Hinrich Schulenburg

A simple method for the calculation of microsatellite genotype distances irrespective of ploidy level.

Microsatellites are powerful molecular markers, used commonly to estimate intraspecific genetic distances. With the exception of band sharing similarity index, available distance measures were developed specifically for diploid organisms and are unsuited for comparisons of polyploids. Here, we present a simple method for calculation of microsatellite genotype distances, which takes into account mutation processes and permits comparison of individuals with different ploidy levels. This method should provide a valuable tool for intraspecific analyses of polyploid organisms, which are widespread among plants and some animal taxa. An illustration is given using data from the planarian flatworm Schmidtea polychroa (Platyhelminthes).

Introduction. Ecological immunology.

An organisms fitness is critically reliant on its immune system to provide protection against parasites and pathogens. The structure of even simple immune systems is surprisingly complex and clearly will have been moulded by the organisms ecology. The aim of this review and the theme issue is to examine the role of different ecological factors on the evolution of immunity. Here, we will provide a general framework of the field by contextualizing the main ecological factors, including interactions with parasites, other types of biotic as well as abiotic interactions, intraspecific selective constraints (life-history trade-offs, sexual selection) and population genetic processes. We then elaborate the resulting immunological consequences such as the diversity of defence mechanisms (e.g. avoidance behaviour, resistance, tolerance), redundancy and protection against immunopathology, life-history integration of the immune response and shared immunity within a community (e.g. social immunity and microbiota-mediated protection). Our review summarizes the concepts of current importance and directs the reader to promising future research avenues that will deepen our understanding of the defence against parasites and pathogens.

Evolution of the innate immune system: the worm perspective.

Summary:  Simple model organisms that are amenable to comprehensive experimental analysis can be used to elucidate the molecular genetic architecture of complex traits. They can thereby enhance our understanding of these traits in other organisms, including humans. Here, we describe the use of the nematode Caenorhabditis elegans as a tractable model system to study innate immunity. We detail our current understanding of the worms immune system, which seems to be characterized by four main signaling cascades: a p38 mitogen‐activated protein kinase, a transforming growth factor‐β‐like, a programed cell death, and an insulin‐like receptor pathway. Many details, especially regarding pathogen recognition and immune effectors, are only poorly characterized and clearly warrant further investigation. We additionally speculate on the evolution of the C. elegans immune system, taking into special consideration the relationship between immunity, stress responses and digestion, the diversification of the different parts of the immune system in response to multiple and/or coevolving pathogens, and the trade‐off between immunity and host life history traits. Using C. elegans to address these different facets of host–pathogen interactions provides a fresh perspective on our understanding of the structure and complexity of innate immune systems in animals and plants.

Anti-Fungal Innate Immunity in C. elegans Is Enhanced by Evolutionary Diversification of Antimicrobial Peptides

Encounters with pathogens provoke changes in gene transcription that are an integral part of host innate immune responses. In recent years, studies with invertebrate model organisms have given insights into the origin, function, and evolution of innate immunity. Here, we use genome-wide transcriptome analysis to characterize the consequence of natural fungal infection in Caenorhabditis elegans. We identify several families of genes encoding putative antimicrobial peptides (AMPs) and proteins that are transcriptionally up-regulated upon infection. Many are located in small genomic clusters. We focus on the nlp-29 cluster of six AMP genes and show that it enhances pathogen resistance in vivo. The same cluster has a different structure in two other Caenorhabditis species. A phylogenetic analysis indicates that the evolutionary diversification of this cluster, especially in cases of intra-genomic gene duplications, is driven by natural selection. We further show that upon osmotic stress, two genes of the nlp-29 cluster are strongly induced. In contrast to fungus-induced nlp expression, this response is independent of the p38 MAP kinase cascade. At the same time, both involve the epidermal GATA factor ELT-3. Our results suggest that selective pressure from pathogens influences intra-genomic diversification of AMPs and reveal an unexpected complexity in AMP regulation as part of the invertebrate innate immune response.

Specificity of the innate immune system and diversity of C-type lectin domain (CTLD) proteins in the nematode Caenorhabditis elegans

The nematode Caenorhabditis elegans has become an important model for the study of innate immunity. Its immune system is based on several signaling cascades, including a Toll-like receptor, three mitogen-activated protein kinases (MAPK), one transforming growth factor-beta (TGF-beta), the insulin-like receptor (ILR), and the programmed cell death (PCD) pathway. Furthermore, it also involves C-type lectin domain- (CTLD) containing proteins as well as several classes of antimicrobial effectors such as lysozymes. Almost all components of the nematode immune system have homologs in other organisms, including humans, and are therefore likely of ancient evolutionary origin. At the same time, most of them are part of a general stress response, suggesting that they only provide unspecific defense. In the current article, we re-evaluate this suggestion and explore the level of specificity in C. elegans innate immunity, i.e. the nematodes ability to mount a distinct defense response towards different pathogens. We draw particular attention to the CTLD proteins, which are abundant in the nematode genome (278 genes) and many of which show a pathogen-specific response during infection. Specificity may also be achieved through the differential activation of antimicrobial genes, distinct functions of the immunity signaling cascades as well as signal integration across pathways. Taken together, our evaluation reveals high potential for immune specificity in C. elegans that may enhance the nematodes ability to fight off pathogens.

Multiple reciprocal adaptations and rapid genetic change upon experimental coevolution of an animal host and its microbial parasite

The coevolution between hosts and parasites is predicted to have complex evolutionary consequences for both antagonists, often within short time periods. To date, conclusive experimental support for the predictions is available mainly for microbial host systems, but for only a few multicellular host taxa. We here introduce a model system of experimental coevolution that consists of the multicellular nematode host Caenorhabditis elegans and the microbial parasite Bacillus thuringiensis. We demonstrate that 48 host generations of experimental coevolution under controlled laboratory conditions led to multiple changes in both parasite and host. These changes included increases in the traits of direct relevance to the interaction such as parasite virulence (i.e., host killing rate) and host resistance (i.e., the ability to survive pathogens). Importantly, our results provide evidence of reciprocal effects for several other central predictions of the coevolutionary dynamics, including (i) possible adaptation costs (i.e., reductions in traits related to the reproductive rate, measured in the absence of the antagonist), (ii) rapid genetic changes, and (iii) an overall increase in genetic diversity across time. Possible underlying mechanisms for the genetic effects were found to include increased rates of genetic exchange in the parasite and elevated mutation rates in the host. Taken together, our data provide comprehensive experimental evidence of the consequences of host–parasite coevolution, and thus emphasize the pace and complexity of reciprocal adaptations associated with these antagonistic interactions.

Shooting darts: co-evolution and counter-adaptation in hermaphroditic snails

BackgroundEvolutionary conflicts of interest between the sexes often lead to co-evolutionary arms races consisting of repeated arisal of traits advantageous for one sex but harmful to the other sex, and counter-adaptations by the latter. In hermaphrodites, these antagonistic interactions are at least an equally important driving force. Here, we investigate the evolution of one of the most striking examples of sexual conflict in hermaphrodites, the so-called shooting of love-darts in land snails. Stabbing this calcareous dart through the partners skin ultimately increases paternity. This trait is obviously beneficial for the shooter, but it manipulates sperm storage in the receiver. Hence, an arms race between the love-dart and the spermatophore receiving organs may be expected.ResultsWe performed a detailed phylogenetic analysis of 28S ribosomal RNA gene sequences from dart-possessing land snail species. Both the Shimodaira-Hasegawa test and Bayesian posterior probabilities rejected a monophyletic origin of most reproductive structures, including the love-dart, indicating that most traits arose repeatedly. Based on the inferred phylogenetic trees, we calculated phylogenetically independent contrasts for the different reproductive traits. Subsequent principal component and correlation analyses demonstrated that these contrasts covary, meaning that correlated evolution of these traits occurred.ConclusionOur study represents the first comprehensive comparative analysis of reproductive organ characteristics in simultaneous hermaphrodites. Moreover, it strongly suggests that co-evolutionary arms races can result from sexual conflict in these organisms and play a key role in the evolution of hermaphroditic mating systems.

Diversity and specificity in the interaction between Caenorhabditis elegans and the pathogen Serratia marcescens

BackgroundCo-evolutionary arms races between parasites and hosts are considered to be of immense importance in the evolution of living organisms, potentially leading to highly dynamic life-history changes. The outcome of such arms races is in many cases thought to be determined by frequency dependent selection, which relies on genetic variation in host susceptibility and parasite virulence, and also genotype-specific interactions between host and parasite. Empirical evidence for these two prerequisites is scarce, however, especially for invertebrate hosts. We addressed this topic by analysing the interaction between natural isolates of the soil nematode Caenorhabditis elegans and the pathogenic soil bacterium Serratia marcescens.ResultsOur analysis reveals the presence of i) significant variation in host susceptibility, ii) significant variation in pathogen virulence, and iii) significant strain- and genotype-specific interactions between the two species.ConclusionsThe results obtained support the previous notion that highly specific interactions between parasites and animal hosts are generally widespread. At least for C. elegans, the high specificity is observed among isolates from the same population, such that it may provide a basis for and/or represent the outcome of co-evolutionary adaptations under natural conditions. Since both C. elegans and S. marcescens permit comprehensive molecular analyses, these two species provide a promising model system for inference of the molecular basis of such highly specific interactions, which are as yet unexplored in invertebrate hosts.

When the Most Potent Combination of Antibiotics Selects for the Greatest Bacterial Load: The Smile-Frown Transition

Finding the most potent combinations of antibiotics in the lab can be a challenge if antibiotic interactions are not robust to evolutionary adaptation.

The genetics of pathogen avoidance in Caenorhabditis elegans

Much attention is rightly focused on how microbes cause disease, but they can also affect other aspects of host physiology, including behaviour. Indeed, pathogen avoidance behaviours are seen across animal taxa and are probably of major importance in nature. Here, we review what is known about the molecular genetics underlying pathogen avoidance in the nematode Caenorhabditis elegans. In its natural environment, the soil, this animal feeds on microbes and is continuously exposed to a diverse mix of microorganisms. Nematodes that develop efficient behavioural responses that enhance their attraction to sources of food and avoidance of pathogens will have an evolutionary advantage. C. elegans can specifically detect natural products of bacteria, including surfactants (such as serrawettin) and acylated homoserine lactone autoinducers, and it can learn to avoid pathogenic species. To date, several distinct mechanisms have been shown to be involved in pathogen avoidance. They are based on G protein‐like, insulin‐like and neuronal serotonin signalling. We discuss recent findings on the mechanisms of pathogen recognition in C. elegans, the relationship between alternative behavioural defences and also between these and other life‐history traits. We propose that the selective pressure associated with avoidance behaviours influence both pathogen and host evolution.