Generalist parasites have the capacity to infect multiple hosts. The temporal pattern of host specificity by generalist parasites is rarely studied, but is critical to understanding what variables underpin infection and thereby the impact of parasites on host species and the way they impose selection on hosts. Here, the temporal dynamics of infection of four species of freshwater mussel by European bitterling fish (Rhodeus amarus) was investigated over three spawning seasons. Bitterling lay their eggs in the gills of freshwater mussels, which suffer reduced growth, oxygen stress, gill damage and elevated mortality as a result of parasitism. The temporal pattern of infection of mussels by European bitterling in multiple populations was examined. Using a Bernoulli Generalized Additive Mixed Model with Bayesian inference it was demonstrated that one mussel species, Unio pictorum, was exploited over the entire bitterling spawning season. As the season progressed, bitterling showed a preference for other mussel species, which were inferior hosts. Temporal changes in host use reflected elevated density-dependent mortality in preferred hosts that were already infected. Plasticity in host specificity by bitterling conformed with the predictions of the host selection hypothesis. The relationship between bitterling and their host mussels differs qualitatively from that of avian brood parasites.
- MeSH
- Bayes Theorem MeSH
- Cyprinidae MeSH
- Host Specificity * MeSH
- Host-Parasite Interactions * MeSH
- Parasites MeSH
- Animals MeSH
- Check Tag
- Animals MeSH
- Publication type
- Journal Article MeSH
UNLABELLED: Lyme disease, caused by spirochetes in the Borrelia burgdorferi sensu lato clade within the Borrelia genus, is transmitted by Ixodes ticks and is currently the most prevalent and rapidly expanding tick-borne disease in Europe and North America. We report complete genome sequences of 47 isolates that encompass all established species in this clade while highlighting the diversity of the widespread human pathogenic species B. burgdorferi. A similar set of plasmids has been maintained throughout Borrelia divergence, indicating that they are a key adaptive feature of this genus. Phylogenetic reconstruction of all sequenced Borrelia genomes revealed the original divergence of Eurasian and North American lineages and subsequent dispersals that introduced B. garinii, B. bavariensis, B. lusitaniae, B. valaisiana, and B. afzelii from East Asia to Europe and B. burgdorferi and B. finlandensis from North America to Europe. Molecular phylogenies of the universally present core replicons (chromosome and cp26 and lp54 plasmids) are highly consistent, revealing a strong clonal structure. Nonetheless, numerous inconsistencies between the genome and gene phylogenies indicate species dispersal, genetic exchanges, and rapid sequence evolution at plasmid-borne loci, including key host-interacting lipoprotein genes. While localized recombination occurs uniformly on the main chromosome at a rate comparable to mutation, lipoprotein-encoding loci are recombination hotspots on the plasmids, suggesting adaptive maintenance of recombinant alleles at loci directly interacting with the host. We conclude that within- and between-species recombination facilitates adaptive sequence evolution of host-interacting lipoprotein loci and contributes to human virulence despite a genome-wide clonal structure of its natural populations. IMPORTANCE: Lyme disease (also called Lyme borreliosis in Europe), a condition caused by spirochete bacteria of the genus Borrelia, transmitted by hard-bodied Ixodes ticks, is currently the most prevalent and rapidly expanding tick-borne disease in the United States and Europe. Borrelia interspecies and intraspecies genome comparisons of Lyme disease-related bacteria are essential to reconstruct their evolutionary origins, track epidemiological spread, identify molecular mechanisms of human pathogenicity, and design molecular and ecological approaches to disease prevention, diagnosis, and treatment. These Lyme disease-associated bacteria harbor complex genomes that encode many genes that do not have homologs in other organisms and are distributed across multiple linear and circular plasmids. The functional significance of most of the plasmid-borne genes and the multipartite genome organization itself remains unknown. Here we sequenced, assembled, and analyzed whole genomes of 47 Borrelia isolates from around the world, including multiple isolates of the human pathogenic species. Our analysis elucidates the evolutionary origins, historical migration, and sources of genomic variability of these clinically important pathogens. We have developed web-based software tools (BorreliaBase.org) to facilitate dissemination and continued comparative analysis of Borrelia genomes to identify determinants of human pathogenicity.
- MeSH
- Borrelia burgdorferi Group genetics classification MeSH
- Borrelia burgdorferi genetics classification MeSH
- Borrelia genetics classification MeSH
- Phylogeny * MeSH
- Genetic Variation MeSH
- Genome, Bacterial * MeSH
- Host Microbial Interactions genetics MeSH
- Ixodes microbiology MeSH
- Humans MeSH
- Lipoproteins * genetics MeSH
- Lyme Disease * microbiology transmission MeSH
- Evolution, Molecular MeSH
- Plasmids genetics MeSH
- Recombination, Genetic * MeSH
- Whole Genome Sequencing MeSH
- Selection, Genetic * MeSH
- Animals MeSH
- Check Tag
- Humans MeSH
- Animals MeSH
- Publication type
- Journal Article MeSH
- Geographicals
- Europe MeSH
- North America MeSH
Studies of parasite population dynamics in natural systems are crucial for our understanding of host-parasite coevolutionary processes. Some field studies have reported that host genotype frequencies in natural populations change over time according to parasite-driven negative frequency-dependent selection. However, the temporal patterns of parasite genotypes have rarely been investigated. Moreover, parasite-driven negative frequency-dependent selection is contingent on the existence of genetic specificity between hosts and parasites. In the present study, the population dynamics and host-genotype specificity of the ichthyosporean Caullerya mesnili, a common endoparasite of Daphnia water fleas, were analysed based on the observed sequence variation in the first internal transcribed spacer (ITS1) of the ribosomal DNA. The Daphnia population of lake Greifensee (Switzerland) was sampled and subjected to parasite screening and host genotyping during C. mesnili epidemics of four consecutive years. The ITS1 of wild-caught C. mesnili-infected Daphnia was sequenced using the 454 pyrosequencing platform. The relative frequencies of C. mesnili ITS1 sequences differed significantly among years: the most abundant C. mesnili ITS1 sequence decreased and rare sequences increased over the course of the study, a pattern consistent with negative frequency-dependent selection. However, only a weak signal of host-genotype specificity between C. mesnili and Daphnia genotypes was detected. Use of cutting edge genomic techniques will allow further investigation of the underlying micro-evolutionary relationships within the Daphnia-C. mesnili system.
- MeSH
- Time Factors MeSH
- Daphnia genetics parasitology MeSH
- Genotype MeSH
- Host Specificity MeSH
- Host-Parasite Interactions genetics immunology MeSH
- Mesomycetozoea genetics physiology MeSH
- DNA, Ribosomal Spacer MeSH
- Selection, Genetic MeSH
- Animals MeSH
- Check Tag
- Animals MeSH
- Publication type
- Journal Article MeSH
Spider wasps of the genus Minagenia have evolved koinobiontism as a relatively rare life strategy within the widely diversified hymenopteran family Pompilidae. In this study, we evaluated several aspects of the parasitic strategy of the wasp Minagenia sp. (hereafter, Minagenia) - namely host specificity, ontogeny, and sex determination as a function of host size. We found that Minagenia is highly host specific, being associated only with the genus Lycosa from the family Lycosidae, namely Lycosa u-album (Mello-Leitão, 1938), Lycosa erythrognatha (Lucas, 1836) and Lycosa poliostoma (Koch, 1847) with a parasitism incidence of 18.9%, 15.8% and 12.5%, respectively. Both ecological and taxonomical host traits determine the host selection and sex allocation of Minagenia female wasps. Charnov's host-size model explains Minagenia's host-size-dependent sex ratio in combination with the effect of host development stage, host species, and host foraging strategy. We also found that the final instar larva of Minagenia induces behavioural changes in spider hosts. The manipulated spider builds a protective silk chamber as a shelter for parasitoid pupation. Our results suggest that host manipulation seems to be narrowly connected with koinobiont life style throughout Hymenoptera. This study provides new information about the host-parasitoid koinobiont life strategy among spider wasps, which probably arose convergently in distant taxonomical groups within Pompilidae.
- MeSH
- Behavior, Animal MeSH
- Host-Parasite Interactions MeSH
- Larva physiology MeSH
- Reproduction physiology MeSH
- Wasps physiology MeSH
- Life Cycle Stages MeSH
- Animals MeSH
- Check Tag
- Male MeSH
- Female MeSH
- Animals MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
The genes of major histocompatibility complex (MHC) provide an excellent opportunity to study host-parasite relationships because they are expected to evolve in response to parasites and variation in parasite communities. In this study, we investigated the potential role of parasite-mediated selection acting on MHC class IIB (DAB) genes in European chub (Squalius cephalus) natural populations. We found significant differences between populations in metazoan parasites, neutral and adaptive genetic diversities. The analyses based on pairwise data revealed that populations with dissimilar MHC allelic profiles were geographically distant populations with significantly different diversity in microsatellites and a dissimilar composition of parasite communities. The results from the generalized estimating equations method (GEE) on the level of individuals revealed that metazoan parasite load in European chub was influenced by the diversity of DAB alleles as well as by the diversity of neutral genetic markers and host traits reflecting condition and immunocompetence. The multivariate co-inertia analysis showed specific associations between DAB alleles and parasite species. DAB1-like alleles were more involved in associations with ectoparasites, while DAB3-like alleles were positively associated with endoparasites which could suggest potential differences between DAB genes caused by different selection pressure. Our study revealed that parasite-mediated selection is not the only variable affecting MHC diversity in European chub; however, we strongly support the role of neutral processes as the main driver of DAB diversity across populations. In addition, our study contributes to the understanding of the evolution of MHC genes in wild living fish.
- MeSH
- Alleles MeSH
- Cyprinidae genetics MeSH
- Animals, Wild MeSH
- Genetic Variation * MeSH
- Major Histocompatibility Complex genetics MeSH
- Host-Parasite Interactions MeSH
- Microsatellite Repeats genetics MeSH
- Fish Diseases parasitology MeSH
- Parasitic Diseases, Animal epidemiology genetics parasitology MeSH
- Parasites MeSH
- Selection, Genetic * MeSH
- Animals MeSH
- Check Tag
- Animals MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Geographicals
- Europe epidemiology MeSH
Positive selection acting on Toll-like receptors (TLRs) has been recently investigated to reveal evolutionary mechanisms of host-pathogen molecular co-adaptation. Much of this research, however, has focused mainly on the identification of sites predicted to be under positive selection, bringing little insight into the functional differences and similarities among species and a limited understanding of convergent evolution in the innate immune molecules. In this study, we provide evidence of phenotypic variability in the avian TLR4 ligand-binding region (LBR), the direct interface between host and pathogen molecular structures. We show that 55 passerine species vary substantially in the distribution of electrostatic potential on the surface of the receptor, and based on these distinct patterns, we identified four species clusters. Seven of the 34 evolutionarily nonconservative and positively selected residues correspond topologically to sites previously identified as being important for lipopolysaccharide, lipid IVa or MD-2 binding. Five of these positions codetermine the identity of the charge clusters. Groups of species that host-related communities of pathogens were predicted to cluster based on their TLR4 LBR charge. Despite some evidence for convergence among taxa, there were no clear associations between the TLR4 LBR charge distribution and any of the general ecological characteristics compared (migration, latitudinal distribution and diet). Closely related species, however, mostly belonged to the same surface charge cluster indicating that phylogenetic constraints are key determinants shaping TLR4 adaptive evolution. Our results suggest that host innate immune evolution is consistent with Fahrenholz's rule on the cospeciation of hosts and their parasites.
- MeSH
- Glycolipids chemistry genetics MeSH
- Host-Pathogen Interactions genetics MeSH
- Protein Conformation MeSH
- Ligands MeSH
- Lipid A analogs & derivatives chemistry genetics MeSH
- Lipopolysaccharides chemistry genetics MeSH
- Lymphocyte Antigen 96 chemistry genetics MeSH
- Microbiota genetics MeSH
- Evolution, Molecular * MeSH
- Models, Molecular MeSH
- Immunity, Innate genetics MeSH
- Birds genetics parasitology MeSH
- Sequence Analysis, DNA MeSH
- Selection, Genetic * genetics MeSH
- Static Electricity MeSH
- Toll-Like Receptor 4 chemistry genetics MeSH
- Protein Binding MeSH
- Animals MeSH
- Check Tag
- Animals MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
The range of hosts exploited by a parasite is determined by several factors, including host availability, infectivity and exploitability. Each of these can be the target of natural selection on both host and parasite, which will determine the local outcome of interactions, and potentially lead to coevolution. However, geographical variation in host use and specificity has rarely been investigated. Maculinea (= Phengaris) butterflies are brood parasites of Myrmica ants that are patchily distributed across the Palæarctic and have been studied extensively in Europe. Here, we review the published records of ant host use by the European Maculinea species, as well as providing new host ant records for more than 100 sites across Europe. This comprehensive survey demonstrates that while all but one of the Myrmica species found on Maculinea sites have been recorded as hosts, the most common is often disproportionately highly exploited. Host sharing and host switching are both relatively common, but there is evidence of specialization at many sites, which varies among Maculinea species. We show that most Maculinea display the features expected for coevolution to occur in a geographic mosaic, which has probably allowed these rare butterflies to persist in Europe. This article is part of the theme issue 'The coevolutionary biology of brood parasitism: from mechanism to pattern'.
- MeSH
- Species Specificity MeSH
- Ants parasitology MeSH
- Nesting Behavior * MeSH
- Host-Parasite Interactions * MeSH
- Biological Coevolution * MeSH
- Butterflies physiology MeSH
- Symbiosis * MeSH
- Animals MeSH
- Check Tag
- Animals MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Geographicals
- Europe MeSH
Virulent brood parasites refrain from arduous parental care, often kill host progeny and inflict rearing costs upon their hosts. Quantifying the magnitude of such costs across the whole period of care (from incubation through to parasite fledgling independence) is essential for understanding the selection pressures on hosts to evolve antiparasitic defences. Despite the central importance of such costs for our understanding of coevolutionary dynamics, they have not yet been comprehensively quantified in any host of any avian brood parasite. We quantified parasite-rearing costs in common redstarts Phoenicurus phoenicurus raising either parasitic common cuckoo Cuculus canorus or their own chicks throughout the complete breeding cycle, and used multiple cost parameters for each breeding stage: incubation, brooding and feeding effort; length of parental/host care; parent/host body condition; and heterophil/lymphocyte ratio (stress-level indicator). Contrary to traditional assumptions, rearing the parasite per se was not associated with overall higher physiological or physical costs to hosts above the natural levels imposed by efforts to rear their own progeny. The low parasite-rearing costs imposed on hosts may, in part, explain the low levels of known host counter-defences in this unusually frequently parasitized cuckoo host.
- MeSH
- Nesting Behavior * MeSH
- Host-Parasite Interactions * MeSH
- Birds physiology MeSH
- Songbirds parasitology MeSH
- Animals MeSH
- Check Tag
- Animals MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Geographicals
- Finland MeSH
