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 males, 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 organisms. Two competing explanations for the widespread prevalence of outcrossing in nature despite this inherent disadvantage are the avoidance of inbreeding depression generated by selfing and the ability of outcrossing populations to adapt more rapidly to environmental change. 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.

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

a, Experimental populations (N2, triangles; CB4856, squares) with different outcrossing rates were exposed to a novel, challenging environment at either natural (solid lines) or elevated (4×; dashed lines) mutation rates for 50 generations. Percent change in population mean fitness over time was assessed by comparing the competitive fitness of the ancestral population to that of the evolved population. Obligately selfing populations showed pronounced fitness decline in the face of elevated mutation rates (or even natural mutation rates in the case of CB4856). Both the rate of adaptation and resistance to mutational degradation increased with increasing levels of outcrossing. b, Within the wildtype outcrossing treatments, populations exposed to elevated mutation rates evolved higher outcrossing rates. c, Experimental populations with a CB4856 background were mutated to generate genetic variation and then exposed to either the bacterial pathogen S. marcescens (dashed lines) or heat-killed S. marcescens control (sold lines) for forty generations, then percent change in mean fitness measured for each population. The outcrossing populations exhibited both rapid and substantial adaptation to the pathogen, however, the obligate selfing populations failed to adapt. d, Populations exposed to S. marcescens evolved higher outcrossing rates within the wildtype outcrossing treatment. Thus, in keeping with theory, both the influx of deleterious mutations and adaptation to a novel environment favor outcrossing over selfing. Error bars represent two standard errors of the mean (errors calculated on arcsine-square-root transformed data for b and d).