Arndt Telschow

How many species are infected with Wolbachia? – a statistical analysis of current data

Wolbachia are intracellular bacteria found in many species of arthropods and nematodes. They manipulate the reproduction of their arthropod hosts in various ways, may play a role in host speciation and have potential applications in biological pest control. Estimates suggest that at least 20% of all insect species are infected with Wolbachia. These estimates result from several Wolbachia screenings in which numerous species were tested for infection; however, tests were mostly performed on only one to two individuals per species. The actual percent of species infected will depend on the distribution of infection frequencies among species. We present a meta-analysis that estimates percentage of infected species based on data on the distribution of infection levels among species. We used a beta-binomial model that describes the distribution of infection frequencies of Wolbachia, shedding light on the overall infection rate as well as on the infection frequency within species. Our main findings are that (1) the proportion of Wolbachia-infected species is estimated to be 66%, and that (2) within species the infection frequency follows a ‘most-or-few’ infection pattern in a sense that the Wolbachia infection frequency within one species is typically either very high (>90%) or very low (<10%).

THE EFFECT OF WOLBACHIA VERSUS GENETIC INCOMPATIBILITIES ON REINFORCEMENT AND SPECIATION

Abstract Wolbachia is a widespread group of intracellular bacteria commonly found in arthropods. In many insect species, Wolbachia induce a cytoplasmic mating incompatibility (CI). If different Wolbachia infections occur in the same host species, bidirectional CI is often induced. Bidirectional CI acts as a postzygotic isolation mechanism if parapatric host populations are infected with different Wolbachia strains. Therefore, it has been suggested that Wolbachia could promote speciation in their hosts. In this article we investigate theoretically whether Wolbachia‐induced bidirectional CI selects for premating isolation and therefore reinforces genetic divergence between parapatric host populations. To achieve this we combined models for Wolbachia dynamics with a well‐studied reinforcement model. This new model allows us to compare the effect of bidirectional CI on the evolution of female mating preferences with a situation in which postzygotic isolation is caused by nuclear genetic incompatibilities (NI). We distinguish between nuclear incompatibilities caused by two loci with epistatic interactions, and a single locus with incompatibility among heterozygotes in the diploid phase. Our main findings are: (1) bidirectional CI and single locus NI select for premating isolation with a higher speed and for a wider parameter range than epistatic NI; (2) under certain parameter values, runaway sexual selection leads to the increase of an introduced female preference allele and fixation of its preferred male trait allele in both populations, whereas under others it leads to divergence in the two populations in preference and trait alleles; and (3) bidirectional CI and single locus NI can stably persist up to migration rates that are two times higher than seen for epistatic NI. The latter finding is important because the speed with which mutants at the preference locus spread increases exponentially with the migration rate. In summary, our results show that bidirectional CI selects for rapid premating isolation and so generally support the view that Wolbachia can promote speciation in their hosts.

Cytoplasmic incompatibility and host population structure

Many arthropod species are infected by maternally inherited bacteria that induce cytoplasmic incompatibility (CI). CI causes embryonic mortality in offspring when infected males mate with either uninfected females or with females that are infected with a different strain of bacteria. Here, we review theoretical and empirical studies concerning the infection dynamics of CI-inducing bacteria, focusing in particular on the impact of the host population structure on the spread of CI. As different theoretical models have often produced divergent predictions with regard to issues such as the speed of CI spread and the stability of infection polymorphisms, we specifically aim to clarify how the various assumptions concerning population structure that underlie these models affect these predictions. We also discuss several implications of population structure, including the impact of CI on host gene flow reduction and speciation, the evolutionary dynamics of CI and strategies to control insect pest populations by means of CI-inducing microbes.

Host-Pathogen Coevolution: The Selective Advantage of Bacillus thuringiensis Virulence and Its Cry Toxin Genes.

Reciprocal coevolution between host and pathogen is widely seen as a major driver of evolution and biological innovation. Yet, to date, the underlying genetic mechanisms and associated trait functions that are unique to rapid coevolutionary change are generally unknown. We here combined experimental evolution of the bacterial biocontrol agent Bacillus thuringiensis and its nematode host Caenorhabditis elegans with large-scale phenotyping, whole genome analysis, and functional genetics to demonstrate the selective benefit of pathogen virulence and the underlying toxin genes during the adaptation process. We show that: (i) high virulence was specifically favoured during pathogen–host coevolution rather than pathogen one-sided adaptation to a nonchanging host or to an environment without host; (ii) the pathogen genotype BT-679 with known nematocidal toxin genes and high virulence specifically swept to fixation in all of the independent replicate populations under coevolution but only some under one-sided adaptation; (iii) high virulence in the BT-679-dominated populations correlated with elevated copy numbers of the plasmid containing the nematocidal toxin genes; (iv) loss of virulence in a toxin-plasmid lacking BT-679 isolate was reconstituted by genetic reintroduction or external addition of the toxins. We conclude that sustained coevolution is distinct from unidirectional selection in shaping the pathogens genome and life history characteristics. To our knowledge, this study is the first to characterize the pathogen genes involved in coevolutionary adaptation in an animal host–pathogen interaction system.

Transmission dynamics of an emerging infectious disease in wildlife through host reproductive cycles.

Emerging infectious diseases are major threats to wildlife populations. To enhance our understanding of the dynamics of these diseases, we investigated how host reproductive behavior and seasonal temperature variation drive transmission of infections among wild hosts, using the model system of cyprinid herpesvirus 3 (CyHV-3) disease in common carp. Our main findings were as follows: (1) a seroprevalence survey showed that CyHV-3 infection occurred mostly in adult hosts, (2) a quantitative assay for CyHV-3 in a host population demonstrated that CyHV-3 was most abundant in the spring when host reproduction occurred and water temperature increased simultaneously and (3) an analysis of the dynamics of CyHV-3 in water revealed that CyHV-3 concentration increased markedly in breeding habitats during host group mating. These results indicate that breeding habitats can become hot spots for transmission of infectious diseases if hosts aggregate for mating and the activation of pathogens occurs during the host breeding season.

Life and Death of an Influential Passenger: Wolbachia and the Evolution of CI-Modifiers by Their Hosts

Background Wolbachia are intracellular bacteria widely distributed among arthropods and nematodes. In many insect species these bacteria induce a cytoplasmic incompatibility (CI) between sperm of infected males and eggs of uninfected females. From an evolutionary point of view, CI is puzzling: In order to induce this modification-rescue system, Wolbachia affect sperm of infected males even though Wolbachia are only transmitted maternally. Phylogenetic studies of Wolbachia and hosts show that the bacteria rarely cospeciate with their hosts, indicating that infections are lost in host species. However, the mechanisms leading to Wolbachia loss are not well understood. Results Using a population genetic model, we investigate the spread of host mutants that enhance or repress Wolbachia action by affecting either bacterial transmission or the level of CI. We show that host mutants that decrease CI-levels in males (e.g. by reducing Wolbachia-density during spermatogenesis) spread, even at cost to mutant males. Increase of these mutants can lead to loss of Wolbachia infections, either as a direct consequence of their increase or in a step-wise manner, and we derive analytically a threshold penetrance above which a mutations spread leads to extinction of Wolbachia. Selection on host modifiers is sexually antagonistic in that, conversely, host mutants that enhance Wolbachia in females are favoured whereas suppressors are not. Conclusions Our results indicate that Wolbachia is likely to be lost from host populations on long evolutionary time scales due to reduction of CI levels in males. This can occur either by evolution of single host modifiers with large effects or through accumulation of several modifier alleles with small effects on Wolbachia action, even at cost to mutant males and even if infected hosts do not incur fecundity costs. This possibility is consistent with recent findings and may help to explain the apparent short evolutionary persistence times of Wolbachia in many host systems.

Effects of Wolbachia on Genetic Divergence Between Populations: Mainland-Island Model'

Abstract Cytoplasmic incompatibility (CI) induced by intracellular bacteria is a possible mechanism for speciation. Growing empirical evidence suggests that bacteria of the group Wolbachia may indeed act as isolating factors in recent insect speciation. Wolbachia are cytoplasmically transmitted and can cause uni- or bidirectional CI. We present a mainland-island model to investigate how much impact Wolbachia can have on genetic divergence between populations. In the first scenario we assume that the island population has diverged at a selected locus and ask whether genetic divergence will be maintained after introduction of migration from the mainland. In the second we explore whether divergence will originate under migration. For simplicity, the host organisms are modeled as haploid sexuals. Simulations show that if each population is initially infected with a different strain of Wolbachia, then higher levels of divergence occur at the locally selected locus than in the absence of Wolbachia. A weaker effect is seen when there is only unidirectional CI caused by a single strain of Wolbachia on the island. CI increases divergence because it reduces effective migration between mainland and island. Migrants suffer from being confronted with the wrong CI system and this also applies to their matrilineal descendants. Moreover, there is a strong linkage disequilibrium between host genotype and infection state, which helps to maintain Wolbachia differences between the populations in the face of migration A sex bias in migration can either increase or decrease the effect of Wolbachia on divergence. Results support the view that Wolbachia has the potential for increasing divergence between populations and thus could enhance probabilities of speciation.

The hitchhiker's guide to Europe: the infection dynamics of an ongoing Wolbachia invasion and mitochondrial selective sweep in Rhagoletis cerasi

Wolbachia is a maternally inherited and ubiquitous endosymbiont of insects. It can hijack host reproduction by manipulations such as cytoplasmic incompatibility (CI) to enhance vertical transmission. Horizontal transmission of Wolbachia can also result in the colonization of new mitochondrial lineages. In this study, we present a 15‐year‐long survey of Wolbachia in the cherry fruit fly Rhagoletis cerasi across Europe and the spatiotemporal distribution of two prevalent strains, wCer1 and wCer2, and associated mitochondrial haplotypes in Germany. Across most of Europe, populations consisted of either 100% singly (wCer1) infected individuals with haplotype HT1, or 100% doubly (wCer1&2) infected individuals with haplotype HT2, differentiated only by a single nucleotide polymorphism. In central Germany, singly infected populations were surrounded by transitional populations, consisting of both singly and doubly infected individuals, sandwiched between populations fixed for wCer1&2. Populations with fixed infection status showed perfect association of infection and mitochondria, suggesting a recent CI‐driven selective sweep of wCer2 linked with HT2. Spatial analysis revealed a range expansion for wCer2 and a large transition zone in which wCer2 splashes appeared to coalesce into doubly infected populations. Unexpectedly, the transition zone contained a large proportion (22%) of wCer1&2 individuals with HT1, suggesting frequent intraspecific horizontal transmission. However, this horizontal transmission did not break the strict association between infection types and haplotypes in populations outside the transition zone, suggesting that this horizontally acquired Wolbachia infection may be transient. Our study provides new insights into the rarely studied Wolbachia invasion dynamics in field populations.

The neutral effective migration rate in a mainland-island context.

Genetic influx into a population often does not correspond to the real migration rate (m) of individuals, due to class structure within the population. The effective migration rate (m(e)) is a concept to measure gene flow in such a situation. The ratio of the effective migration rate to the real migration rate (m(e)/m) is called the gene flow factor, and represents the degree of gene flow modification. Prior authors proposed different definitions of the effective migration rate. These may be categorized into two groups: the neutral effective migration rate and the selective effective migration rate. In this article, we construct a general model of a class-structured population with a mainland-island structure. Using the model, we prove that the gene flow factor of the neutral effective migration rate converges to the mean reproductive value of immigrants if the limit is taken with the real migration rate converging to zero. This limit theorem provides a novel interpretation of gene flow and can be used to derive approximation formulae of the neutral effective migration rate. We illustrate this method analyzing two examples, sex ratio distortion due to extrinsic factors and hybrid zones with underdominance.

Rapid evolution of virulence leading to host extinction under host-parasite coevolution

BackgroundHost-parasite coevolution is predicted to result in changes in the virulence of the parasite in order to maximise its reproductive success and transmission potential, either via direct host-to-host transfer or through the environment. The majority of coevolution experiments, however, do not allow for environmental transmission or persistence of long lived parasite stages, in spite of the fact that these may be critical for the evolutionary success of spore forming parasites under natural conditions. We carried out a coevolution experiment using the red flour beetle, Tribolium castaneum, and its natural microsporidian parasite, Paranosema whitei. Beetles and their environment, inclusive of spores released into it, were transferred from generation to generation. We additionally took a modelling approach to further assess the importance of transmissive parasite stages on virulence evolution.ResultsIn all parasite treatments of the experiment, coevolution resulted in extinction of the host population, with a pronounced increase in virulence being seen. Our modelling approach highlighted the presence of environmental transmissive parasite stages as being critical to the trajectory of virulence evolution in this system.ConclusionsThe extinction of host populations was unexpected, particularly as parasite virulence is often seen to decrease in host-parasite coevolution. This, in combination with the increase in virulence and results obtained from the model, suggest that the inclusion of transmissive parasite stages is important to improving our understanding of virulence evolution.