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Mutation load and rapid adaptation favour outcrossing over self-fertilization

Abstract

The tendency of organisms to reproduce by cross-fertilization despite numerous disadvantages relative to self-fertilization is one of the oldest puzzles in evolutionary biology. For many species, the primary obstacle to the evolution of outcrossing is the cost of production of males1, individuals that do not directly contribute offspring and thus diminish the long-term reproductive output of a lineage. Self-fertilizing (‘selfing’) organisms do not incur the cost of males and therefore should possess at least a twofold numerical advantage over most outcrossing organisms2. Two competing explanations for the widespread prevalence of outcrossing in nature despite this inherent disadvantage are the avoidance of inbreeding depression generated by selfing3,4,5 and the ability of outcrossing populations to adapt more rapidly to environmental change1,6,7. Here we show that outcrossing is favoured in populations of Caenorhabditis elegans subject to experimental evolution both under conditions of increased mutation rate and during adaptation to a novel environment. In general, fitness increased with increasing rates of outcrossing. Thus, each of the standard explanations for the maintenance of outcrossing are correct, and it is likely that outcrossing is the predominant mode of reproduction in most species because it is favoured under ecological conditions that are ubiquitous in natural environments.

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Figure 1: Experimental test of the major theories of the evolution of outcrossing.

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Acknowledgements

We thank S. Scholz, A. Ohdera and J. Chiem for logistical help, S. Katz for providing the S. marcescens 2170 strain, and J. Thornton for use of laboratory space and equipment. We also thank B. Cresko, C. Lively, J. Thornton and the members of the Phillips and Cresko laboratories for comments and discussion pertaining to this work. Funding was provided by NSF grants DEB-0236180, DEB-0710386 and DEB-0641066, and an NIH Genetics Fellowship awarded to L.T.M. Some nematode strains used in this work were provided by the Caenorhabditis Genetics Center, which is funded by the NIH National Center for Research Resources (NCRR).

Author Contributions L.T.M. and P.C.P. designed the experiments. L.T.M. and M.D.P. performed the experiments. L.T.M. and P.C.P. analysed the data. L.T.M. and P.C.P. wrote the paper.

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Correspondence to Patrick C. Phillips.

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This file contains Supplementary Methods, Supplementary Table S1, Supplementary References and Supplementary Figures S1-S2 with Legends. (PDF 1362 kb)

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Morran, L., Parmenter, M. & Phillips, P. Mutation load and rapid adaptation favour outcrossing over self-fertilization. Nature 462, 350–352 (2009). https://doi.org/10.1038/nature08496

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