Dataset Information

The Integral Role of Genetic Variation in the Evolution of Outcrossing in the Caenorhabditis elegans-Serratia marcescens Host-Parasite System.

ABSTRACT: 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.

SUBMITTER: Parrish RC

PROVIDER: S-EPMC4847799 | biostudies-literature | 2016

REPOSITORIES: biostudies-literature

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The Integral Role of Genetic Variation in the Evolution of Outcrossing in the Caenorhabditis elegans-Serratia marcescens Host-Parasite System.

Parrish Raymond C RC Penley McKenna J MJ Morran Levi T LT

PloS one 20160427 4

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 t ...[more]

PMID: 27119159

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Project description:BackgroundWhy most organisms reproduce via outcrossing rather than selfing is a central question in evolutionary biology. It has long ago been suggested that outcrossing is favoured when it facilitates adaptation to novel environments. We have previously shown that the experimental evolution of increased outcrossing rates in populations of the male-hermaphrodite nematode Caenorhabditis elegans were correlated with the experimental evolution of increased male fitness. However, it is unknown whether outcrossing led to adaptation, and if so, which fitness components can explain the observed increase in outcrossing rates.ResultsUsing experimental evolution in six populations with initially low standing levels of genetic diversity, we show with head-to-head competition assays that population-wide fitness improved during 100 generations. Since outcrossing rates increased during the same period, this result demonstrates that outcrossing is adaptive. We also show that there was little evolution of hermaphrodite fitness under conditions of selfing or under conditions of outcrossing with unrelated tester males. We nonetheless find a positive genetic correlation between hermaphrodite self-fitness and population-wide fitness, and a negative genetic correlation between hermaphrodite mating success and population-wide fitness. These results suggest that the several hermaphrodite traits measured are fitness components. Tradeoffs expressed in hermaphrodites, particularly noticed between self-fitness and mating success, may in turn explain their lack of change during experimental evolution.ConclusionsOur findings indicate that outcrossing facilitates adaptation to novel environments. They further indicate that the experimental evolution of increased outcrossing rates depended little on hermaphrodites because of fitness tradeoffs between selfing and outcrossing. Instead, the evolution of increased outcrossing rates appears to have resulted from unhindered selection on males.

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.

Dataset Information

The Integral Role of Genetic Variation in the Evolution of Outcrossing in the Caenorhabditis elegans-Serratia marcescens Host-Parasite System.

Publications

The Integral Role of Genetic Variation in the Evolution of Outcrossing in the Caenorhabditis elegans-Serratia marcescens Host-Parasite System.

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