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Evolution of Caenorhabditis elegans host defense under selection by the bacterial parasite Serratia marcescens.

ABSTRACT: 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 C. elegans host populations after experimental evolution with the bacterial parasite, S. marcescens. Similar to previous studies, we found that both mixed mating and obligately outcrossing host populations adapted to S. marcescens 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.

SUBMITTER: Penley MJ

PROVIDER: S-EPMC5549931 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BackgroundAdaptation to a stressor can lead to costs on other traits. These costs play an unavoidable role on fitness and influence the evolutionary trajectory of a population. Host defense seems highly subject to these costs, possibly because its maintenance is energetically costly but essential to the survival. When assessing the ecological risk related to pollution, it is therefore relevant to consider these costs to evaluate the evolutionary consequences of stressors on populations. However, to the best of our knowledge, the effects of evolution in irradiate environment on host defense have never been studied. Using an experimental evolution approach, we analyzed fitness across 20 transfers (about 20 generations) in Caenorhabditis elegans populations exposed to 0, 1.4, and 50.0 mGy.h- 1 of 137Cs gamma radiation. Then, populations from transfer 17 were placed in the same environmental conditions without irradiation (i.e., common garden) for about 10 generations before being exposed to the bacterial parasite Serratia marcescens and their survival was estimated to study host defense. Finally, we studied the presence of an evolutionary trade-off between fitness of irradiated populations and host defense.ResultsWe found a lower fitness in both irradiated treatments compared to the control ones, but fitness increased over time in the 50.0 mGy.h- 1, suggesting a local adaptation of the populations. Then, the survival rate of C. elegans to S. marcescens was lower for common garden populations that had previously evolved under both irradiation treatments, indicating that evolution in gamma-irradiated environment had a cost on host defense of C. elegans. Furthermore, we showed a trade-off between standardized fitness at the end of the multigenerational experiment and survival of C. elegans to S. marcescens in the control treatment, but a positive correlation between the two traits for the two irradiated treatments. These results indicate that among irradiated populations, those most sensitive to ionizing radiation are also the most susceptible to the pathogen. On the other hand, other irradiated populations appear to have evolved cross-resistance to both stress factors.ConclusionsOur study shows that adaptation to an environmental stressor can be associated with an evolutionary cost when a new stressor appears, even several generations after the end of the first stressor. Among irradiated populations, we observed an evolution of resistance to ionizing radiation, which also appeared to provide an advantage against the pathogen. On the other hand, some of the irradiated populations seemed to accumulate sensitivities to stressors. This work provides a new argument to show the importance of considering evolutionary changes in ecotoxicology and for ecological risk assessment.

Project description:Ongoing investigations into the interactions between microbial communities and their associated hosts are changing how emerging diseases are perceived and ameliorated. Of the numerous host-microbiome-disease systems of study, the emergence of chytridiomycosis (caused by Batrachochytrium dendrobatidis, hereafter Bd) has been implicated in ongoing declines and extinction events of amphibians worldwide. Interestingly, there has been differential survival among amphibians in resisting Bd infection and subsequent disease. One factor thought to contribute to this resistance is the host-associated cutaneous microbiota. This has raised the possibility of using genetically modified probiotics to restructure the host-associated microbiota for desired anti-fungal outcomes. Here, we use a previously described strain of Serratia marcescens (Sm) for the manipulation of amphibian cutaneous microbiota. Sm was genetically altered to have a dysfunctional pathway for the production of the extracellular metabolite prodigiosin. This genetically altered strain (Δpig) and the functional prodigiosin producing strain (wild-type, WT) were compared for their microbial community and anti-Bd effects both in vitro and in vivo. In vitro, Bd growth was significantly repressed in the presence of prodigiosin. In vivo, the inoculation of both Sm strains was shown to significantly influence amphibian microbiota diversity with the Δpig-Sm treatment showing increasing alpha diversity, and the WT-Sm having no temporal effect on diversity. Differences were also seen in host mortality with Δpig-Sm treatments exhibiting significantly decreased survival probability when compared with WT-Sm in the presence of Bd. These results are an important proof-of-concept for linking the use of genetically modified probiotic bacteria to host microbial community structure and disease outcomes, which in the future may provide a way to ameliorate disease and address critical frontiers in disease and microbial ecology.

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Evolution of Caenorhabditis elegans host defense under selection by the bacterial parasite Serratia marcescens.

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