Nomenclatural stability and the longevity of helminth species names.

Although most Latin binomial names of species are valid, many are eventually unaccepted when they are found to be synonyms of previously described species, or superseded by a new combination when the species they denote are moved to a different genus. What proportion of parasite species names become unaccepted over time, and how long does it take for incorrect names to become unaccepted? Here, we address these questions using a dataset comprising thousands of species names of parasitic helminths from four higher taxa (Acanthocephala, Nematoda, Cestoda, and Trematoda). Overall, among species names proposed in the past two-and-a-half centuries, nearly one-third have since been unaccepted, the most common reason being that they have been superseded by a new combination. A greater proportion of older names (proposed pre-1950) have since been unaccepted compared to names proposed more recently, however most taxonomic acts leading to species names being unaccepted (through either synonymy or reclassification) occurred in the past few decades. Overall, the average longevity of helminth species names that are currently unaccepted was 29 years; although many remained in use for over 100 years, about 50% of the total were invalidated within 20 years of first being proposed. The patterns observed were roughly the same for all four higher helminth taxa considered here. Our results provide a quantitative illustration of the self-correcting nature of parasite taxonomy, and can also help to calibrate future estimates of total parasite biodiversity.

Genome assembly and annotation of the mermithid nematode Mermis nigrescens.

Genetic studies of nematodes have been dominated by Caenorhabditis elegans as a model species. A lack of genomic resources has limited the expansion of genetic research to other groups of nematodes. Here, we report a draft genome assembly of a mermithid nematode, Mermis nigrescens. Mermithidae are insect parasitic nematodes with hosts including a wide range of terrestrial arthropods. We sequenced, assembled, and annotated the whole genome of M. nigrescens using nanopore long reads and 10X Chromium link reads. The assembly is 524 Mb in size consisting of 867 scaffolds. The N50 value is 2.42 Mb, and half of the assembly is in the 30 longest scaffolds. The assembly BUSCO score from the eukaryotic database (eukaryota_odb10) indicates that the genome is 86.7% complete and 5.1% partial. The genome has a high level of heterozygosity (6.6%) with a repeat content of 83.98%. mRNA-seq reads from different sized nematodes (≤2 cm, 3.5-7 cm, and >7 cm body length) representing different developmental stages were also generated and used for the genome annotation. Using ab initio and evidence-based gene model predictions, 12,313 protein-coding genes and 24,186 mRNAs were annotated. These genomic resources will help researchers investigate the various aspects of the biology and host-parasite interactions of mermithid nematodes.

Vector species richness predicts local mortality rates from Chagas disease.

Vector species richness may drive the prevalence of vector-borne diseases by influencing pathogen transmission rates. The dilution effect hypothesis predicts that higher biodiversity reduces disease prevalence, but with inconclusive evidence. In contrast, the amplification effect hypothesis suggests that higher vector diversity may result in greater disease transmission by increasing and diversifying the transmission pathways. The relationship between vector diversity and pathogen transmission remains unclear and requires further study. Chagas disease is a vector-borne disease most prevalent in Brazil and transmitted by multiple species of insect vectors of the subfamily Triatominae, yet the drivers of spatial variation in its impact on human populations remain unresolved. We tested whether triatomine species richness, latitude, bioclimatic variables, human host population density, and socioeconomic variables predict Chagas disease mortality rates across over 5000 spatial grid cells covering all of Brazil. Results show that species richness of triatomine vectors is a good predictor of mortality rates caused by Chagas disease, which supports the amplification effect hypothesis. Vector richness and the impact of Chagas disease may also be driven by latitudinal components of climate and human socioeconomic factors. We provide evidence that vector diversity is a strong predictor of disease prevalence and give support to the amplification effect hypothesis.

Global analysis of seasonal changes in trematode infection levels reveals weak and variable link to temperature.

Seasonal changes in environmental conditions drive phenology, i.e., the annual timing of biological events ranging from the individual to the ecosystem. Phenological patterns and successional abundance cycles have been particularly well studied in temperate freshwater systems, showing strong and predictable synchrony with seasonal changes. However, seasonal successional changes in the abundance of parasites or their infection levels in aquatic hosts have not yet been shown to follow universal patterns. Here, using a compilation of several hundred estimates of spring-to-summer changes in infection by trematodes in their intermediate and definitive hosts, spanning multiple species and habitats, we test for general patterns of seasonal (temperature) driven changes in infection levels. The data include almost as many decreases in infection levels from spring to summer as there are increases, across different host types. Our results reveal that the magnitude of the spring-to-summer change in temperature had a weak positive effect on the concurrent change in prevalence of infection in first intermediate hosts, but no effect on the change in prevalence or abundance of infection in second intermediate or definitive hosts. This was true across habitat types and host taxa, indicating no universal effect of seasonal temperature increase on trematode infections. This surprising variation across systems suggests a predominance of idiosyncratic and species-specific responses in trematode infection levels, at odds with any clear phenological or successional pattern. We discuss possible reasons for the minimal and variable effect of seasonal temperature regimes, and emphasise the challenges this poses for predicting ecosystem responses to future climate change.

Trematode genetic patterns at host individual and population scales provide insights about infection mechanisms.

Multiple parasites can infect a single host, creating a dynamic environment where each parasite must compete over host resources. Such interactions can cause greater harm to the host than single infections and can also have negative consequences for the parasites themselves. In their first intermediate hosts, trematodes multiply asexually and can eventually reach up to 20% of the host's biomass. In most species, it is unclear whether this biomass results from a single infection or co-infection by 2 or more infective stages (miracidia), the latter being more likely a priori in areas where prevalence of infection is high. Using as model system the trematode Bucephalus minimus and its first intermediate host cockles, we examined the genetic diversity of the cytochrome c oxidase subunit I region in B. minimus from 3 distinct geographical areas and performed a phylogeographic study of B. minimus populations along the Northeast Atlantic coast. Within localities, the high genetic variability found across trematodes infecting different individual cockles, compared to the absence of variability within the same host, suggests that infections could be generally originating from a single miracidium. On a large spatial scale, we uncovered significant population structure of B. minimus, specifically between the north and south of Bay of Biscay. Although other explanations are possible, we suggest this pattern may be driven by the population structure of the final host.

Model worms: knowledge gains and risks associated with the use of model species in parasitological research.

Model parasite species, whose entire life cycle can be completed in the laboratory and maintained for multiple generations, have played a fundamental role in our understanding of host­parasite interactions. Yet, keeping parasites in laboratory conditions may expose them to unnatural evolutionary pressures, and using laboratory cultures for research is therefore not without limitations. Using 2 widely-used model helminth species, the cestode Hymenolepis diminuta and the nematode Heligmosomoides polygyrus, I illustrate the caution needed when interpreting experimental results on model species. I first review more than 1200 experimental studies published on these species in the past 4 decades, to determine which research areas they have contributed to. This is followed by an examination of the institutional laboratory cultures that have provided the parasites used in these studies. Some of these have persisted for decades and accounted for a substantial proportion of published studies, whereas others have been short-lived. Using information provided by the curators of active cultures, I summarize data on their origins and maintenance conditions. Finally, I discuss how laboratory cultures may have been subject to the influence of evolutionary genetic processes, such as founder effects, genetic drift and inbreeding. I also address the possibility that serial passage through laboratory hosts across multiple generations has exerted artificial selection on several parasite traits, resulting in genetic and phenotypic divergence among laboratory cultures, and between these cultures and natural parasite populations. I conclude with recommendations for the continued usage of laboratory helminth cultures aimed at maximizing their important contribution to parasitological research.

Light pollution may alter host-parasite interactions in aquatic ecosystems.

With growing human populations living along freshwater shores and marine coastlines, aquatic ecosystems are experiencing rising levels of light pollution. Through its effects on hosts and parasites, anthropogenic light at night can disrupt host-parasite interactions evolved under a normal photoperiod. Yet its impact on aquatic parasites has been ignored to date. Here, I discuss the direct effects of light on the physiology and behaviour of parasite infective stages and their hosts. I argue that night-time lights can change the spatiotemporal dynamics of infection risk and drive the rapid evolution of parasites. I then highlight knowledge gaps and how impacts on parasitic diseases should be incorporated into the design of measures aimed at mitigating the impact of anthropogenic light on wildlife.

Different trematode parasites in the same snail host: Species-specific or shared microbiota?

The concept that microbes associated with macroorganisms evolve as a unit has swept evolutionary ecology. However, this idea is controversial due to factors such as imperfect vertical transmission of microbial lineages and high microbiome variability among conspecific individuals of the same population. Here, we tested several predictions regarding the microbiota of four trematodes (Galactosomum otepotiense, Philophthalmus attenuatus, Acanthoparyphium sp. and Maritrema novaezealandense) that parasitize the same snail host population. We predicted that each parasite species would harbour a distinct microbiota, with microbial composition similarity decreasing with increasing phylogenetic distance among parasite species. We also predicted that trematode species co-infecting the same individual host would influence each other's microbiota. We detected significant differences in alpha and beta diversity, as well as differential abundance, in the microbiota of the four trematode species. We found no evidence that phylogenetically closely related trematodes had more similar microbiota. We also uncovered indicator bacterial taxa that were significantly associated with each trematode species. Trematode species sharing the same snail host showed evidence of mostly one-sided bacterial exchanges, with the microbial community of one species approaching that of the other. We hypothesize that natural selection acting on specific microbial lineages may be important to maintain differences in horizontally acquired microbes, with vertical transmission also playing a role. In particular, one trematode species had a more consistent and diverse bacteriota than the others, potentially a result of stronger stabilizing pressures. We conclude that species-specific processes shape microbial community assembly in different trematodes exploiting the same host population.

Adoption of alternative life cycles in a parasitic trematode is linked to microbiome differences.

For parasites with complex multi-host life cycles, the facultative truncation of the cycle represents an adaptation to challenging conditions for transmission. However, why certain individuals are capable of abbreviating their life cycle while other conspecifics are not remains poorly understood. Here, we test whether conspecific trematodes that either follow the normal three-host life cycle or skip their final host by reproducing precociously (via progenesis) in an intermediate host differ in the composition of their microbiomes. Characterization of bacterial communities based on sequencing of the V4 hypervariable region of the 16S SSU rRNA gene revealed that the same bacterial taxa occur in both normal and progenetic individuals, independent of host identity and temporal variation. However, all bacterial phyla recorded in our study, and two-thirds of bacterial families, differed in abundance between the two morphs, with some achieving higher abundance in the normal morph and others in the progenetic morph. Although the evidence is purely correlative, our results reveal a weak association between microbiome differences and intraspecific plasticity in life cycle pathways. Advances in functional genomics and experimental microbiome manipulation will allow future tests of the significance of these findings.

Biases in parasite biodiversity research: why some helminth species attract more research than others.

As the number of known and described parasite species grows every year, one might ask: how much do we actually know about these species beyond the fact they exist? For free-living taxa, research effort is biased toward a small subset of species based on their properties or human-centric factors. Here, using a large data set on over 2500 helminth parasite species described in the past two decades, we test the importance of several predictors on two measures of research effort: the number of times a species description is cited following its publication, and the number of times a species' name is mentioned in the scientific literature. Our analysis highlights some taxonomic biases: for instance, descriptions of acanthocephalans and nematodes tend to receive more citations than those of other helminths, and species of cestodes are less frequently mentioned in the literature than other helminths. We also found that helminths infecting host species of conservation concern receive less research attention, perhaps because of the constraints associated with research on threatened animals, while those infecting host species of human use receive greater research effort. Intriguingly, we found that species originally described by many co-authors subsequently attract more research effort than those described by one or few authors, and that research effort correlates negatively with the human population size of the country where a species was discovered, but not with its economic strength, measured by its gross domestic product. Overall, our findings reveal that we have conducted very little research, or none at all, on the majority of helminth parasite species following their discovery. The biases in study effort we identify have serious implications for future research into parasite biodiversity and conservation.

Physical evidence of direct antagonistic interactions between trematodes in the host gut: the kiss of death?

Although within-host competition among parasites if often assumed to occur based on statistical patterns, actual physical evidence of direct antagonistic interactions between parasites, either intraspecific or interspecific, is very rare. Here, we report such evidence between and within two species of hemiurid trematodes infecting the deep-sea grenadier fish Coryphaenoides subserrulatus. We found pairs of worms attached together, with one worm using its ventral sucker against another worm, and sucking out a large protuberance on the victim. We also found single worms showing clear signs of past attacks. There was no evidence that these interactions were more common at high intensities of infection, where the conditions would be expected to be more conducive to competitive interactions. Our findings provide evidence that trematodes may cause some harm to co-occurring individuals, suggesting a direct form of interference competition among intestinal helminths.

Effects of forest loss and fragmentation on bat-ectoparasite interactions.

Human land use causes habitat loss and fragmentation, influencing host-parasite associations through changes in infestation rates, host mortality and possibly local extinction. Bat-ectoparasite interactions are an important host-parasite model possibly affected by such changes, as this system acts as both reservoirs and vectors of several pathogens that can infect different wild and domestic species. This study aimed to assess how the prevalence and abundance of bat ectoparasites respond to forest loss, fragmentation, and edge length. Bats and ectoparasites were sampled at twenty sites, forming a gradient of forest cover, in southwestern Brazil during two wet (2015 and 2016) and two dry (2016 and 2017) seasons. Effects of landscape metrics on host abundance as well as parasite prevalence and abundance were assessed through structural equation models. Nine host-parasite associations provided sufficient data for analyses, including one tick and eight flies on four bat species. Forest cover positively influenced the prevalence or abundance of three fly species, but negatively influenced one fly and the tick species. Prevalence or abundance responded positively to edge length for three fly species, and negatively for the tick. In turn, number of fragments influenced the prevalence or abundance of four fly species, two positively and two negatively. Our results support species-specific responses of ectoparasites to landscape features, and a tendency of host-generalist ticks to benefit from deforestation while most host-specialist flies are disadvantaged. Differences in host traits and abundance, along with parasite life cycles and environmental conditions, are possible explanations to our findings.

Battle of the sexes: analysis of sex bias in host use and reporting practices in parasitological experiments.

Experimental approaches are among the most powerful tools available to biologists, yet in many disciplines their results have been questioned due to an underrepresentation of female animal subjects. In parasitology, experiments are crucial to understand host-parasite interactions, parasite development, host immune responses, as well as the efficacy of different control methods. However, distinguishing between species-wide and sex-specific effects requires the balanced inclusion of both male and female hosts in experiments and the reporting of results for each sex separately. Here, using data from over 3600 parasitological experiments on helminth-mammal interactions published in the past four decades, we investigate patterns of male versus female subject use and result reporting practices in experimental parasitology. We uncover multiple effects of the parasite taxon used, the type of host used (rats and mice for which subject selection is fully under researcher control versus farm animals), the research subject area and the year of publication, on whether host sex is even specified, whether one or both host sexes have been used (and if only one then which one), and whether the results are presented separately for each host sex. We discuss possible reasons for biases and unjustifiable selection of host subjects, and for poor experimental design and reporting of results. Finally, we make some simple recommendations for increased rigour in experimental design and to reset experimental approaches as a cornerstone of parasitological research.

Tracking life cycles of parasites across a broad taxonomic scale in a marine ecosystem.

Parasitic helminths exhibit remarkable diversity in their life cycles, although few parasite species have their whole life cycles resolved. Owing to the fact that parasite life stages within hosts are often not comparable using morphological data, genetic data provides convincing evidence of transmission pathways between intermediate and definitive hosts. We took this approach to an ecosystem level, genetically matching parasite (acanthocephalan, cestode, nematode and trematode) life stages across a broad taxonomic range of intermediate and definitive hosts (invertebrates, seabirds, elasmobranchs and teleost fish) in Otago's (New Zealand) coastal marine ecosystem. We identified which transmission routes are utilized by the most parasite species and assessed which intermediate hosts are most important in facilitating the transmission of parasites in this ecosystem. Our findings reveal 59 new records of larval parasites infecting their respective intermediate hosts and 289 transmission pathways utilized by 35 helminth species to complete their life cycles. Sprat, triplefin and arrow squid all hosted the highest number of larval parasite species, suggesting they play important roles as intermediate hosts. We then used the new life cycle data to provide a synthetic overview of the life cycles known for various parasite groups in New Zealand. This study highlights how studying parasite life cycles can enhance our understanding of the ecology and evolution of parasites and hosts in natural systems, beyond simply resolving life cycles.

The proof is in the poo: Non-invasive method to detect endoparasitic infection.

Almost every animal trait is strongly associated with parasitic infection or the potential exposure to parasites. Despite this importance, one of the greatest challenges that researchers still face is to accurately determine the status and severity of the endoparasitic infection without killing and dissecting the host. Thus, the precise detection of infection with minimal handling of the individual will improve experimental designs in live animal research. Here, we quantified extracellular DNA from two species of endoparasitic worm that grow within the host body cavity, hairworms (phylum Nematomorpha) and mermithids (phylum Nematoda), from the frass of their insect host, a cave weta (Orthoptera: Rhaphidophoridae) and an earwig (Dermaptera: Forficulidae), respectively. Frass collection was done at two successive time periods, to test if parasitic growth correlated with relative DNA quantity in the frass. We developed and optimized two highly specific TaqMan assays, one for each parasite-specific DNA amplification. We were able to detect infection prevalence with 100% accuracy in individuals identified as infected through post-study dissections. An additional infection in earwigs was detected with the TaqMan assay alone, probably because some worms were either too small or degraded to observe during dissection. No difference in DNA quantity was detected between sampling periods, although future protocols could be refined to support such a trend. This study demonstrates that a noninvasive and minimally stressful method can be used to detect endoparasitic infection with greater accuracy than dissection alone, helping improve protocols for live animal studies.

Assigning cause for emerging diseases of aquatic organisms.

Resolving the cause of disease (= aetiology) in aquatic organisms is a challenging but essential goal, heightened by increasing disease prevalence in a changing climate and an interconnected world of anthropogenic pathogen spread. Emerging diseases play important roles in evolutionary ecology, wildlife conservation, the seafood industry, recreation, cultural practices, and human health. As we emerge from a global pandemic of zoonotic origin, we must focus on timely diagnosis to confirm aetiology and enable response to diseases in aquatic ecosystems. Those systems' resilience, and our own sustainable use of seafood, depend on it. Synchronising traditional and recent advances in microbiology that span ecological, veterinary, and medical fields will enable definitive assignment of risk factors and causal agents for better biosecurity management and healthier aquatic ecosystems.

Vector microbiome: will global climate change affect vector competence and pathogen transmission?

Vector-borne diseases are among the greatest causes of human suffering globally. Several studies have linked climate change and increasing temperature with rises in vector abundance, and in the incidence and geographical distribution of diseases. The microbiome of vectors can have profound effects on how efficiently a vector sustains pathogen development and transmission. Growing evidence indicates that the composition of vectors' gut microbiome might change with shifts in temperature. Nonetheless, due to a lack of studies on vector microbiome turnover under a changing climate, the consequences for vector-borne disease incidence are still unknown. Here, we argue that climate change effects on vector competence are still poorly understood and the expected increase in vector-borne disease transmission might not follow a relationship as simple and straightforward as past research has suggested. Furthermore, we pose questions that are yet to be answered to enhance our current understanding of the effect of climate change on vector microbiomes, competence, and, ultimately, vector-borne diseases transmission.

Historical dispersal and host-switching formed the evolutionary history of a globally distributed multi-host parasite - The Ligula intestinalis species complex.

Studies on parasite biogeography and host spectrum provide insights into the processes driving parasite diversification. Global geographical distribution and a multi-host spectrum make the tapeworm Ligula intestinalis a promising model for studying both the vicariant and ecological modes of speciation in parasites. To understand the relative importance of host association and biogeography in the evolutionary history of this tapeworm, we analysed mtDNA and reduced-represented genomic SNP data for a total of 139 specimens collected from 18 fish-host genera across a distribution range representing 21 countries. Our results strongly supported the existence of at least 10 evolutionary lineages and estimated the deepest divergence at approximately 4.99-5.05 Mya, which is much younger than the diversification of the fish host genera and orders. Historical biogeography analyses revealed that the ancestor of the parasite diversified following multiple vicariance events and was widespread throughout the Palearctic, Afrotropical, and Nearctic between the late Miocene and early Pliocene. Cyprinoids were inferred as the ancestral hosts for the parasite. Later, from the late Pliocene to Pleistocene, new lineages emerged following a series of biogeographic dispersal and host-switching events. Although only a few of the current Ligula lineages show narrow host-specificity (to a single host genus), almost no host genera, even those that live in sympatry, overlapped between different Ligula lineages. Our analyses uncovered the impact of historical distribution shifts on host switching and the evolution of host specificity without parallel host-parasite co-speciation. Historical biogeography reconstructions also found that the parasite colonized several areas (Afrotropical and Australasian) much earlier than was suggested by only recent faunistic data.

Resetting our expectations for parasites and their effects on species interactions: a meta-analysis.

Despite the ubiquitous nature of parasitism, how parasitism alters the outcome of host-species interactions such as competition, mutualism and predation remains unknown. Using a phylogenetically informed meta-analysis of 154 studies, we examined how the mean and variance in the outcomes of species interactions differed between parasitized and non-parasitized hosts. Overall, parasitism did not significantly affect the mean or variance of host-species interaction outcomes, nor did the shared evolutionary histories of hosts and parasites have an effect. Instead, there was considerable variation in outcomes, ranging from strongly detrimental to strongly beneficial for infected hosts. Trophically-transmitted parasites increased the negative effects of predation, parasites increased and decreased the negative effects of interspecific competition for parasitized and non-parasitized heterospecifics, respectively, and parasites had particularly strong negative effects on host species interactions in freshwater and marine habitats, yet were beneficial in terrestrial environments. Our results illuminate the diverse ways in which parasites modify critical linkages in ecological networks, implying that whether the cumulative effects of parasitism are considered detrimental depends not only on the interactions between hosts and their parasites but also on the many other interactions that hosts experience.

Inter-individual variation in parasite manipulation of host phenotype: A role for parasite microbiomes?

Alterations in host phenotype induced by metazoan parasites are widespread in nature, yet the underlying mechanisms and the sources of intraspecific variation in the extent of those alterations remain poorly understood. In light of the microbiome revolution sweeping through ecology and evolutionary biology, we hypothesise that the composition of symbiotic microbial communities living within individual parasites influences the nature and extent of their effect on host phenotype. The interests of both the parasite and its symbionts are aligned through the latter's vertical transmission, favouring joint contributions to the manipulation of host phenotype. Our hypothesis can explain the variation in the extent to which parasites alter host phenotype, as microbiome composition varies among individual parasites. We propose two non-exclusive approaches to test the hypothesis, furthering the integration of microbiomes into studies of host-parasite interactions.