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Strength and variability of postmating reproductive isolating barriers between four European white oak species

Abstract

The identification and quantification of the relative importance of reproductive isolating barriers is of fundamental importance to understand species maintenance in the face of interspecific gene flow between hybridising species. Yet, such assessments require extensive experimental fertilisations that are particularly difficult when dealing with more than two hybridising and long-generation-time species such as oaks. Here, we quantify the relative contribution of four postmating reproductive isolating barriers consisting of two prezygotic barriers (gametic incompatibility, conspecific pollen precedence) and two postzygotic barriers (germination rate, early survival) from extensively controlled pollinations between four oak species (Quercus robur, Quercus petraea, Quercus pubescens and Quercus pyrenaica) that have been shown to frequently hybridise in natural populations. We found high variation in the strength of total reproductive isolation between species, ranging from total reproductive isolation to advantage toward hybrid formation. As previously found, Q. robur pollen was unable to fertilise Q. petraea due to a strong reproductive isolating mechanism. On the contrary, Q. pubescens pollen was more efficient at fertilising Q. petraea than conspecific pollen. Overall, prezygotic barriers contribute far more than postzygotic barriers to isolate species reproductively, suggesting a role for reinforcement in the development of prezygotic barriers. Conspecific pollen precedence reduced hybrid formation when pollen competition was allowed; however, presence of conspecific pollen did not totally prevent hybridization. Our results suggest that pollen competition depends on multiple ecological and environmental parameters, including species local abundance, and that it may be of uppermost importance to understand interspecific gene flow among natural multispecies populations.

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Acknowledgments

We would like to thank E. Bertocchi and the Unité Expérimentale de l’Hermitage (UE0570, INRA Bordeaux Aquitaine), in particular O. Lagardère, for their help during the experimentation. We are grateful to R. Petit and P Garnier-Géré for discussions during this project. We thank P. Léger, V. léger, P-Y. Dumolin and F. Salin for technical assistance in the lab. We thank S. Aitken (associate editor) and two anonymous reviewers for their suggestions that improved the manuscript. Genotyping presented in this publication was performed at the Genome-Transcriptome facility of Bordeaux (grants from the Conseil Régional d'Aquitaine no. 20030304002FA and no. 20040305003FA and from the European Union, FEDER no. 2003227). OL was supported by a Ph.D. grant from the Ministère de l'Éducation Nationale, de l'Enseignement Supérieur et de la Recherche.

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The authors declare that they have no conflict of interest.

Ethical standards

The experiments presented in this manuscript comply with the current law of the country in which they were performed.

Data Archiving Statement

Data use in this manuscript will be made publicly available though DRYAD.

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Correspondence to O. Lepais.

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Communicated by S. Aitken

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Lepais, O., Roussel, G., Hubert, F. et al. Strength and variability of postmating reproductive isolating barriers between four European white oak species. Tree Genetics & Genomes 9, 841–853 (2013). https://doi.org/10.1007/s11295-013-0602-3

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  • DOI: https://doi.org/10.1007/s11295-013-0602-3

Keywords

  • Reproductive isolation
  • Controlled crosses
  • Pollen competition
  • Reinforcement
  • Hybridization
  • Quercus