired profile: We are looking for a student with a particular interest in genomics, informatics and multidisciplinary research.

References

·        Chapuisat, M. (2023). Supergenes as drivers of ant evolution. Myrmecological News 33. 1-18. https://doi.org/10.25849/myrmecol.news_033:001

·        Clobert, J., and others (eds), (2013) Dispersal Ecology and Evolution (Oxford, 2012; online edn, Oxford Academic, 17 Dec. 2013), https://doi.org/10.1093/acprof:oso/9780199608898.001.0001,

·        Ito, F. (1996) Colony Characteristics of the Indonesian Myrmicine Ant Myrmecina sp. (Hymenoptera, Formicidae, Myrmicinae): Polygynous Reproduction by Ergatoid Queens. Annals of the Entomological Society of America 89:550–554. https://doi.org/10.1093/aesa/89.4.550

·        Kay, T., Helleu, Q., and Keller, L. (2022). Iterative evolution of supergene-based social polymorphism in ants. Phil. Trans. R. Soc. B 377, 20210196. https://doi.org/10.1098/rstb.2021.0196.

·        Martin, S.H., and Van Belleghem S.M. (2017) Exploring Evolutionary Relationships Across the Genome Using Topology Weighting. Genetics. 206(1):429-438. doi: 10.1534/genetics.116.194720.

·        Matschiner, M., Barth, J.M.I., Tørresen, O.K., Star, B., Baalsrud, H.T., Brieuc, M.S.O., Pampoulie, C., Bradbury, I., Jakobsen, K.S., and Jentoft, S. (2022). Supergene origin and maintenance in Atlantic cod.Nat Ecol Evol 17;6(4):469–481. doi: 10.1038/s41559-022-01661-x.

·        Mirarab, S., Reaz, R., Bayzid, Md.S., Zimmermann, T., Swenson, M.S., and Warnow, T. (2014) ASTRAL: genome-scale coalescent-based species tree estimation, Bioinformatics, Volume 30, Issue 17, September 2014, Pages i541–i548, https://doi.org/10.1093/bioinformatics/btu462

·        Mona, S., Gay, E.J., Taupenot, A., Ducancel, J., Laso-Jadart, R., Helleu, Q., Chifflet-Belle, P., Teodori, E., Aury, J.M., Xiong, Z., Schrader, L., Vizueta, J., Molet, M., and Doums, C. (2025) Genomic evidence of a complex supergene system linking dispersal to social polymorphism. Curr Biol. 2025 15;35(24):6155-6162.e5. doi: 10.1016/j.cub.2025.10.065

·        Peeters, C., and Ito, F. (2001). Colony Dispersal and the Evolution of Queen Morphology in Social Hymenoptera. Annual Review of Entomology 46, 601–630. https://doi.org/10.1146/annurev.ento.46.1.601.

·        Scarparo, G., Palanchon, M., Brelsford, A., and Purcell, J. (2023). Social antagonism facilitates supergene expansion in ants. Current Biology, S0960982223014501. https://doi.org/10.1016/j.cub.2023.10.049.

·        Schwander, T., Libbrecht, R., and Keller, L. (2014). Supergenes and Complex Phenotypes. Current Biology 24, R288–R294. https://doi.org/10.1016/j.cub.2014.01.056.

·        Steiner, F., Schlick-Steiner, B., Konrad, H., Linksvayer, T., Quek, S-P., Christian, E., Stauffer, C., and Buschinger, A. (2006). Phylogeny and evolutionary history of queen polymorphic Myrmecina ants (Hymenoptera: Formicidae). European Journal of Entomology. 103. 619-626. 10.14411/eje.2006.083.

·        Tegenfeldt, F., Kuznetsov, D., Manni, M., Berkeley, M., Zdobnov, E.M., and Kriventseva E.V. (2025) OrthoDB and BUSCO update: annotation of orthologs with wider sampling of genomes.  Nucleic Acids Research, Volume 53, Issue D1, 6 January 2025, Pages D516–D522, https://doi.org/10.1093/nar/gkae987