Host-parasite Population Research Articles

Spatial invasion of cooperative parasites

In this paper we study invasion probabilities and invasion times of cooperative parasites spreading in spatially structured host populations. The spatial structure of the host population is given by a random geometric graph on [0,1]n, n∈N, with a Poisson(N)-distributed number of vertices and in which vertices are connected over an edge when they have a distance of at most rN with rN of order N(β−1)/n for some 0<β<1. At a host infection many parasites are generated and parasites move along edges to neighbouring hosts. We assume that parasites have to cooperate to infect hosts, in the sense that at least two parasites need to attack a host simultaneously. We find lower and upper bounds on the invasion probability of the parasites in terms of survival probabilities of branching processes with cooperation. Furthermore, we characterize the asymptotic invasion time.An important ingredient of the proofs is a comparison with infection dynamics of cooperative parasites in host populations structured according to a complete graph, i.e. in well-mixed host populations. For these infection processes we can show that invasion probabilities are asymptotically equal to survival probabilities of branching processes with cooperation. Furthermore, we build on proof techniques developed in Brouard and Pokalyuk (2022), where an analogous invasion process has been studied for host populations structured according to a configuration model.We substantiate our results with simulations.

Contrasting Host-Parasite Population Structure: Morphology and Mitogenomics of a Parasitic Flatworm on Pelagic Deepwater Cichlid Fishes from Lake Tanganyika.

Simple SummarySpecies richness in open water areas is generally lower than in coastal zones. Fish parasites have been targeted as biological tags potentially magnifying biological patterns of their hosts including long-distance migrations notoriously difficult to trace. Lake Tanganyika (Africa) is an ideal place to study general mechanisms of host-parasite interactions in an open water environment and Cichlidogyrus, a monogenean flatworm lineage also present in Lake Tanganyika, has been proposed as a model system to study parasite-host relationships. The present study revealed the lake-wide occurrence (600 km) of Cichlidogyrus casuarinus, a parasite with a broad host range infecting pelagic fishes endemic to Lake Tanganyika. Our comparative approach highlighted incongruence between morphological and genetic differentiation of the populations of Cichlidogyrus casuarinus. Our results show a limitation of the parasite’s magnifying potential for the focal host species due to the parasites’ broad host range including highly mobile host species. Using different sequencing technologies, the study further provides the first assessment of the genetic variation of mitochondrial data in Cichlidogyrus showing contrasting patterns within and between parasite species. Given the now considerable baseline knowledge on its morphological and genetic variation, we propose C. casuarinus as a model to study (1) mechanisms driving host range and (2) the role of phenotypic plasticity in diversification and speciation.Little phylogeographic structure is presumed for highly mobile species in pelagic zones. Lake Tanganyika is a unique ecosystem with a speciose and largely endemic fauna famous for its remarkable evolutionary history. In bathybatine cichlid fishes, the pattern of lake-wide population differentiation differs among species. We assessed the congruence between the phylogeographic structure of bathybatine cichlids and their parasitic flatworm Cichlidogyrus casuarinus to test the magnifying glass hypothesis. Additionally, we evaluated the use of a PoolSeq approach to study intraspecific variation in dactylogyrid monogeneans. The lake-wide population structure of C. casuarinus ex Hemibates stenosoma was assessed based on a portion of the cox1 gene combined with morphological characterisation. Additionally, intraspecific mitogenomic variation among 80 parasite samples from one spatially constrained metapopulation was assessed using shotgun NGS. While no clear geographic genetic structure was detected in parasites, both geographic and host-related phenotypic variation was apparent. The incongruence with the genetic north-south gradient observed in H. stenosoma may be explained by the broad host range of this flatworm including eupelagic bathybatine host species that form panmictic populations across the lake. In addition, we present the first parasite mitogenome from Lake Tanganyika and propose a methodological framework for studying the intraspecific mitogenomic variation of dactylogyrid monogeneans.

Three methods to measure parasite aggregation using examples from Australian fish parasites

Abstract The distribution of parasites in host populations is integral to simulations of parasite populations. We compared three methods to measure parasite aggregation, namely the Hoover, coefficient of variation and I10 indices, using field data from a range of fish parasites. These included anisakid nematodes, trypanorhynch cestodes and polyopisthocotylean monogeneans from 10 previously published studies and one unpublished study. Positive correlations among the three methods were high. Standard errors and estimated biases obtained by bootstrap methods were smallest for the Hoover index. There was no evidence for a bias–variance trade‐off. The analyses suggest that the Hoover index is to be preferred as a measure of aggregation although difficulties remain in deriving theoretical and operational definitions of aggregation.

Spatial Dynamics of Two Host-Parasite Relationships on Intertidal Oyster Reefs

Intertidal reefs comprised of the eastern oyster (Crassostrea virginica) have long experienced habitat loss, altering habitat patch characteristics of size and distance from edge to interior, potentially influencing spatial dynamics of host-parasite relationships. Using two parasitic relationships, one between eastern oyster host and parasitic oyster pea crab (Zaops ostreum) and the other between a xanthid crab (Eurypanopeus depressus) and a parasitic rhizocephalan barnacle (Loxothylacus panopaei), we examined how host-parasite population characteristics varied on intertidal reefs by season, reef size, and distance from edge to interior. Pea crab prevalence was more related to habitat characteristics rather than host density, as pea crab prevalence was the highest on large reefs and along edges, areas of comparatively lower oyster densities. Reef size did not influence densities of parasitized or non-parasitized xanthid crabs, but densities varied from edge to interior. Non-parasitized xanthids had significantly lower densities along the reef edge compared to more interior reef locations, while parasitized xanthid crabs had no significant edge to interior pattern. Organismal size had a varied relationship based upon habitat characteristics, as pea crab carapace width (CW) varied interactively with season and reef size, whereas CW of parasitized/non-parasitized xanthid crabs varied significantly between edge and interior locations. These results demonstrated that influential habitat characteristics, such as patch size and edge versus interior, are both highly species and host-parasite specific. Therefore, continued habitat alteration and fragmentation of critical marine habitats may further impact spatial dynamics of host-parasite relationships.

"Parasite turnover zone" at secondary contact: A new pattern in host-parasite population genetics.

We describe here a new pattern of population genetic structure in a host-parasite system that can arise after secondary contact of previously isolated populations. Due to different generation times, and therefore different tempos of molecular evolution, the host and parasite populations reach different degrees of genetic differentiation during their separation (e.g., in refugia). Consequently, upon secondary contact, the host populations are able to re-establish a single panmictic population across the area of contact, while the parasite populations stop their dispersal at the secondary contact zone and create a narrow hybrid zone. From the host's perspective, the parasite's hybrid zone functions on a microevolutionary scale as a "parasite turnover zone": while the hosts are passing from area A to area B, their parasites turn genetically from the area A genotypes to the area B genotypes. We demonstrate this novel pattern with a model composed of Apodemus mice and Polyplax lice by comparing maternally inherited markers (complete mitochondrial genomes, and complete genomes of the vertically transmitted symbiont Legionella polyplacis) with single nucleotide polymorphisms derived from louse genomic data. We discuss the circumstances that may lead to this pattern and possible reasons why it has been overlooked in studies of host-parasite population genetics.

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About the Influences of Some Major Biotic Drivers on the Population Dynamics in Host-parasite Systems: Interpretative Lessons from an Extended Nicholson-Bailey Model

Population dynamics within host-parasite systems in insects is governed by a series of factors, both endogenous and exogenous. Among them, five factors may be considered as major drivers: the respective inherent rates of increase of the host and of the parasite, the level of resource available to the host, the respective immigration rates of the host and of the parasite. While only the first two (the inherent rates of increase of host and parasite) are considered in the original Nicholson and Bailey model, an extended version of the model includes also the other three parameters, thus providing a broader (although still schematic) approach to the host-parasite population dynamics. A brief analysis of the respective influences of each of these five driving parameters on the main features of host-parasite dynamics is derived accordingly, based upon this extended model. Finally, specific attention is paid to the major concerns due to the cyclic outbreaks of both the host and the parasite, regarding in particular the amplitude, the periodicity and the conditions of onset of the cyclicity. Both the practical aspects of the cyclic regime and its possible adaptative significance are discussed. As a whole, this approach aims to provide some general clues for the interpretation of various features of the host-parasite dynamics, as reported from field observations.

Using a multistate occupancy approach to determine molecular diagnostic accuracy and factors affecting avian haemosporidian infections

The use of a sensitive and accurate parasite detection methodology is crucial in studies exploring prevalence of parasites in host populations or communities, and uncertainty in identifying parasite genera and/or lineages may limit the understanding of host-parasite interactions. Here, we used a multistate occupancy approach that accounts for imperfect detection to assess whether sex and breeding season influenced the prevalence of a specific Haemoproteus lineage (TARUF02) in a white-lined tanager population. Likewise, we explored whether the probability of detecting the target parasite in an infected bird using PCR and sequencing analyses may be influenced by season and host sex. We found little evidence that sex influenced the probability of an individual host being infected by a haemosporidian parasite. Conversely, we found that the probability of infection by Haemoproteus TARUF02 was ~30% higher during the breeding season, reflecting a higher prevalence of this parasite in this season. The probability that PCR detects DNA of haemosporidian parasite was higher for female birds, suggesting that they are more prone to be parasitized with parasitemia levels that are more successfully detected by molecular analysis. Sequencing successfully determined the Haemoproteus TARUF02 lineage in 60% of samples collected during the breeding season and 84% of samples collected during the non-breeding season. Understanding the ecology of hosts and aspects of their physiology that may influence the parasite infection is essential to better understanding of hemoparasite infections and how parasites influence their native hosts, through decreasing reproductive success, lifespan, and/or survival.

Modeling and Stability Analysis of Host-parasite Population Dynamics

In this study, a mathematical model is developed to explore the population dynamics of two host species. Both the hosts depend on the same resources and the availability of such resources is limited in nature. If the host populations increase abnormally the limited natural resources will be used up. Hence, the concept of parasite is brought in to the picture to regulate the host populations. The parasite is a mechanism that reduces the host populations. However, on one hand if the parasite attacks more the hosts may extinct and on the other hand if the parasite do not attack then the host populations may increase and resource may be used up. Hence, the parasite is expected to maintain a balance so that neither the host populations nor the resources extinct. Here, both the hosts are classified in to susceptible and infected and hence the model comprises of four populations: Susceptible Host–1, Infected Host–1, Susceptible Host–2 and Infected Host–2. Thus, the mathematical model comprises of a system of four first order non-linear ordinary differential equations. Mathematical analysis of the model is conducted. Positivity and boundedness of the solution have been verified and thus shown that the model is physically meaningful and biologically acceptable. Equilibrium points of the model are identified and stability analysis is conducted. Simulation study is conducted in order to support the mathematical analysis using software packages Mat lab and DeDiscover.

Rapid divergence, molecular evolution, and morphological diversification of coastal host-parasite systems from southern Brazil.

This study assessed the role of historical processes on the geographic isolation, molecular evolution, and morphological diversification of host-parasite populations from the southern Brazilian coast. Adult specimens of Scleromystax barbatus and Scleromystax macropterus were collected from the sub-basin of the Nhundiaquara River and the sub-basin of the Paranaguá Bay, state of Paraná, Brazil. Four species of Gyrodactylus were recovered from the body surface of both host species. Morphometric analysis of Gyrodactylus spp. and Scleromystax spp. indicated that subpopulations of parasites and hosts could be distinguished from different sub-basins and locations, but the degree of morphological differentiation seems to be little related to geographic distance between subpopulations. Phylogenetic relationships based on DNA sequences of Gyrodactylus spp. and Scleromystax spp. allowed distinguishing lineages of parasites and hosts from different sub-basins. However, the level of genetic structuring of parasites was higher in comparison to host species. Evidence of positive selection in mtDNA sequences is likely associated with local adaptation of lineages of parasites and hosts. A historical demographic analysis revealed that populations of Gyrodactylus and Scleromystax have expanded in the last 250 000 years. The genetic variation of parasites and hosts is consistent with population-specific selection, population expansions, and recent evolutionary co-divergence.

Microparasite dispersal in metapopulations: a boon or bane to the host population?

Although connectivity can promote host species persistence in a metapopulation, dispersal may also enable disease transmission, an effect further complicated by the impact that parasite distribution may have on host-parasite population dynamics. We investigated the effects of connectivity and initial parasite distribution (clustered or dispersed) on microparasite-host dynamics in experimental metapopulations, using guppies and Gyrodactylus turnbulli We created metapopulations of guppies divided into four subpopulations and introduced either a low level of parasites to all subpopulations (dispersed) or a high level of parasites to one subpopulation (clustered). Controlled migration among subpopulations occurred every 10 days. In additional trials, we introduced low or high levels of parasites to isolated populations. Parasites persisted longer in metapopulations than in isolated populations. Mortality was lowest in isolated populations with low-level introductions. The interaction of connectivity and initial parasite distribution influenced parasite abundance. With low-level introductions, connectivity helped the parasite persist longer but had little effect on the hosts. With high levels, connectivity also benefited the hosts, lowering parasite burdens. These findings have implications for disease management and species conservation.

The contrasting roles of host species diversity and parasite population genetic diversity in the infection dynamics of a keystone parasitic plant

AbstractDiversity among species and genetic diversity within species are both important components of ecological communities that can determine the outcome of species interactions, especially between hosts and parasites. We sought to understand the impact of species diversity on host community resistance to infection by a keystone parasitic plant (Rhinanthus minorL.) and genetic diversity of the parasite on its successful establishment in a grassland community.We used an experimental approach where large pots were planted with mixtures of mesotrophic grassland species at high and low species diversity. The parasitic plant was sown in a proportion of these with high and low genetic diversity treatments. Establishment of the parasite was monitored over 2 years and the pots harvested at the end of each growing season to determine the impact of infection on plant community biomass.We found a strong effect of host plant species diversity on the establishment of the parasitic plant, with successful establishment considerably lower in the high species diversity treatment. Genetic diversity appeared to promote establishment of the parasite in the high species diversity treatment, and also facilitated longer term fitness in the low species diversity treatment. Host community structure was influenced byR. minor, with grass relative biomass decreasing and legume relative biomass increasing when the parasite was present. There was no direct impact of the presence of the parasite on the relative biomass of nonleguminous forbs.Synthesis. Our data demonstrate the importance of host community species diversity in deterring the establishment of a generalist parasite. They also highlight the role of genetic diversity in determining the outcome of host–parasite interactions in multispecies communities. These findings, therefore, have important implications for the establishment and management of species‐rich grasslands and provide insight into the community dynamics of parasitic plants and their hosts.

Responses to a warming world: Integrating life history, immune investment, and pathogen resistance in a model insect species.

Environmental temperature has important effects on the physiology and life history of ectothermic animals, including investment in the immune system and the infectious capacity of pathogens. Numerous studies have examined individual components of these complex systems, but little is known about how they integrate when animals are exposed to different temperatures. Here, we use the Indian meal moth (Plodia interpunctella) to understand how immune investment and disease resistance react and potentially trade‐off with other life‐history traits. We recorded life‐history (development time, survival, fecundity, and body size) and immunity (hemocyte counts, phenoloxidase activity) measures and tested resistance to bacterial (E. coli) and viral (Plodia interpunctella granulosis virus) infection at five temperatures (20–30°C). While development time, lifespan, and size decreased with temperature as expected, moths exhibited different reproductive strategies in response to small changes in temperature. At cooler temperatures, oviposition rates were low but tended to increase toward the end of life, whereas warmer temperatures promoted initially high oviposition rates that rapidly declined after the first few days of adult life. Although warmer temperatures were associated with strong investment in early reproduction, there was no evidence of an associated trade‐off with immune investment. Phenoloxidase activity increased most at cooler temperatures before plateauing, while hemocyte counts increased linearly with temperature. Resistance to bacterial challenge displayed a complex pattern, whereas survival after a viral challenge increased with rearing temperature. These results demonstrate that different immune system components and different pathogens can respond in distinct ways to changes in temperature. Overall, these data highlight the scope for significant changes in immunity, disease resistance, and host–parasite population dynamics to arise from small, biologically relevant changes to environmental temperature. In light of global warming, understanding these complex interactions is vital for predicting the potential impact of insect disease vectors and crop pests on public health and food security.

Simulated climate change, epidemic size, and host evolution across host-parasite populations.

Climate change is causing warmer and more variable temperatures as well as physical flux in natural populations, which will affect the ecology and evolution of infectious disease epidemics. Using replicate seminatural populations of a coevolving freshwater invertebrate-parasite system (host: Daphnia magna, parasite: Pasteuria ramosa), we quantified the effects of ambient temperature and population mixing (physical flux within populations) on epidemic size and population health. Each population was seeded with an identical suite of host genotypes and dose of parasite transmission spores. Biologically reasonable increases in environmental temperature caused larger epidemics, and population mixing reduced overall epidemic size. Mixing also had a detrimental effect on host populations independent of disease. Epidemics drove parasite-mediated selection, leading to a loss of host genetic diversity, and mixed populations experienced greater evolution due to genetic drift over the season. These findings further our understanding of how diversity loss will reduce the host populations' capacity to respond to changes in selection, therefore stymying adaptation to further environmental change.

Intra- and interspecific genetic diversity of New Zealand hairworms (Nematomorpha).

Hairworms (Nematomorpha) are a little-known group of parasites, and despite having been represented in the taxonomic literature for over a century, the implementation of molecular genetics in studies of hairworm ecology and evolution lags behind that of other parasitic taxa. In this study, we characterize the genetic diversity of the New Zealand nematomorph fauna and test for genetic structure within the most widespread species found. We provide new mitochondrial and nuclear ribosomal sequence data for three previously described species from New Zealand: Gordius paranensis, Parachordodes diblastus and Euchordodes nigromaculatus. We also present genetic data on a previously reported but undescribed Gordius sp., as well as data from specimens of a new Gordionus sp., a genus new for New Zealand. Phylogenetic analyses of CO1 and nuclear rDNA regions correspond with morphological classification based on scanning electron microscopy, and demonstrate paraphyly of the genus Gordionus and the potential for cryptic species within G. paranensis. Population-level analyses of E. nigromaculatus showed no genetic differentiation among sampling locations across the study area, in contrast to previously observed patterns in known and likely definitive hosts. Taken together, this raises the possibility that factors such as definitive host specificity, intermediate host movement, and passive dispersal of eggs and larvae may influence host-parasite population co-structure in hairworms.

A Model for Evolutionary Ecology of Disease: The Case for Caenorhabditis Nematodes and Their Natural Parasites

Many of the outstanding questions in disease ecology and evolution call for combining observation of natural host-parasite populations with experimental dissection of interactions in the field and the laboratory. The "rewilding" of model systems holds great promise for this endeavor. Here, we highlight the potential for development of the nematode Caenorhabditis elegans and its close relatives as a model for the study of disease ecology and evolution. This powerful laboratory model was disassociated from its natural habitat in the 1960s. Today, studies are uncovering that lost natural history, with several natural parasites described since 2008. Studies of these natural Caenorhabditis-parasite interactions can reap the benefits of the vast array of experimental and genetic tools developed for this laboratory model. In this review, we introduce the natural parasites of C. elegans characterized thus far and discuss resources available to study them, including experimental (co)evolution, cryopreservation, behavioral assays, and genomic tools. Throughout, we present avenues of research that are interesting and feasible to address with caenorhabditid nematodes and their natural parasites, ranging from the maintenance of outcrossing to the community dynamics of host-associated microbes. In combining natural relevance with the experimental power of a laboratory supermodel, these fledgling host-parasite systems can take on fundamental questions in evolutionary ecology of disease.

Superparasitism and Population Regulation of the Mosquito-Parasitic Mermithid Nematodes Romanomermis iyengari and Strelkovimermis spiculatus

Superparasitism is a common phenomenon in mosquito-parasitic mermithid nematodes. Multiple nematodes are needed in a single host to produce males. Host selection behavior and intraspecific competition among Romanomermis iyengari and Strelkovimermis spiculatus were investigated against their host, Culex pipiens pipiens in laboratory experiments. In a choice assay between previously infected and uninfected host larvae, infectious preparasites of both nematode species could distinguish not only between infected and uninfected hosts, but even between different parasite loads in showing a strong preference for uninfected hosts or hosts with a low parasite load. Host heart rate declined briefly immediately after parasitism. Superparasitism resulted in increased parasite mortality. Scramble competition within mosquito larvae for limited host nutrients, coupled with a skewed sex ratio favoring males, is assumed to lead to parasite population decline and subsequently toward host-parasite population equilibrium. The ability of mermithid preparasites to accurately assess parasite load likely plays an important role in host population dynamics and regulation.

The impact of resource quality on the evolution of virulence in spatially heterogeneous environments

Understanding the drivers of parasite evolution and in particular disease virulence remains a major focus of evolutionary theory. Here, we examine the role of resource quality and in particular spatial environmental heterogeneity in the distribution of these resources on the evolution of virulence. There may be direct effects of resources on host susceptibility and pathogenicity alongside effects on reproduction that indirectly impact host-parasite population dynamics. Therefore, we assume that high resource quality may lead to both increased host reproduction and/or increased disease resistance. In completely mixed populations there is no effect of resource quality on the outcome of disease evolution. However, when there are local interactions higher resource quality generally selects for higher virulence/transmission for both linear and saturating transmission-virulence trade-off assumptions. The exception is that in castrators (i.e., infected hosts have no reproduction), higher virulence is selected for both low and high resource qualities at mixed local and global infection. Heterogeneity in the distribution of environment resources only has an effect on the outcome in castrators where random distributions generally select for higher virulence. Overall, our results further underline the importance of considering spatial structure in order to understand evolutionary processes.

Long‐term dynamics in local host–parasite interactions linked to regional population trends

AbstractTemporal changes in the relative abundances of host–parasite populations can influence the magnitude of the effects of corresponding interspecific interactions. When parasite populations are at relatively low abundance, the negative effects on host populations may be insignificant, but when parasite abundance increases beyond critical thresholds, they can have population limiting effects on the host. Here, we used data from a 40‐yr demographic study on breeding Wood Thrushes (Hylocichla mustelina) and avian brood parasitic Brown‐headed Cowbirds (Molothrus ater) in the mid‐Atlantic United States to disentangle host–parasite interactions. The relative abundance for these two species has changed both locally and regionally over this time period with a reduction in host abundance coincident with an increase in the parasite population. We detected a fivefold increase in Brown‐headed Cowbird parasitism rates of Wood Thrushes over the 40‐yr time period leading to a reduction in Wood Thrush fitness (i.e., adult survival, fecundity, and recruitment). After accounting for the effects of Wood Thrush age, individual, and annual and within‐season variation in reproduction, we found that Wood Thrushes exhibited increased reproductive effort (produced more nests per year) as nest parasitism rates increased. Additionally, we found that as parasitism rates increased, both Wood Thrush clutch size and fecundity declined. In conjunction with widespread habitat loss and land use change on both wintering and breeding ranges, increasing rates of Brown‐headed Cowbird parasitism are reducing Wood Thrush fitness, and are likely contributing to observed regional Wood Thrush population declines. Coordinated local and regional efforts to reduce Brown‐headed Cowbird populations, particularly in fragmented landscapes, may help reduce the decline for Wood Thrushes, and likely other parasitized Neotropical migratory species.

Parasite diversity drives rapid host dynamics and evolution of resistance in a bacteria-phage system.

Host–parasite evolutionary interactions are typically considered in a pairwise species framework. However, natural infections frequently involve multiple parasites. Altering parasite diversity alters ecological and evolutionary dynamics as parasites compete and hosts resist multiple infection. We investigated the effects of parasite diversity on host–parasite population dynamics and evolution using the pathogen Pseudomonas aeruginosa and five lytic bacteriophage parasites. To manipulate parasite diversity, bacterial populations were exposed for 24 hours to either phage monocultures or diverse communities containing up to five phages. Phage communities suppressed host populations more rapidly but also showed reduced phage density, likely due to interphage competition. The evolution of resistance allowed rapid bacterial recovery that was greater in magnitude with increases in phage diversity. We observed no difference in the extent of resistance with increased parasite diversity, but there was a profound impact on the specificity of resistance; specialized resistance evolved to monocultures through mutations in a diverse set of genes. In summary, we demonstrate that parasite diversity has rapid effects on host–parasite population dynamics and evolution by selecting for different resistance mutations and affecting the magnitude of bacterial suppression and recovery. Finally, we discuss the implications of phage diversity for their use as biological control agents.