Abstracts (first author)


Lotka and Volterra kill the Red Queen

Author(s): Schulenburg H, Gokhale CS, Papkou A, Traulsen A


Host-parasite coevolution is generally believed to follow so-called Red Queen dynamics consisting of ongoing oscillations in the frequencies of interacting host and parasite alleles. This view is based on current empirical and theoretical work, which specifically focuses on the evolutionary dynamics of these interactions (i.e., the change in host and parasite allele frequencies). Here, we demonstrate that consideration of a central ecological component, population size fluctuations, dramatically alters these dynamics. In particular, reciprocal selection among antagonists causes inter-dependent demographic variations, as described by the Lotka-Volterra relationship. These population size fluctuations are thus an inherent characteristic of host-parasite coevolution. As they associate with repeated bottlenecks, they increase the likelihood of genetic drift. This in turn favours fast fixation of one of the interacting alleles, often including the allele that is originally rare. As a consequence, any ongoing Red Queen dynamics is rapidly terminated. Taken together, our results suggest that host-parasite coevolution is mainly driven by selective sweeps rather than continuous negative frequency-dependent selection. Long-term coevolution consistent with the Red Queen hypothesis is only possible if new alleles are repeatedly introduced de novo into the interacting host and parasite populations.

Abstracts (coauthor)


More or less all organisms, ranging from sponges to humans, associate with an often extremely diverse microflora. Microbial associations are known to be of immense importance for a host's development, immunity, and life history - all biological fields where the bacteriovorus nematode Caenorhabditis elegans has been studied with great success. On the other hand, laboratory cultures of the worm are axenic or monoxenic by default and we lack basic knowledge about its natural ecology; we even do not know what the nematode feeds on in nature. As a result, complex microbial interactions have mostly been created artificially by studying human pathogens or simply ignored. To rectify this discrepancy, we here used 16S rDNA deep sequencing of natural samples in combination with 16S rDNA Sanger sequencing of culturable bacteria to demonstrate a rich and diverse microflora associated with C. elegans. The prominent identified orders included Bacteroidetes (Flavobacteriales, Sphingobacteriales), Proteobacteria (Rhizobiales, Pseudomonadales, Enterobacteriales) and Firmicutes (Lactobacillales). We furthermore characterized the exact relationship between individual bacterial strains and the nematode host, using fitness assays, behavioral tests, differential interference contrast microscopy, and fluorescence in situ hybridization. Our analysis revealed high nematode fitness on Gammaproteobacteria, whereas Bacteroidetes and Proteobacteria were over time generally more attractive than Actinobacteria and Firmicutes. Our project combines the power of C. elegans as a model organism with its natural ecology to establish a tractable genetic model system for the in-depth analysis of naturally occurring host-microbiota interactions.

Metagenomic analysis of gut bacteria from the red flour beetle Tribolium castaneum

Author(s): Futo, M, Mitschke A, Rosenstiel P, Schulenburg H, Joop G, Kurtz J


The relevance of symbiotic microbial communities in the gut is increasingly being studied in a large number of animal species, from sponges to primates. Although the red flour beetle Tribolium castaneum represents a well-established experimental model organism for studying ecological, evolutionary and developmental topics, to the best of our knowledge, there are no studies on the composition of the gut microbiota of this insect. We examined the bacterial composition of the digestive tract of T. castaneum. For this, two approaches were combined: a culture-independent metagenomic analysis based on 16S rRNA sequences and a classical bacterial cultivation method. The comparison of bacterial 16S rRNA sequences between guts of larval and adult beetles revealed a generally lower diversity of bacterial genera, compared to other insect species. Moreover, the diversity of bacterial genera was higher in guts of adults than in larvae. As expected, cultivation of gut contents on different growth media confirmed only a minor part of the genera found in the metagenomic analysis. The information on bacterial communities in the gut of T. castaneum will be useful for future studies testing interactions between T. castaneum and its microbiota, potential symbionts and pathogens.


Novel infectious diseases have been emerging at an alarming rate over the last few decades, with sometimes devastating consequences for public health. Prime examples include the rise of HIV or the increasing incidences of tuberculosis and MRSA. To understand the origin of these novel strains, detailed knowledge is required on the adaptive evolution underlying successful establishment and spread of emergent strains in new host populations. Both theoretical studies and occasional epidemiological reports identified host immune state as a key factor in disease emergence. However, the importance of this factor has not been studied in a rigorous experimental framework that explicitly allows for long-term evolution.

I will present the results of an evolution experiment in which Pseudomonas aeruginosa PA14 adapted to populations of immunocompetent C. elegans and immunocompromised (mutant) host strains. Phenotypic analyses revealed rapid, to a large extent parallel evolution across all treatments. Strong increases in bacterial fitness were especially observed in immunocompromised hosts, suggesting immunocompromised hosts facilitated faster bacterial adaptation. Genomic analyses confirm the observed phenotypes and the large amount of parallel evolution. However, they further revealed distinct evolutionary paths chosen by bacteria adapting to immunocompromised hosts compared to those adapting to immunocompetent hosts. These results provide important insights for the understanding of bacterial adaptation to host populations, and may assist the development of theoretical models on pathogen evolution and adaptation.

Rapid genomic changes in pathogenic Bacillus thuringiensis during adaptation to its nematode host

Author(s): Branca, A, Masri L, Sheppard A, Rosenstiel P, Bornberg-Bauer E, Schulenburg H


Bacillus thuringiensis is a pathogenic bacterium of invertebrates with a wide host spectrum, including the nematode Caenorhabditis elegans. We studied its ability to adapt to the nematode host with the help of an evolution experiment, during which a mixture of B. thuringiensis strains was either coevolved with C. elegans (coevolution treatment), adapted to a non-changing host population (one-sided adaptation), or evolved in the absence of the host (control evolution). Experimental evolution produced distinct phenotypic changes in virulence and also other life-history traits. Here, I present results on our analysis of the genetic basis of evolutionary changes based on whole-genome sequencing of replicate populations. Firstly, we were able to identify a central role for clonal selection during experimental evolution, especially under coevolution and control conditions. Each of these conditions was dominated by two different chromosomal genotypes, whereas an unexpected variability among replicate populations was observed in the one-sided adaptation treatment. Secondly, we were able to demonstrate that adaptation to the host is additionally influenced by the spread of genomic SNP and indel alleles as well as changes in plasmid composition and presence of phage infection. Taken together, our results highlight that the trajectory of evolution depends on multiple interaction levels: (i) host – pathogen; (ii) competition between pathogen strains and (iii) selfish mobile elements comprised of plasmids and phages.


Pseudomonas aeruginosa is a widespread Gram-negative bacterium found in water, soil, plants and animals. Its diverse array of virulence factors allows it to establish and proliferate in environments ranging from plant roots to the human respiratory tract. It plays an important role in chronic infections such as in cystic fibrosis (CF), and is the most commonly isolated nosocomial bacterium. Pseudomonads naturally possess multiple response mechanisms against antimicrobial treatments granting it resistance against the most commonly used antibiotics. They range from efflux pump systems and complex genetic regulation to intricate social behaviours like biofilm formation or swarming. However, to date, we lack detailed understanding of the relative importance of each of these mechanisms and their interplay during resistance evolution. Thus, our study uses controlled evolution experiments to evaluate in how far different resistance mechanisms are selectively favored throughout P.aeruginosa adaptation to different types of antibiotics.

A stumbling Red Queen: host-parasite coevolution handicapped by Feeble males

Author(s): Masri, L, Schulte RD, Timmermeyer N, Thanisch S, Crummenerl L, Jansen G, Michiels NK, Schulenburg H


Our work highlights the potential influence of intra-specific variations among the sexes in immunocompetence on host-parasite coevolution. In particular, the Red Queen hypothesis proposes that coevolving parasites select for outcrossing in the host. Outcrossing relies on males, which often show lower immune investment as a consequence of sexual selection. Here, we show that such sex-specific variation in immunity significantly interferes with parasite-mediated selection. Two independent coevolution experiments with Caenorhabditis elegans and its microparasite Bacillus thuringiensis produced a decreased yet stable frequency of outcrossing male hosts. Subsequent tests verified that male C. elegans suffered from a direct selective disadvantage. In the presence of its microparasite, males showed lower survival, decreased sexual activity, and altered escape behavior. Each of these responses can reduce outcrossing frequencies. At the same time, males also offered an indirect selective benefit, because male-mediated outcrossing increased offspring resistance. As such intra-specific variations in immunity are widespread among animals, the resulting interference of opposing selective constraints may impose a fundamental limit to host adaptation during antagonistic coevolution.


Although the nematode Caenorhabditis elegans is a major model organism in diverse biological areas and well studied under laboratory conditions, little is known about its ecology and evolutionary history. Therefore, characterization of the species’ natural habitats should provide a new perspective on the otherwise well-characterized biology and life-history of this nematode. C. elegans was for a long time thought to be a soil nematode, but actually seems to prefer nutrient- and microorganism-rich substrates. In order to extend these findings, this project focuses on a continuous long term sampling of C. elegans in rotting apples and compost heaps. Since these habitats degrade rapidly and are only available temporarily, nematodes need to escape harsh conditions and food limitation. We observed that slugs and isopods are likely vectors for transport to new environments. Moreover, C. elegans was found to share its habitat with the related nematode species Caenorhabditis remanei, which could thus represent an important competitor for a similar ecological niche. Microsatellite markers are currently used to characterize population genetic differentiation of the recently isolated C. elegans and those isolated in 2002 from the same location.

The influence of population size on host-parasite coevolution

Author(s): Papkou, A, Schalkowski R, Barg MC, Schulenburg H


Host-parasite interactions are ubiquitous in nature and have a strong impact on species evolution. The signatures of this impact have been identified in genomes, natural communities and on a phylogenetic level. It is not surprising that many aspects of host-parasite relationships have received particular attention from evolutionary biologists. Paradoxically, one indispensible and basic property of host-parasite interaction, population size oscillations, has been overlooked as a factor in host-parasite coevolution. Parasites, by reducing host fecundity and survival, strongly affect population size of the host, which very often is their only ecological niche. Already in the 1920s Lotka and Volterra showed that antagonistic interactions between species would lead to interdependent oscillations in their population size. However, most of the current models of host-parasite coevolution ignore population size changes or use a deterministic approach which cannot realistically imitate the finite nature of real populations. Similarly, in most experimental studies on host-parasite coevolution the population size is kept constant as a matter of good practice. To enhance a more realistic understanding of the coevolutionary dynamics, we performed laboratory-controlled evolution experiments with the model nematode host Caenorhabditis elegans and its microparasite Bacillus thuringiensis and specifically varied the factor population size. Here, we will show our results on temporal changes in host fitness and parasite virulence under different population size regimes.


One prediction of host-parasite coevolution is that the virulence of the pathogen may change as it adapts to its host in a way that maximises its reproductive success and transmission potential. This has indeed been demonstrated in several controlled laboratory coevolution experiments, with both reductions and increases in virulence being seen. The majority of coevolution experiments, however, use discrete host generations taking only a limited number of usually uninfected hosts to start the next generation. Parasite generations are also often, to some extent, discrete, often being extracted from dead or infected hosts to start the next generation, discarding any spores or longer lasting parasite stages that made their way into the environment. For spore forming parasites, however, this is quite different from the likely natural scenario, where spores can survive for long periods of time in the environment and therefore may obtain the greatest evolutionary benefit by getting as many spores into the environment as possible. If under experimental conditions only spores from dead individuals are taken to the next generation, this benefit is not realised, potentially resulting in an outcome, substantially different to what might be seen in nature. I carried out a coevolution experiment using the red flour beetle, Tribolium castaneum, and its natural microsporidian pathogen, Paranosema whitei, with an overlap in host generations. Flour from the beetles’ environment, including any spores which made their way into it, was also transferred from generation to generation. Three treatments with different starting pathogen concentrations and a pathogen free control were used. In all cases coevolution resulted in extinction of the host population, with a pronounced increase in virulence being seen.


Chairman: Octávio S. Paulo
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XIV Congress of the European Society for Evolutionary Biology

Organization Team
Department of Animal Biology (DBA)
Faculty of Sciences of the University of Lisbon
P-1749-016 Lisbon


Computational Biology & Population Genomics Group