Parasite Host Range Research Articles

Invading the Occupied Niche: How a Parasitic Copepod of Introduced Oysters Can Expel a Congener From Native Mussels

In species introductions, non-native species are often confronted with new niches occupied by more specialized natives, and for introduced parasites this conflict can be amplified because they also face novel hosts. Despite these obstacles, invasions of introduced parasites occur frequently, but the mechanisms that facilitate parasite invasion success are only rarely explored. Here, we investigated how the parasitic copepod Mytilicola orientalis, that recently spilled over from its principal host - the Pacific oyster Crassostrea gigas, managed to invade the niche of blue mussel Mytilus edulis intestines, which is densely occupied by its specialist congener, Mytilicola intestinalis. From field observations demonstrating invasion dynamics in nature, we designed a series of experiments addressing potential mechanisms facilitating a successful occupation of the new niche. As expected the specialist M. intestinalis can only infect mussel hosts, but displayed higher infection success there than M. orientalis in both principal host species combined. In the absence of direct competitive interactions M. orientalis compensated its lower infection success (1) by recurrent spill-over from its high-fitness reservoir oyster host, and (2) by active aggregation interference enhancing its own mating success while limiting that of M. intestinalis. The introduced parasite could thus avoid direct competition by changing its own epidemiology and indirectly decreasing the reproductive success of its competitor in the new host. Such mechanisms outside of direct competition have seldom been considered, but are crucial to understand invasion success, parasite host range and community assembly in the context of species introductions.

Parasite species richness and host range are not spatially conserved

AbstractAimInteractor richness in host–parasite networks, corresponding to either parasite species richness for host species or host range for parasite species, can be a function of taxonomic or trait constraints. Species appearing in multiple networks can have similar interactor richness in each network owing to these taxonomic and trait constraints, resulting in a spatially conserved mean interactor richness and lower variation in interaction richness relative to a null expectation. Here, we used a global database of host–helminth interactions to examine the variability in interactor richness across a spatially explicit collection of 299 host–helminth networks.LocationGlobal.Time period1800–2003.Major taxa studiedHelminth parasite species and their host species.MethodsWe used randomization tests to examine spatial conservation of species interactions for both host and helminth species.ResultsWe failed to detect a signal of interactor richness conservation for > 95% of host and helminth parasite species relative to a set of three null models, where both the mean number of interactions per species and the variation in the number of interactions per species did not differ from a random draw. Furthermore, we detected a significant taxonomic signal in divergence in parasite species richness from a null model for host species, indicating that slight departures from null expectations are related to host phylogenetic relationships.Main conclusionsOverall, this indicates that interactor richness can vary widely for the same species and that host and helminth parasite species can play very different functional roles in interaction networks across spatial or environmental gradients.

Plasmodium early transcribed membrane proteins appear tailored to the host range of malaria parasites

Early transcribed membrane proteins form a unique protein family in malaria parasites. These molecules are expressed during Plasmodium intracellular phases and inserted at the parasite parasitophorus vacuole membrane, which constitutes the host–parasite interface. Upregulated in infectious sporozoites 4 (UIS4) is an essential early transcribed membrane protein of liver stages of the murine malaria model parasite Plasmodium berghei. Despite its relevance for liver stage maturation, the molecular functions of UIS4 remain elusive, and UIS4 orthologs in human malaria parasites have not yet been identified. In order to characterise functional domains of UIS4, we generated P. berghei parasites carrying a carboxy-terminally truncated version of UIS4. We observed that uis4Δc parasites are severely impaired in liver stage development, similar to uis4(−) parasites, indicating an important role of the C-terminal domain for UIS4 function. To test whether members of the P. falciparum early transcribed membrane protein family are potential UIS4 orthologs, we selected candidates based on structural homology and parasitophorous vacuole membrane localization. We generated transgenic P. berghei parasites where UIS4 was replaced by Plasmodium falciparum ETRAMP8 or ETRAMP10.3. Both early transcribed membrane proteins were expressed in transgenic parasite lines, but liver stage maturation was impaired, indicating that the selected early transcribed membrane proteins failed to substitute the function of UIS4. As a control, we included the UIS4 ortholog from the murine parasite Plasmodium chaubaudi. We observed that PcUIS4 successfully restores UIS4 function in P. berghei. Together, these results suggest that Plasmodium parasites express tailor-made parasitophorous vacuole membrane proteins that might at least partially explain the narrow host range of malaria parasites.

Transcriptional response to host chemical cues underpins the expansion of host range in a fungal plant pathogen lineage.

The host range of parasites is an important factor in assessing the dynamics of disease epidemics. The evolution of pathogens to accommodate new hosts may lead to host range expansion, a process the molecular bases of which are largely enigmatic. The fungus Sclerotinia sclerotiorum has been reported to parasitize more than 400 plant species from diverse eudicot families while its close relative, S. trifoliorum, is restricted to plants from the Fabaceae family. We analyzed S. sclerotiorum global transcriptome reprogramming on hosts from six botanical families and reveal a flexible, host-specific transcriptional program. We generated a chromosome-level genome assembly for S. trifoliorum and found near-complete gene space conservation in two representative strains of broad and narrow host range Sclerotinia species. However, S. trifoliorum showed increased sensitivity to the Brassicaceae defense compound camalexin. Comparative analyses revealed a lack of transcriptional response to camalexin in the S. trifoliorum strain and suggest that regulatory variation in detoxification and effector genes at the population level may associate with the genetic accommodation of Brassicaceae in the Sclerotinia host range. Our work proposes transcriptional plasticity and the co-existence of signatures for generalist and polyspecialist adaptive strategies in the genome of a plant pathogen.

Prevalence and Diversity of Avian Haemosporidians May Vary with Anthropogenic Disturbance in Tropical Habitats in Myanmar

Avian malaria and related haemosporidians (genera Haemoproteus, Plasmodium and Leucocytozoon) infect most clades of bird. Although these parasites are present in almost all continents, they have been irregularly studied across different geographical regions. Despite the high bird diversity in Asia, the diversity of avian haemosporidians in this region is largely unknown. Moreover, anthropogenic changes to habitats in tropical regions may have a profound impact on the overall composition of haemosporidian communities. Here we analyzed the diversity and host association of bird haemosporidians from areas with different degrees of anthropogenic disturbance in Myanmar, revealing an unexplored diversity of these parasites (27% of newly-discovered haemosporidian lineages, and 64% of new records of host–parasite assemblages) in these tropical environments. This newly discovered diversity will be valuable for detecting host range and transmission areas of haemosporidian parasites. We also found slightly higher haemosporidian prevalence and diversity in birds from paddy fields than in individuals from urban areas and hills, thus implying that human alteration of natural environments may affect the dynamics of vector-borne diseases. These outcomes provide valuable insights for biodiversity conservation management in threatened tropical ecosystems.

Predicting patch occupancy reveals the complexity of host range expansion.

Specialized plant-insect interactions are a defining feature of life on earth, yet we are only beginning to understand the factors that set limits on host ranges in herbivorous insects. To better understand the recent adoption of alfalfa as a host plant by the Melissa blue butterfly, we quantified arthropod assemblages and plant metabolites across a wide geographic region while controlling for climate and dispersal inferred from population genomic variation. The presence of the butterfly is successfully predicted by direct and indirect effects of plant traits and interactions with other species. Results are consistent with the predictions of a theoretical model of parasite host range in which specialization is an epiphenomenon of the many barriers to be overcome rather than a consequence of trade-offs in developmental physiology.

Phylogenetic aggregation increases zoonotic potential of mammalian viruses.

While many viruses of wild mammals are capable of infecting humans, our understanding of zoonotic potential is incomplete. Viruses vary in their degree of generalism, characterized by the phylogenetic relationships of their hosts. Among the dimensions of this phylogenetic landscape, phylogenetic aggregation, which is largely overlooked in studies of parasite host range, emerges in this study as a key predictor of zoonotic status of viruses. Plausibly, viruses that exhibit aggregation, typified by discrete clusters of related host species, may (i) have been able to close the phylogenetic distance to humans, (ii) have subsequently acquired an epidemiologically relevant host and (iii) exhibit relatively high fitness in realized host communities, which are frequently phylogenetically aggregated. These mechanisms associated with phylogenetic aggregation may help explain why correlated fundamental traits, such as the ability of viruses to replicate in the cytoplasm, are associated with zoonoses.

An inverse latitudinal gradient in infection probability and phylogenetic diversity for Leucocytozoon blood parasites in New World birds.

Geographic variation in environmental conditions as well as host traits that promote parasite transmission may impact infection rates and community assembly of vector-transmitted parasites. Identifying the ecological, environmental and historical determinants of parasite distributions and diversity is therefore necessary to understand disease outbreaks under changing environments. Here, we identified the predictors and contributions of infection probability and phylogenetic diversity of Leucocytozoon (an avian blood parasite) at site and species levels across the New World. To explore spatial patterns in infection probability and lineage diversity for Leucocytozoon parasites, we surveyed 69 bird communities from Alaska to Patagonia. Using phylogenetic Bayesian hierarchical models and high-resolution satellite remote-sensing data, we determined the relative influence of climate, landscape, geography and host phylogeny on regional parasite community assembly. Infection rates and parasite diversity exhibited considerable variation across regions in the Americas. In opposition to the latitudinal gradient hypothesis, both the diversity and prevalence of Leucocytozoon parasites decreased towards the equator. Host relatedness and traits known to promote vector exposure neither predicted infection probability nor parasite diversity. Instead, the probability of a bird being infected with Leucocytozoon increased with increasing vegetation cover (NDVI) and moisture levels (NDWI), whereas the diversity of parasite lineages decreased with increasing NDVI. Infection rates and parasite diversity also tended to be higher in cooler regions and higher latitudes. Whereas temperature partially constrains Leucocytozoon diversity and infection rates, landscape features, such as vegetation cover and water body availability, play a significant role in modulating the probability of a bird being infected. This suggests that, for Leucocytozoon, the barriers to host shifting and parasite host range expansion are jointly determined by environmental filtering and landscape, but not by host phylogeny. Our results show that integrating host traits, host ancestry, bioclimatic data and microhabitat characteristics that are important for vector reproduction are imperative to understand and predict infection prevalence and diversity of vector-transmitted parasites. Unlike other vector-transmitted diseases, our results show that Leucocytozoon diversity and prevalence will likely decrease with warming temperatures.

A keeper of many crypts: a behaviour-manipulating parasite attacks a taxonomically diverse array of oak gall wasp species

Parasites of animals and plants can encounter trade-offs between their specificity to any single host and their fitness on alternative hosts. For parasites that manipulate their host's behaviour, the added complexity of that manipulation may further limit the parasite's host range. However, this is rarely tested. The recently described crypt-keeper wasp, Euderus set, changes the behaviour of the gall wasp Bassettia pallida such that B. pallida chews a significantly smaller exit hole in the side of its larval chamber and 'plugs' that hole with its head before dying. Euderus set benefits from this head plug, as it facilitates the escape of the parasitoid from the crypt after it completes development. Here, we find direct and indirect evidence that E. set attacks and manipulates the behaviour of at least six additional gall wasp species, and that these hosts are taxonomically diverse. Interestingly, each of E. set's hosts has converged upon similarities in their extended phenotypes: the galls they induce on oaks share characters that may make them vulnerable to attack by E. set. The specialization required to behaviourally manipulate hosts may be less important in determining the range of hosts in this parasitoid system than other dimensions of the host-parasitoid interaction, like the host's physical defences.

Host genetic diversity limits parasite success beyond agricultural systems: a meta-analysis.

There is evidence that human activities are reducing the population genetic diversity of species worldwide. Given the prediction that parasites better exploit genetically homogeneous host populations, many species could be vulnerable to disease outbreaks. While agricultural studies have shown the devastating effects of infectious disease in crop monocultures, the widespread nature of this diversity-disease relationship remains unclear in natural systems. Here, we provide broad support that high population genetic diversity can protect against infectious disease by conducting a meta-analysis of 23 studies, with a total of 67 effect sizes. We found that parasite functional group (micro- or macroparasite) affects the presence of the effect and study setting (field or laboratory-based environment) influences the magnitude. Our study also suggests that host genetic diversity is overall a robust defence against infection regardless of host reproduction, parasite host range, parasite diversity, virulence and the method by which parasite success was recorded. Combined, these results highlight the importance of monitoring declines of host population genetic diversity as shifts in parasite distributions could have devastating effects on at-risk populations in nature.

Nematodes and cestodes of rodents in South Africa: baseline data on diversity and geographic distribution.

Currently, descriptive information on the host range and geographic distribution of helminth parasites associated with naturally occurring rodents in South and southern Africa is scant. Therefore, we embarked on a countrywide study to: (1) identify gastrointestinal helminths and their host range, and (2) provide baseline data on the geographic distribution of helminths across the country. Altogether, 55 helminth taxa were recovered from at least 13 rodent species (n = 1030) at 26 localities across South Africa. The helminth taxa represented 25 genera (15 nematodes, nine cestodes and one acanthocephalan). Monoxenous nematodes were the most abundant and prevalent group, while the occurrence of heteroxenous nematodes and cestodes was generally lower. The study recorded several novel helminth-host associations. Single-host-species infections were common, although multiple-host-species infections by helminth species were also recorded. Monoxenous nematodes and some cestodes were recovered countrywide, whereas heteroxenous nematodes were restricted to the eastern regions of South Africa. The study highlights the as yet unexplored diversity of helminth species associated with naturally occurring rodent species and provides initial data on their geographical distribution in South Africa.

Food web structure selects for parasite host range.

Complex life cycle parasites, including helminths, use intermediate hosts for development and definitive hosts for reproduction, with interactions between the two host types governed by food web structure. I study how a parasite's intermediate host range is controlled by the diet breadth of definitive host species and the cost of parasite generalism, a putative fitness cost that assumes host range trades off against fitness derived from a host species. In spite of such costs, a benefit to generalism may occur when the definitive host exhibits a large diet breadth, enhancing transmission of generalist parasites via consumption of a broad array of infected intermediate hosts. I develop a simple theoretical model to demonstrate how different host range infection strategies are differentially selected for across a gradient of definitive host diet breadth according to the cost of generalism. I then use a parasitic helminth-host database in conjunction with a food web database to show that diet breadth of definitive hosts promotes generalist infection strategies at the intermediate host level, indicating relatively low costs of parasite generalism among helminths.

Gender bias when interacting with avatars

Within host communities, related species are more likely to share common parasitic agents, and as a result, morphological similarities have led researchers to conclude that parasites infecting closely related hosts within a community represent a single species. However, genetic diversity within parasite genera and host range remain poorly investigated in most systems. Strongyloides is a genus of soil-transmitted nematode that has been reported from several primate species in Africa and Asia, and has been estimated to infect hundreds of millions of people worldwide, although no precise estimates are available. Here we describe a case of infection with a cryptic species of Strongyloides in a Bornean (Philippine) slow loris (Nycticebus menagensis) living within a diverse community of several primate species in the Lower Kinabatangan Wildlife Sanctuary, Malaysian Borneo. Fresh fecal samples were collected from five primate species and nematode larvae cultured from these samples were selected for phylogenetic analyses. Sequences obtained for most larvae were identified as S. fuelleborni, grouping into three different clusters and showing no aggregation within specific hosts or geographic location. In contrast, a set of parasite sequences obtained from a slow loris clustered closely with S. stercoralis into a different group, being genetically distinct to sequences reported from other primate hosts, humans included. Our results suggest that although S. fuelleborni infects all haplorrhines sampled in this primate community, a different species might be infecting the slow loris, the only strepsirrhine in Borneo and one of the least studied primates in the region. Although more data are needed to support this conclusion, we propose that Strongyloides species in primates might be more diverse than previously thought, with potential implications for ecological and evolutionary host-parasite associations, as well as epidemiological dynamics.

High prevalence and narrow host range of haemosporidian parasites in Godlewski's bunting (Emberiza godlewskii) in northern China

Avian haemosporidian parasites are highly diverse, have a wide range of host specificity, and reveal diverse compatibility with regard to host range and geographical distribution. Therefore, understanding haemosporidian parasite diversity in different host species and different regions is crucial. A survey of the haemosporidian parasite in 186 Godlewski's buntings in Beijing was conducted to compare infection patterns between Godlewski's bunting, local passerines and the global avian host. High prevalence (88.7%) was found in the bunting and displayed annual stability during the research period. Most of the infections were caused by four dominant lineages, three of which were clustered with lineages of morphological species. In comparison with other lineages in local passerines, the dominant lineages were relative specialists. The findings suggest that the compatibility of dominant lineages in the bunting hosts may play important roles in high haemosporidian prevalence, and the narrow host range of the dominant lineages may be due to coevolution between the parasites and host species.

Lurking in the dark: Cryptic Strongyloides in a Bornean slow loris.

Within host communities, related species are more likely to share common parasitic agents, and as a result, morphological similarities have led researchers to conclude that parasites infecting closely related hosts within a community represent a single species. However, genetic diversity within parasite genera and host range remain poorly investigated in most systems. Strongyloides is a genus of soil-transmitted nematode that has been reported from several primate species in Africa and Asia, and has been estimated to infect hundreds of millions of people worldwide, although no precise estimates are available. Here we describe a case of infection with a cryptic species of Strongyloides in a Bornean (Philippine) slow loris (Nycticebus menagensis) living within a diverse community of several primate species in the Lower Kinabatangan Wildlife Sanctuary, Malaysian Borneo. Fresh fecal samples were collected from five primate species and nematode larvae cultured from these samples were selected for phylogenetic analyses. Sequences obtained for most larvae were identified as S. fuelleborni, grouping into three different clusters and showing no aggregation within specific hosts or geographic location. In contrast, a set of parasite sequences obtained from a slow loris clustered closely with S. stercoralis into a different group, being genetically distinct to sequences reported from other primate hosts, humans included. Our results suggest that although S. fuelleborni infects all haplorrhines sampled in this primate community, a different species might be infecting the slow loris, the only strepsirrhine in Borneo and one of the least studied primates in the region. Although more data are needed to support this conclusion, we propose that Strongyloides species in primates might be more diverse than previously thought, with potential implications for ecological and evolutionary host-parasite associations, as well as epidemiological dynamics.

Babesia vesperuginis, a neglected piroplasmid: new host and geographical records, and phylogenetic relations

BackgroundBabesia spp. are hemoparasites which infect the red blood cells of a large variety of mammals. In bats, the only known species of the genus is Babesia vesperuginis. However, except a few old reports, the host range and geographical distribution of this bat parasite have been poorly studied. This study aimed to investigate the presence of piroplasms in tissues of bats collected in four different countries from eastern and central Europe: Austria, Czech Republic, Hungary and Romania.MethodsA total of 461 bat carcasses (24 species) were collected between 2001 and 2016 from caves, mines and buildings. PCR was performed using specific primers targeting a portion of the 18S rDNA nuclear gene and cytochrome c oxidase subunit 1 mitochondrial gene, followed by sequencing.ResultsThe results of this study show for the first time the presence of B. vesperuginis in bats in central and eastern Europe. The phylogenetic analysis of the 18S rDNA nuclear gene revealed no variability between the sequences and the phylogenetic analysis of the cox1 mitochondrial gene proved that B. vesperuginis could be divided into two subclades.ConclusionOur study showed a broad geographical distribution of B. vesperuginis in European bats, reporting its presence in five new host species (M. cf. alcathoe, M. bechsteinii, M. myotis, Pi. nathusii and V. murinus) and three new countries.

Estimating parasite host range.

Estimating the number of host species that a parasite can infect (i.e. host range) provides key insights into the evolution of host specialism and is a central concept in disease ecology. Host range is rarely estimated in real systems, however, because variation in species relative abundance and the detection of rare species makes it challenging to confidently estimate host range. We applied a non-parametric richness indicator to estimate host range in simulated and empirical data, allowing us to assess the influence of sampling heterogeneity and data completeness. After validating our method on simulated data, we estimated parasite host range for a sparsely sampled global parasite occurrence database (Global Mammal Parasite Database) and a repeatedly sampled set of parasites of small mammals from New Mexico (Sevilleta Long Term Ecological Research Program). Estimation accuracy varied strongly with parasite taxonomy, number of parasite occurrence records, and the shape of host species-abundance distribution (i.e. the dominance and rareness of species in the host community). Our findings suggest that between 20% and 40% of parasite host ranges are currently unknown, highlighting a major gap in our understanding of parasite specificity, host-parasite network structure, and parasite burdens.

A review on epidemiology, global prevalence and economical losses of fasciolosis in ruminants.

Fasciolosis is an important plant borne trematode zoonosis in ruminants caused by the Fasciola hepatica and Fasciola gigentica, It is classified as a neglected tropical disease and found in more than 50 countries especially where sheep and cattle are reared. Fasciolosis is a serious animal health problems in many rural and urban areas of world, causing significant financial losses due to decrease in production and viscera condemnation in animals. Accurate diagnosis of fasciolosis is always remained a challenging task for the field practitioners. There is no comprehensive summary on the occurrence and distribution of the infection at international level. Therefore, we intended to provide a complete overview on the prevalence and epidemiology of fasciolosis in farm animals from a global prospective. It includes to map the global distribution of fasciolosis in different areas of the world to identify the endemic regions which may be a source of potential disease outbreak. The financial liability related to fasciolosis on the livestock production has also been addressed. For this purpose, the published data during 2000-2015 (15 years) on fasciolosis was reviewed and collected by electronic literature search of four databases including Google, PubMed, Science Direct, and Web of Science. Data presented are contemplated to enhance our current understanding of the parasite's geographical distribution, host range, and economic losses. Information provided would be useful for the application of more effective control strategies against fasciolosis in different geo-economics regions of the world.

Novel application of species richness estimators to predict the host range of parasites

Host range is a critical life history trait of parasites, influencing prevalence, virulence and ultimately determining their distributional extent. Current approaches to measure host range are sensitive to sampling effort, the number of known hosts increasing with more records. Here, we develop a novel application of results-based stopping rules to determine how many hosts should be sampled to yield stable estimates of the number of primary hosts within regions, then use species richness estimation to predict host ranges of parasites across their distributional ranges. We selected three mistletoe species (hemiparasitic plants in the Loranthaceae) to evaluate our approach: a strict host specialist (Amyema lucasii, dependent on a single host species), an intermediate species (Amyema quandang, dependent on hosts in one genus) and a generalist (Lysiana exocarpi, dependent on many genera across multiple families), comparing results from geographically-stratified surveys against known host lists derived from herbarium specimens. The results-based stopping rule (stop sampling bioregion once observed host richness exceeds 80% of the host richness predicted using the Abundance-based Coverage Estimator) worked well for most bioregions studied, being satisfied after three to six sampling plots (each representing 25 host trees) but was unreliable in those bioregions with high host richness or high proportions of rare hosts. Although generating stable predictions of host range with minimal variation among six estimators trialled, distribution-wide estimates fell well short of the number of hosts known from herbarium records. This mismatch, coupled with the discovery of nine previously unrecorded mistletoe-host combinations, further demonstrates the limited ecological relevance of simple host-parasite lists. By collecting estimates of host range of constrained completeness, our approach maximises sampling efficiency while generating comparable estimates of the number of primary hosts, with broad applicability to many host-parasite systems.

Predictability of helminth parasite host range using information on geography, host traits and parasite community structure.

Host-parasite associations are complex interactions dependent on aspects of hosts (e.g. traits, phylogeny or coevolutionary history), parasites (e.g. traits and parasite interactions) and geography (e.g. latitude). Predicting the permissive host set or the subset of the host community that a parasite can infect is a central goal of parasite ecology. Here we develop models that accurately predict the permissive host set of 562 helminth parasites in five different parasite taxonomic groups. We developed predictive models using host traits, host taxonomy, geographic covariates, and parasite community composition, finding that models trained on parasite community variables were more accurate than any other covariate group, even though parasite community covariates only captured a quarter of the variance in parasite community composition. This suggests that it is possible to predict the permissive host set for a given parasite, and that parasite community structure is an important predictor, potentially because parasite communities are interacting non-random assemblages.