Most organisms reproduce through outcrossing, even though it comes with significant costs. The Red Queen hypothesis proposes that selection from coevolving pathogens facilitates the persistence of outcrossing in spite of these costs. We utilized experimental coevolution to test the Red Queen hypothesis, and found that coevolution with a bacterial pathogen (Serratia marcescens) resulted in significantly more outcrossing in mixed mating experimental populations of the nematode Caenorhabditis elegans. Furthermore, we found that coevolution with the pathogen rapidly drove obligately selfing populations to extinction, while outcrossing populations persisted through reciprocal coevolution. Thus, consistent with the Red Queen hypothesis, coevolving pathogens can select for biparental sex.

Given the cost of sex, outcrossing populations should be susceptible to invasion and replacement by self-fertilization or parthenogenesis. However, biparental sex is common in nature, suggesting that cross-fertilization has substantial short-term benefits. The Red Queen hypothesis (RQH) suggests that coevolution with parasites can generate persistent selection favoring both recombination and outcrossing in host populations. We tested the prediction that coevolving parasites can constrain the spread of self-fertilization relative to outcrossing. We introduced wild-type Caenorhabditis elegans hermaphrodites, capable of both self-fertilization and outcrossing, into C. elegans populations that were fixed for a mutant allele conferring obligate outcrossing. Replicate C. elegans populations were exposed to the parasite Serratia marcescens for 33 generations under three treatments: a control (avirulent) parasite treatment, a fixed (non-evolving) parasite treatment, and a copassaged (potentially coevolving) parasite treatment. Self-fertilization rapidly invaded C. elegans host populations in the control and the fixed-parasite treatments, but remained rare throughout the entire experiment in the copassaged treatment. Further, the frequency of the wild-type allele (which permits selfing) was strongly positively correlated with the frequency of self-fertilization across host populations at the end of the experiment. Hence, consistent with the RQH, coevolving parasites can limit the spread of self-fertilization in outcrossing populations.

Host-parasite interactions can drive rapid, reciprocal genetic changes (coevolution), provided both hosts and parasites have high heritabilities for resistance/infectivity. Similarly, the host’s mating system should also affect the rate of coevolutionary change in host-parasite interactions. Using experimental coevolution, we determined the effect of obligate outcrossing verses partial self-fertilization (mixed mating) on the rate of evolutionary change in a nematode host (Caenorhabditis elegans) and its bacterial parasite (Serratia marcescens). Bacterial populations were derived from a common ancestor. We measured the effects of host mating system on host adaptation to the parasite. We then determined the extent of parasite adaptation to their local host populations. Obligately outcrossing hosts exhibited more rapid adaptation to parasites than did mixed mating hosts. In addition, most of the parasites became adapted to infecting their “local” hosts; but parasites from obligately outcrossing hosts showed a greater level of local adaptation. These results suggest that host populations evolved along separate trajectories, and that outcrossing host populations diverged further than partially selfing populations. Finally, parasites “tracking” outcrossing host populations diverged further than parasites tracking the partially selfing host populations. These results show that the evolutionary trajectories of both hosts and parasites can be shaped by the host’s mating system.

Cross-fertilization is predicted to facilitate the short-term response and the long-term persistence of host populations engaged in antagonistic coevolutionary interactions. Consistent with this idea, our previous work has shown that coevolving bacterial pathogens (Serratia marcescens) can drive obligately selfing hosts (Caenorhabditis elegans) to extinction, while the obligately outcrossing and partially outcrossing populations persisted. We focused the present study on the partially outcrossing (mixed mating) and obligately outcrossing hosts, and analyzed the changes in the host resistance/avoidance (and pathogen infectivity) over time. We found that host mortality rates increased in the mixed mating populations over the first ten generations of coevolution when outcrossing rates were initially low. However, mortality rates decreased after elevated outcrossing rates evolved during the experiment. In contrast, host mortality rates decreased in the obligately outcrossing populations during the first ten generations of coevolution, and remained low throughout the experiment. Therefore, predominant selfing reduced the ability of the hosts to respond to coevolving pathogens compared to outcrossing hosts. Thus, we found that host-pathogen coevolution can generate rapid evolutionary change, and that host mating system can influence the outcome of coevolution at a fine temporal scale.

Outcrossing is predicted to facilitate more rapid adaptation than self-fertilization as a result of genetic exchange between genetically variable individuals. Such genetic exchange may increase the efficacy of selection by breaking down Hill-Robertson interference, as well as promoting the maintenance of within-lineage genetic diversity. Experimental studies have demonstrated the selective advantage of outcrossing in novel environments. Here, we assess the specific role of genetic variation in the evolution of outcrossing. We experimentally evolved genetically variable and inbred populations of mixed mating (outcrossing and self-fertilizing) Caenorhabditis elegans nematodes under novel ecological conditions—specifically the presence of the virulent parasite Serratia marcescens. Outcrossing rates increased in genetically variable host populations evolved in the presence of the parasite, whereas parasite exposure in inbred populations resulted in reduced rates of host outcrossing. The host populations with genetic variation also exhibited increased fitness in the presence of the parasite over eight generations, whereas inbred populations did not. This increase in fitness was primarily the result of adaptation to the parasite, rather than recovery from initial inbreeding depression. Therefore, the benefits of outcrossing were only manifested in the presence of genetic variation, and outcrossing was favored over self-fertilization as a result. As predicted, the benefits of outcrossing under novel ecological conditions are a product of genetic exchange between genetically diverse lineages.