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Widespread coexistence of self-compatible and self-incompatible phenotypes in a diallelic self-incompatibility system in Ligustrum vulgare (Oleaceae)

Abstract

The breakdown of self-incompatibility (SI) in angiosperms is one of the most commonly observed evolutionary transitions. While multiple examples of SI breakdown have been documented in natural populations, there is strikingly little evidence of stable within-population polymorphism with both inbreeding (self-compatible) and outcrossing (self-incompatible) individuals. This absence of breeding system polymorphism corroborates theoretical expectations that predict that in/outbreeding polymorphism is possible only under very restricted conditions. However, theory also predicts that a diallelic sporophytic SI system should facilitate the maintenance of such polymorphism. We tested this prediction by studying the breeding system of Ligustrum vulgare L., an insect-pollinated hermaphroditic species of the Oleaceae family. Using stigma tests with controlled pollination and paternity assignment of open-pollinated progenies, we confirmed the existence of two self-incompatibility groups in this species. We also demonstrated the occurrence of self-compatible individuals in different populations of Western Europe arising from a mutation affecting the functioning of the pollen component of SI. Our results show that the observed low frequency of self-compatible individuals in natural populations is compatible with theoretical predictions only if inbreeding depression is very high.

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Fig. 1: Ligustrum vulgare geographic species range across Europe and position of the seven studied natural populations.
Fig. 2: Illustration of the different compatibility relationships observed using stigma tests in Ligustrum vulgare.
Fig. 3: Diagram representing all pollination events detected by paternity analysis in the experimental garden.
Fig. 4: Predicted inbreeding depression and prior selfing rate consistent with the estimated observed frequencies of the self-compatible (SC) phenotype in natural populations of Ligustrum vulgare.

Data availability

Data for this study (results of the stigma tests performed on the plants in the experimental garden, multilocus microsatellite genotypes of all adults from the experimental population, along with multilocus microsatellite genotypes of 1209 offspring collected on ten mother plants) are available from the Dryad Digital Repository: https://doi.org/10.5061/dryad.pvmcvdnmb.

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Acknowledgements

We thank Nathalie Faure, Eric Schmitt, and Cédric Glorieux for support in caring for the plants at the University of Lille greenhouse (Plateforme serre, cultures et terrains expérimentaux). We are very grateful to Géraldine Coste and Sandrine Descave from the Cevennes Natural Park for facilitating access to individuals in natural sites at the optimal time in regard to their phenology. We thank John Pannell, Vincent Castric, and Xavier Vekemans for scientific discussions and helpful comments on the paper, as well as both anonymous referees for their constructive input. This research is a contribution to the CPER research project CLIMIBIO. The authors thank the French Ministry for Higher Education and Research, the Hauts-de-France Regional Council and the European Regional Development Fund for their financial support for this project.

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Correspondence to Isabelle De Cauwer.

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De Cauwer, I., Vernet, P., Billiard, S. et al. Widespread coexistence of self-compatible and self-incompatible phenotypes in a diallelic self-incompatibility system in Ligustrum vulgare (Oleaceae). Heredity 127, 384–392 (2021). https://doi.org/10.1038/s41437-021-00463-4

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