Multiple mating in the context of interspecific hybridization between two Tetramorium ant species

Abstract

In eusocial Hymenoptera, haplodiploidy and polyandry may facilitate selection for hybridization. Interspecific hybridization is widespread in ants and can lead to hybrid inviability as well as the formation of new species through hybrid speciation. However, in ants, polyandry is uncommon. By analyzing microsatellite markers on 15 ant workers per colony, we show that the mating system of 28 pure colonies of Tetramorium immigrans, 15 pure colonies of Tetramorium caespitum, and 27 hybrid colonies is a monogyne/polyandrous mating system, with a higher mating rate in T. caespitum (mean = 2.4 males vs. 1.7 in T. immigrans). Hybrid queens, but no hybrid fathers, were deduced from workers’ genotypes, in accordance with Haldane’s rule extended to haplodiploid organisms, which states that the haploid sex should more often be sterile or inviable. In five colonies, hybridization and multiple mating allowed the simultaneous production of both hybrid and nonhybrid offspring. Although rare, these situations hinted at asymmetrical, larger contributions of T. immigrans vs. T. caespitum males to offspring production. Together, these findings point toward a complex and dynamic mating system in T. immigrans and T. caespitum, and contribute to better understand interspecific hybridization mechanisms and their consequences on genetic and taxonomic diversity. The study of polyandry within a hybrid zone is unprecedented and opens new opportunities to better understand interspecific hybridization mechanisms and their short- to long-term consequences.

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Fig. 1: Map of the study area.
Fig. 2: Top—barplot obtained from STRUCTURE Bayesian clustering based on the 1008 worker genotypes and the 198 reconstructed genotypes of parents (68 females and 130 males).
Fig. 3: Illustration of the situations observed in the 15 backcrossed colonies.
Fig. 4: Observed number of mating (Kobs) in each pure species (T. caespitum and T. immigrans) and for each area (North, Center, and South) in the hybrid zone.
Fig. 5: Offspring contribution of each male in the five mixed colonies where females mated with both conspecific and heterospecific males.

Data availability

Data are available from the Dryad Digital Repository: https://datadryad.org/stash/dataset/doi:10.5061/dryad.qjq2bvqcb.

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Acknowledgements

This study was funded by the Conseil Départemental de l’Isère. It was also supported by the French National Research Agency (ANR) through the LABEX IMU (ANR-10-LABX-0088) of Université de Lyon, within the program “Investissements d’Avenir” (ANR-11-IDEX-0007). We also thank temporary lab assistants, E. Vernay, M. Reina, L. Herpe, M. Dumet, and C. Richalet, for their invaluable help.

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Correspondence to Marion Cordonnier.

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Cordonnier, M., Escarguel, G., Dumet, A. et al. Multiple mating in the context of interspecific hybridization between two Tetramorium ant species. Heredity 124, 675–684 (2020). https://doi.org/10.1038/s41437-020-0310-3

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