Increased responsiveness in feeding behaviour of<i>Caenorhabditis elegans</i>after experimental coevolution with its microparasite<i>Bacillus thuringiensis</i>

Schulte, Rebecca D.; Hasert, Barbara; Makus, Carsten; Michiels, Nico K.; Schulenburg, Hinrich

doi:10.1098/rsbl.2011.0684

Cited by 14 publications

(12 citation statements)

References 21 publications

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“…The interaction between C. elegans and B. thuringiensis was established as a model for experimental evolution, to study the dynamics of host–pathogen coevolution. Using genetically diverse host populations, C. elegans was shown in three fully independent evolution experiments to be able to adapt rapidly and in a highly specific manner to the continuously evolving pathogen challenge ( Schulte et al 2010 , 2011 , 2012 , Masri et al 2013 , 2015 ; H. Schulenburg, unpublished data). At the same time, B. thuringiensis adapted to the host in a similarly specific manner ( Schulte et al 2010 , 2011 ; Masri et al 2015 ), apparently through changes in the copy number of a toxin-encoding plasmid and possibly also additional virulence factors ( Masri et al 2015 ).…”

Section: Pathogens and Parasitesmentioning

confidence: 99%

The Natural Biotic Environment ofCaenorhabditis elegans

2017

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Organisms evolve in response to their natural environment. Consideration of natural ecological parameters are thus of key importance for our understanding of an organism’s biology. Curiously, the natural ecology of the model species Caenorhabditis elegans has long been neglected, even though this nematode has become one of the most intensively studied models in biological research. This lack of interest changed ∼10 yr ago. Since then, an increasing number of studies have focused on the nematode’s natural ecology. Yet many unknowns still remain. Here, we provide an overview of the currently available information on the natural environment of C. elegans. We focus on the biotic environment, which is usually less predictable and thus can create high selective constraints that are likely to have had a strong impact on C. elegans evolution. This nematode is particularly abundant in microbe-rich environments, especially rotting plant matter such as decomposing fruits and stems. In this environment, it is part of a complex interaction network, which is particularly shaped by a species-rich microbial community. These microbes can be food, part of a beneficial gut microbiome, parasites and pathogens, and possibly competitors. C. elegans is additionally confronted with predators; it interacts with vector organisms that facilitate dispersal to new habitats, and also with competitors for similar food environments, including competitors from congeneric and also the same species. Full appreciation of this nematode’s biology warrants further exploration of its natural environment and subsequent integration of this information into the well-established laboratory-based research approaches.

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Section: Pathogens and Parasitesmentioning

confidence: 99%

The Natural Biotic Environment ofCaenorhabditis elegans

2017

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“…This model previously allowed us to obtain experimental evidence for the manifold consequences of host–parasite coevolution, including reciprocal changes in parasite virulence and host defence, reciprocal life‐history trade‐offs, reciprocal increases in evolutionary rates and genetic diversity and an increase in local adaptation (Schulte et al . , , ).…”

Section: Introductionmentioning

confidence: 99%

Sex differences in host defence interfere with parasite‐mediated selection for outcrossing during host–parasite coevolution

Masri

Schulte

Timmermeyer³

et al. 2013

Ecology Letters

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The Red Queen hypothesis proposes that coevolving parasites select for outcrossing in the host. Outcrossing relies on males, which often show lower immune investment due to, for example, sexual selection. Here, we demonstrate that such sex differences in immunity interfere with parasite-mediated selection for outcrossing. Two independent coevolution experiments with Caenorhabditis elegans and its microparasite Bacillus thuringiensis produced decreased yet stable frequencies of outcrossing male hosts. A subsequent systematic analysis verified that male C. elegans suffered from a direct selective disadvantage under parasite pressure (i.e. lower resistance, decreased sexual activity, increased escape behaviour), which can reduce outcrossing and thus male frequencies. At the same time, males offered an indirect selective benefit, because male-mediated outcrossing increased offspring resistance, thus favouring male persistence in the evolving populations. As sex differences in immunity are widespread, such interference of opposing selective constraints is likely of central importance during host adaptation to a coevolving parasite.

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“…Interestingly, experimental evidence for this idea is still scarce. One of the available case studies is based on an evolution experiment, which we previously performed using the nematode Caenorhabditis elegans as host and its microparasite Bacillus thuringiensis (Schulte et al ., , , ). This evolution experiment allowed us to demonstrate for the first time that, relative to the control, coevolution simultaneously favours genetic diversity in both antagonists and not just one of the two (Schulte et al ., ).…”

Section: Introductionmentioning

confidence: 99%

Host–parasite coevolution favours parasite genetic diversity and horizontal gene transfer

Schulte

Makus

Schulenburg

2013

J of Evolutionary Biology

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Host-parasite coevolution is predicted to favour genetic diversity and the underlying mechanisms (e.g. sexual reproduction and, more generally, genetic exchange), because diversity enhances the antagonists' potential for rapid adaptation. To date, this prediction has mainly been tested and confirmed for the host. It should similarly apply to the parasite. Indeed, our previous work demonstrated that experimental coevolution between the nematode Caenorhabditis elegans and its microparasite Bacillus thuringiensis selects for genetic diversity in both antagonists. For the parasite, the previous analysis was based on plasmid-encoded toxin gene markers. Thus, it was restricted to a very small part of the bacterial genome and did not cover the main chromosome, which harbours a large variety of virulence factors. Here, we present new data for chromosomal gene markers of B. thuringiensis and combine this information with the previous results on plasmid-encoded toxins. Our new results demonstrate that, in comparison with the control treatment, coevolution with a host similarly leads to higher levels of genetic diversity in the bacterial chromosome, thus indicating the relevance of chromosomal genes for coevolution. Furthermore, the frequency of toxin gene gain is significantly elevated during coevolution, highlighting the importance of horizontal gene transfer as a diversity-generating mechanism. In conclusion, our study emphasizes the strong influence of antagonistic coevolution on parasite genetic diversity and gene exchange.

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Increased responsiveness in feeding behaviour ofCaenorhabditis elegansafter experimental coevolution with its microparasiteBacillus thuringiensis

Cited by 14 publications

References 21 publications

The Natural Biotic Environment ofCaenorhabditis elegans

The Natural Biotic Environment ofCaenorhabditis elegans

Sex differences in host defence interfere with parasite‐mediated selection for outcrossing during host–parasite coevolution

Host–parasite coevolution favours parasite genetic diversity and horizontal gene transfer

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