Purging Deleterious Mutations under Self Fertilization: Paradoxical Recovery in Fitness with Increasing Mutation Rate in Caenorhabditis elegans

Background: The accumulation of deleterious mutations can drastically reduce population mean fitness. Self-fertilization is thought to be an effective means of purging deleterious mutations. However, widespread linkage disequilibrium generated and maintained by self-fertilization is predicted to reduce the efficacy of purging when mutations are present at multiple loci. Methodology/Principal Findings: We tested the ability of self-fertilizing populations to purge deleterious mutations at multiple loci by exposing obligately self-fertilizing populations of Caenorhabditis elegans to a range of elevated mutation rates and found that mutations accumulated, as evidenced by a reduction in mean fitness, in each population. Therefore, purging in obligate selfing populations is overwhelmed by an increase in mutation rate. Surprisingly, we also found that obligate and predominantly self-fertilizing populations exposed to very high mutation rates exhibited consistently greater fitness than those subject to lesser increases in mutation rate, which contradicts the assumption that increases in mutation rate are negatively correlated with fitness. The high levels of genetic linkage inherent in self-fertilization could drive this fitness increase. Conclusions: Compensatory mutations can be more frequent under high mutation rates and may alleviate a portion of the fitness lost due to the accumulation of deleterious mutations through epistatic interactions with deleterious mutations. Th

Data from: The effects of Bacillus subtilis on Caenorhabditis elegans fitness after heat stress

Microbes can provide their hosts with protection from biotic and abiotic factors. While many studies have examined how certain bacteria can increase host lifespan, fewer studies have examined how host reproduction can be altered. The nematode Caenorhabditis elegans has been a particularly useful model system to examine how bacteria affect the fitness of their hosts under different contexts. Here, we examine how the bacterium Bacillus subtilis, compared to the standard C. elegans lab diet, Escherichia coli, affects C. elegans survival and reproduction after experiencing a period of intense heat stress. We find that under standard conditions, nematodes reared on B. subtilis produce fewer offspring than when reared on E. coli. However, despite greater mortality rates on B. subtilis after heat shock, young adult nematodes produced more offspring after heat shock when fed B. subtilis compared to E. coli. Because offspring production is necessary for host population growth and evolution, the reproductive advantage conferred by B. subtilis supersedes the survival advantage of E. coli. Furthermore, we found that nematodes must be reared on B. subtilis (particularly at the early stages of development) and not merely be exposed to the bacterium during heat shock, to obtain the reproductive benefits provided by B. subtilis. Taken together, our findings lend insight into the importance of environmental context and interaction timing in shaping the protective benefits conferred by a microbe toward its host

Experimental evolution as an underutilized tool for studying beneficial animal-microbe interactions

Microorganisms play a significant role in the evolution and functioning of the eukaryotes with which they interact. Much of our understanding of beneficial host-microbe interactions stems from studying already established associations; we often infer the genotypic and environmental conditions that led to the existing host-microbe relationships. However, several outstanding questions remain, including understanding how host and microbial (internal) traits, and ecological and evolutionary (external) processes, influence the origin of beneficial host-microbe associations. Experimental evolution has helped address a range of evolutionary and ecological questions across different model systems; however, it has been greatly underutilized as a tool to study beneficial host-microbe associations. In this review, we suggest ways in which experimental evolution can further our understanding of the proximate and ultimate mechanisms shaping mutualistic interactions between eukaryotic hosts and microbes. By tracking beneficial interactions under defined conditions or evolving novel associations among hosts and microbes with little prior evolutionary interaction, we can link specific genotypes to phenotypes that can be directly measured. Moreover, this approach will help address existing puzzles in beneficial symbiosis research: how symbioses evolve, how symbioses are maintained, and how both host and microbe influence their partner’s evolutionary trajectories. By bridging theoretical predictions and empirical tests, experimental evolution provides us with another approach to test hypotheses regarding the evolution of beneficial host-microbe associations

Data from: Turnover in local parasite populations temporarily favors host outcrossing over self-fertilization during experimental evolution

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

Data from: The effects of Bacillus subtilis on Caenorhabditis elegans fitness after heat stress

Microbes can provide their hosts with protection from biotic and abiotic factors. While many studies have examined how certain bacteria can increase host lifespan, fewer studies have examined how host reproduction can be altered. The nematode Caenorhabditis elegans has been a particularly useful model system to examine how bacteria affect the fitness of their hosts under different contexts. Here, we examine how the bacterium Bacillus subtilis, compared to the standard C. elegans lab diet, Escherichia coli, affects C. elegans survival and reproduction after experiencing a period of intense heat stress. We find that under standard conditions, nematodes reared on B. subtilis produce fewer offspring than when reared on E. coli. However, despite greater mortality rates on B. subtilis after heat shock, young adult nematodes produced more offspring after heat shock when fed B. subtilis compared to E. coli. Because offspring production is necessary for host population growth and evolution, the reproductive advantage conferred by B. subtilis supersedes the survival advantage of E. coli. Furthermore, we found that nematodes must be reared on B. subtilis (particularly at the early stages of development) and not merely be exposed to the bacterium during heat shock, to obtain the reproductive benefits provided by B. subtilis. Taken together, our findings lend insight into the importance of environmental context and interaction timing in shaping the protective benefits conferred by a microbe toward its host

Evolution of <i>Caenorhabditis elegans</i> host defense under selection by the bacterial parasite <i>Serratia marcescens</i>

<div><p>Parasites can impose strong selection on hosts. In response, some host populations have adapted via the evolution of defenses that prevent or impede infection by parasites. However, host populations have also evolved life history shifts that maximize host fitness despite infection. Outcrossing and self-fertilization can have contrasting effects on evolutionary trajectories of host populations. While selfing and outcrossing are known to affect the rate at which host populations adapt in response to parasites, these mating systems may also influence the specific traits that underlie adaptation to parasites. Here, we determined the role of evolved host defense versus altered life history,in mixed mating (selfing and outcrossing) and obligately outcrossing <i>C</i>. <i>elegans</i> host populations after experimental evolution with the bacterial parasite, <i>S</i>. <i>marcescens</i>. Similar to previous studies, we found that both mixed mating and obligately outcrossing host populations adapted to <i>S</i>. <i>marcescens</i> exposure, and that the obligately outcrossing populations exhibited the greatest rates of adaptation. Regardless of the host population mating system, exposure to parasites did not significantly alter reproductive timing or total fecundity over the course of experimental evolution. However, both mixed mating and obligately outcrossing host populations exhibited significantly reduced mortality rates in the presence of the parasite after experimental evolution. Therefore, adaptation in both the mixed mating and obligately outcrossing populations was driven, at least in part, by the evolution of increased host defense and not changes in host life history. Thus, the host mating system altered the rate of adaptation, but not the nature of adaptive change in the host populations.</p></div

ANOVA table for competitive fitness.

<p>ANOVA table for competitive fitness.</p

ANOVA table for mean lifetime fecundity.

<p>ANOVA table for mean lifetime fecundity.</p

Host lifetime fecundity.

<p>Lifetime fecundity was assessed in the absence of <i>S</i>. <i>marcescens</i> for Control, Evolution, and Ancestral populations in the (A) mixed mating populations and the (B) obligately outcrossing populations. Control populations exhibited greater levels of fecundity than the Ancestral and Evolution populations in obligately outcrossing populations, but no treatment differences were detected in the mixed mating populations.</p