Coevolutionary interactions with parasites constrain the spread of self-fertilization into outcrossing host populations

Abstract

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 (nonevolving) 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.

Keywords: Breeding system; Red Queen hypothesis; coevolution; evolution; host-parasite coevolution; sex.

Figure 1

A conceptual diagram depicting all of the possible reproductive combinations that can occur between different genotypes of males, females, and hermaphrodites in our experiment, and the expected frequencies of sexes and genotypes in the offspring that would result from each of these possible crosses. The expected frequencies of sexes and genotypes in the offspring of selfing hermaphrodites include males which are produced by nondisjunction of the X chromosome during meiosis (Brenner 1974). Our figure depicts males produced at a nondisjunction rate of 0.0015 (panels D and H). 95% of the individuals in our generation zero host populations were obligately outcrossing males and females which were homozygous for the obligate-outcrossing allele, designated as “o” in the figure. 5% of the individuals in our generation zero host populations were homozygous for the mixed-mating allele (designated as ‘m’ in the figure). Almost all of the mixed-mating homozygotes at the start of our experiment were hermaphrodites, although there may also have been rare males homozygous for the mixed-mating allele. Because mixed-mating hermaphrodites can mate with males carrying the obligate-outcrossing allele (panels E, F, I, and J), and because obligately outcrossing females can mate with males carrying the mixed-mating allele (panels B and C), the mixed-mating and obligately outcrossing breeding systems could freely mix in our experimental populations. The mixed-mating allele is dominant, so hermaphrodites heterozygous at the fog-2 locus (i.e. hermaphrodites with the ‘m/o’ genotype) were capable of both self-fertilization (panel D) and outcrossing (panels E, F, and G).

Figure 2

Mean selfing rates (± one standard error) over the course of the experiment. Host populations were exposed to three different treatments: control (heat-killed S. marcescens; dotted line and triangular markers), fixed-parasite treatment (fixed strain of S. marcescens; dashed line and circle markers), copassaged (copassaged S. marcescens; solid line and square markers) for 33 generations.

Figure 3

A bivariate plot showing the frequency of individuals with mixed-mating genotypes (i.e. the frequency of individuals with genotypes that permit both outcrossing and selfing) plotted against selfing rates for 12 host populations at generation 33 (our experimental endpoint).