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Low seed fertility of hermaphrodites is maintained in a gynodioecious species throughout the distribution range in Japan

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Abstract

Dioecy, the separation of sex at the individual level, evolved in angiosperms from hermaphroditic ancestors. One of the postulated evolutionary pathways is by way of the gynodioecious stage, i.e., the coexistence of female and hermaphroditic individuals. In a morphologically gynodioecious species, Daphne jezoensis., seed fertility in hermaphrodites is limited compared to that of females, indicating that its sexual system is close to dioecy. The aim of this study was to clarify whether the gynodioecy in this species is a stable sexual system or a transitional state leading to dioecy. We evaluated variations in the degree of pollen limitation, sexual and mating systems, floral morphology, sex ratio, and the genetic structure of 14 populations across the species’ distribution range in Japan. Sexual systems were similar among populations throughout the distribution range although the southernmost populations had unique genetic structures to some extent. Hermaphrodites were commonly self-compatible, but their fruiting capacity was low in every population. This suggests that gynodioecy composed of females and hermaphrodites having low seed fertility is a consistent sexual system in D. jezoensis. Low seed fertility in hermaphrodites throughout the distribution range suggests that this sexual system is not necessarily a transitional state from gynodioecy to dioecy if occasional seed production in hermaphrodites has any advantage. One possible ecological advantage for the maintenance of hermaphrodites is that seed production by autonomous self-pollination may be beneficial in the colonization process after long-distance seed dispersal.

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Availability of data and material

The datasets used in the current study are available from the corresponding author on reasonable request.

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Acknowledgements

We thank all members of the Plant Ecology Lab of the Graduate School of Environmental Science, Hokkaido University, for their kind assistance in the fieldwork and helpful discussions on this study. We appreciate the following persons for their help with the permission procedure and their practical supports for the field survey: K. Narita, N. Nakamura, K. Horie, I. Honda, M. Masuda, and M. Tada. We would like to thank Editage (www.editage.com) for English editing.

Funding

This study was supported by JSPS KAKENHI (19J10583, 18H02504).

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Authors

Contributions

A.S. and G.K. designed the study, and collected and analyzed the data. Y.K. developed microsatellite markers. A.S. wrote the first draft of the manuscript and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

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Correspondence to Akari Shibata.

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The authors declare that they have no conflict of interest.

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Handling editor: Martin A. Lysak.

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Supplementary Information

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Information on Electronic Supplementary Material

Online Resource 1. Mean fruit number in females (F) and hermaphrodites (H) and relative fruit number in F to H under open pollination and outcross pollination conditions.

Online Resource 2. The number of flowers used for floral measurements.

Online Resource 3. Sequences for newly developed primer pairs.

Online Resource 4. Relationships between the degree of pollen limitation and fruit-set rate of hermaphrodites, selfing rate of hermaphrodites, allelic richness, and FIS.

Online Resource 5. Unrooted neighbor-joining tree using Cavalli-Sforza and Edwards’ chord distances among 14 Daphne jezoensis populations.

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Shibata, A., Kameyama, Y. & Kudo, G. Low seed fertility of hermaphrodites is maintained in a gynodioecious species throughout the distribution range in Japan. Plant Syst Evol 307, 55 (2021). https://doi.org/10.1007/s00606-021-01780-1

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  • DOI: https://doi.org/10.1007/s00606-021-01780-1

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