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Genomic incompatibilities are persistent barriers when speciation happens with gene flow in Formica ants
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Genomic incompatibilities are persistent barriers when speciation happens with gene flow in Formica ants

Patrick Heidbreder, Noora Poikela, Pierre Nouhaud, Tuomas Puukko, Konrad Lohse et Jonna Kulmuni
Molecular Biology and Evolution, Vol.43(5)
11/03/2026
PMCID: PMC13143019
PMID: 41810521

Résumé

evolutionary genetics and genomics barrier loci Bateson-Dobzhansky-Muller incompatibility (BDMI) network demographic modeling speciation evolutionary biology demogenetic model demogenetic modeling demogenetic modelling population dynamics population development demographic change taxa genetic hybridization interspecific hybridization gene flow haplotype diversity frequency analysis genetic divergence coding sequence transposon mobile element jumping gene transposable element regulation of gene expression gene expression regulation gene regulation reproductive barrier evolutionary genetics evolutionary genomics ant Formicidae population genomic data demographic analysis history of a biological invasion history of biological invasion
A current goal of speciation research is identifying loci underlying reproductive barriers between species. Locating barrier loci in population genomic data is difficult due to the often-complex demographic history of diverged taxa and heterogeneity in evolutionary forces across the genome. We take advantage of natural hybridization between two wood ant species (Formica aquilonia and F. polyctena) to identify regions of reduced long-term gene flow using demographically explicit scans of non-admixed genomes. In addition, we identify candidate Bateson-Dobzhansky-Muller incompatibilities (BDMIs) through an imbalanced recombinant haplotype frequency analysis using a large sample of natural F. aquilonia × F. polyctena hybrid genomes. These approaches find barriers and BDMIs scattered across the genome. Furthermore, BDMIs significantly overlap with long-term barriers, indicating that some BDMIs have persisted despite divergence with gene flow. Intriguingly, the number of pairwise interactions a BDMI has correlates with its long-term barrier strength: hub-like BDMIs with many interactions reduce gene flow more effectively. Finally, we find that long-term barriers are depleted for both coding sequences (CDS) and transposable elements (TEs), while candidate BDMIs are associated with snRNAs and LTR transposons, specifically Ty1-copia. In contrast, regions where long-term barriers and BDMIs co-locate are significantly associated with introns but not CDS or TEs, implying a potential role of alternative splicing or gene regulation in long-term incompatibilities. Our results highlight the underappreciated impact of BDMI connectivity on the persistence of reproductive barriers over time.

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