Abstract

The ubiquity of outcrossing in plants and animals is difficult to explain given its costs relative to self‐fertilization. Despite these costs, exposure to changing environmental conditions can temporarily favor outcrossing over selfing. Therefore, recurring episodes of environmental change are predicted to favor the maintenance of outcrossing. Studies of host–parasite coevolution have provided strong support for this hypothesis. However, it is unclear whether multiple exposures to novel parasite genotypes in the absence of coevolution are sufficient to favor outcrossing. Using the nematode Caenorhabditis elegans and the bacterial parasite Serratia marcescens, we studied host responses to parasite turnover. We passaged several replicates of a host population that was well‐adapted to the S. marcescens strain Sm2170 with either Sm2170 or one of three novel S. marcescens strains, each derived from Sm2170, for 18 generations. We found that hosts exposed to novel parasites maintained higher outcrossing rates than hosts exposed to Sm2170. Nonetheless, host outcrossing rates declined over time against all but the most virulent novel parasite strain. Hosts exposed to the most virulent novel strain exhibited increased outcrossing rates for approximately 12 generations, but did not maintain elevated levels of outcrossing throughout the experiment. Thus, parasite turnover can transiently increase host outcrossing. These results suggest that recurring episodes of parasite turnover have the potential to favor the maintenance of host outcrossing. However, such maintenance may require frequent exposure to novel virulent parasites, rapid rates of parasite turnover, and substantial host gene flow.

Highlights

  • One of the central mysteries in evolutionary biology is the overwhelming prevalence of sexual reproduction via outcrossing in plant and animal species

  • To study the effects of parasite turnover on host adaptation and outcrossing rates, we passaged replicate C. elegans populations that had previously adapted to the S. marcescens strain Sm2170 with three novel parasite strains and Sm2170 for 18 generations

  • Host populations passaged with the most virulent novel parasite strain, ES1, exhibited the highest outcrossing rates throughout the experiment (Figure 2; Table 1) and their outcrossing rates increased significantly over the first 12 generations, an effect that was not observed in any other treatment (Table 2)

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Summary

| INTRODUCTION

One of the central mysteries in evolutionary biology is the overwhelming prevalence of sexual reproduction via outcrossing in plant and animal species. | 6653 beneficial mutations into genotypes that confer high levels of fitness, but they may break apart locally adapted genotypes (Hill & Robertson, 1966) These opposing effects may combine to favor sex and recombination if offspring from local × migrant crosses have higher average fitness than offspring from local × local and migrant × migrant crosses (Agrawal, 2009; Otto, 2009). Production of sexual offspring declined throughout the experiment in all treatments, suggesting that selective pressures in the experiment were insufficient to favor the long-­term maintenance of high levels of sex. Long-­term maintenance of high levels of sex and recombination may require frequently changing environmental conditions that impose strong selective pressures on local populations. We measured outcrossing rates every six generations to test whether higher levels of outcrossing would be favored as host populations adapted to novel parasite strains. We tested whether host resistance to the original parasite strain (Sm2170) would decrease as host populations adapted to the novel parasite strains, which would indicate cross-­ resistance trade-­offs

| MATERIALS AND METHODS
| DISCUSSION
Findings
CONFLICT OF INTEREST
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