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Context-dependent autonomous self-fertilization yields reproductive assurance and mixed mating

Abstract

The evolution of self-fertilization in hermaphrodites is opposed by costs that decrease the value of self progeny relative to that of outcross progeny1,2,3. However, self-fertilization is common in plants4; 20% are highly selfing and 33% are intermediate between selfing and outcrossing5. Darwin6 proposed an adaptive benefit of self-pollination in providing reproductive assurance when outcrossing is impossible6,7,8,9. Moreover, if outcross pollen receipt is inconsistent within or between years, these conditions likewise favour self-pollination10, and this can result in a mixture of self and outcross seed production (mixed mating). Despite wide acceptance, the reproductive assurance hypothesis has lacked the support of complete empirical evidence to show that variable pollination can create both the ecological and genetic conditions favouring self-pollination. We recently showed in Collinsia verna that during periods of infrequent pollinator visits, autonomous self-pollination boosted seed output per flower11, the key ecological condition. Here we show low inbreeding depression and marker-based estimates of selfing, demonstrating that when the pollination environment in wild populations necessitates reproductive assurance, selfing rates increase. We provide a complete demonstration of reproductive assurance under variable pollination environments and mechanistically link reproductive assurance to intermediate selfing rates through mixed mating.

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Figure 1: Populations of the annual species, C. verna, have low values of inbreeding depression, δ.
Figure 2: Annual variation in selfing rates in C. verna populations results from an increase in autonomous self pollination when pollinators fail to visit flowers.

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Acknowledgements

We thank J. Dunn for technical assistance and J. Dunn, P. Zemrowski, A. Richter, C. Jarzab, H. Lang, R. Brown and A. Mergenthaler for field assistance. D.W. Schemske and S. J. Tonsor provided valuable comments on the manuscript. This work was supported by research grants from the National Science Foundation (USA) and the Research Development Fund of The University of Pittsburgh (S.K.).

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Correspondence to Susan Kalisz.

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Kalisz, S., Vogler, D. & Hanley, K. Context-dependent autonomous self-fertilization yields reproductive assurance and mixed mating. Nature 430, 884–887 (2004). https://doi.org/10.1038/nature02776

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