Periodic Reporting for period 2 - RoyalMess (Evolutionary genomics of royalty in Messor hybridogenetic ants)
Reporting period: 2023-03-01 to 2024-08-31
The RoyalMess project aims to understand why some ant larvae can become nearly sterile individuals with short lifespan (the worker caste) while others can develop as large hyper-fertile individuals that can live up to 30 years (the queen caste). Royalty in social insects is typically environmentally acquired rather than genetically determined. However, this is not the case in an exceptional reproductive system, known as social hybridogenesis. Here, two distinct royal lineages of ants can only produce queens by their own while they need to hybridize to produce workers. Eggs with a pure royal genome are thus genetically fated to become queens while hybrid genomes are fated to become workers. Convergent evolution toward such a baroque reproductive strategy appears common in harvester ant species, but its origin is still completely mysterious. In this project, we plan to unravel the evolution of this unique system via cutting-edge genomic and molecular approaches.
1. Prevalence of social hybridogenesis: we will use genome-wide sequence data to identify novel occurrences of social hybridogenesis across hundred of ant species, in search for potential ecological determinants (e.g. climate or diet) that could favour evolution towards genetic caste determination.
2. History of royal lineages: we will use population genomics in three pairs of ant royal lineages to trace back their evolutionary origin. For this, we will develop new approaches to detect selection along royal lineage genomes in order to detect past hybridization events or fixation of caste-biasing alleles.
3. Identifying caste-determining genes: We will use comparative transcriptomics in early ant embryos to identify genes differentially expressed between castes before developmental divergence. Candidate genes will be experimentally validated via controlled matings or genome editing.
If successful, this project will enable the first genetic manipulation of ant royalty, deciphering how such an iconic example of phenotypic plasticity can become genetically hardwired. This might reveal how small genetic changes can trigger the most dramatic increase of fertility and longevity in the living world, which might open the door to future research for a better understanding of ageing. Overall, this research contributes to a broader understanding of evolutionary biology and the complex dynamics of eusociality. Ants in general and particularly harvester ants are considered as keystone species for ecosystems, as they participate to plant dispersion and organic material recycling. In the same time, many pest species are social insects, and cost a lot of resources to human societies. Understanding the reproductive systems of ants, their hybridization patterns and caste determination can thus provide valuable insights for either protecting their valuable ecosystem services or controlling their invasions.
1. Prevalence of social hybridogenesis: we will use genome-wide sequence data to identify novel occurrences of social hybridogenesis across hundred of ant species, in search for potential ecological determinants (e.g. climate or diet) that could favour evolution towards genetic caste determination.
2. History of royal lineages: we will use population genomics in three pairs of ant royal lineages to trace back their evolutionary origin. For this, we will develop new approaches to detect selection along royal lineage genomes in order to detect past hybridization events or fixation of caste-biasing alleles.
3. Identifying caste-determining genes: We will use comparative transcriptomics in early ant embryos to identify genes differentially expressed between castes before developmental divergence. Candidate genes will be experimentally validated via controlled matings or genome editing.
If successful, this project will enable the first genetic manipulation of ant royalty, deciphering how such an iconic example of phenotypic plasticity can become genetically hardwired. This might reveal how small genetic changes can trigger the most dramatic increase of fertility and longevity in the living world, which might open the door to future research for a better understanding of ageing. Overall, this research contributes to a broader understanding of evolutionary biology and the complex dynamics of eusociality. Ants in general and particularly harvester ants are considered as keystone species for ecosystems, as they participate to plant dispersion and organic material recycling. In the same time, many pest species are social insects, and cost a lot of resources to human societies. Understanding the reproductive systems of ants, their hybridization patterns and caste determination can thus provide valuable insights for either protecting their valuable ecosystem services or controlling their invasions.
The initial phase of the project has been dedicated to focus on a number of important tasks:
- Sampling taxon thanks to international collaborations, fieldworks, and visits of Museum collections
- Developing a theoretical model validating an evolutionary scenario for social hybridogenesis emergence
- Developing a method to detect a hybrid individual from a single genome
- Sequencing a population genomic dataset and a reference genome for a target species complex
- Sequencing genome-wide data from museum specimen and reconstruct a large phylogeny of the Messor genus
- Clarifying the reproductive system of some pairs of hybridogenetic lineages
- Sampling taxon thanks to international collaborations, fieldworks, and visits of Museum collections
- Developing a theoretical model validating an evolutionary scenario for social hybridogenesis emergence
- Developing a method to detect a hybrid individual from a single genome
- Sequencing a population genomic dataset and a reference genome for a target species complex
- Sequencing genome-wide data from museum specimen and reconstruct a large phylogeny of the Messor genus
- Clarifying the reproductive system of some pairs of hybridogenetic lineages
Our first study introduces a novel perspective by investigating the effects of hybridization on caste determination in an unique ecological setting where hybrid larvae develop into sterile workers. We have developed mathematical models that demonstrate an evolutionary arms race between nonhybrid larvae biased towards queen development and queens that increasingly hybridize to produce workers. This research has led to significant advancements in understanding the repeated evolution of remarkable reproductive systems, such as social hybridogenesis, observed in several ant species.
The second study presents a novel statistical method for detecting first generation hybrids from single-individual genome sequencing data. This innovative approach has enabled us to reveal the prevalence and distribution of current hybridization across various taxa, with Hymenoptera, and particularly ants, displaying the highest number of hybrid candidates. Our method has opened new avenues for large-scale genomic comparative studies of recent hybridization across whole taxa.
With these new approaches, we expect to discover novel unusual reproductive systems in ants.
The second study presents a novel statistical method for detecting first generation hybrids from single-individual genome sequencing data. This innovative approach has enabled us to reveal the prevalence and distribution of current hybridization across various taxa, with Hymenoptera, and particularly ants, displaying the highest number of hybrid candidates. Our method has opened new avenues for large-scale genomic comparative studies of recent hybridization across whole taxa.
With these new approaches, we expect to discover novel unusual reproductive systems in ants.