Assessing global drivers of parasite diversity: host diversity and body mass boost avian haemosporidian diversity.

Biodiversity varies worldwide and is influenced by multiple factors, such as environmental stability and past historical events (e.g. Panama Isthmus). At the same time, organisms with unique life histories (e.g. parasites) are subject to unique selective pressures that structure their diversity patterns. Parasites represent one of the most successful life strategies, impacting, directly and indirectly, ecosystems by cascading effects on host fitness and survival. Here, I focused on a highly diverse, prevalent and cosmopolitan group of parasites (avian haemosporidians) to investigate the main drivers (e.g. host and environmental features) of regional parasite diversity on a global scale. To do so, I compiled data from 4 global datasets on (i) avian haemosporidian (malaria and malaria-like) parasites, (ii) bird species diversity, (iii) avian functional traits and (iv) climate data. Then, using generalized least square models, I evaluated the effect of host and environmental features on haemosporidian diversity. I found that haemosporidian diversity mirrors host regional diversity and that higher host body mass increases haemosporidian diversity. On the other hand, climatic conditions had no effect on haemosporidian diversity in any model. When evaluating Leucocytozoon parasites separately, I found parasite diversity was boosted by a higher proportion of migratory hosts. In conclusion, I demonstrated that haemosporidian parasite diversity is intrinsically associated with their hosts' diversity and body mass.

Co-infection with Leucocytozoon and Other Haemosporidian Parasites Increases with Latitude and Altitude in New World Bird Communities.

Establishing how environmental gradients and host ecology drive spatial variation in infection rates and diversity of pathogenic organisms is one of the central goals in disease ecology. Here, we identified the predictors of concomitant infection and lineage richness of blood parasites in New Word bird communities. Our multi-level Bayesian models revealed that higher latitudes and elevations played a determinant role in increasing the probability of a bird being co-infected with Leucocytozoon and other haemosporidian parasites. The heterogeneity in both single and co-infection rates was similarly driven by host attributes and temperature, with higher probabilities of infection in heavier migratory host species and at cooler localities. Latitude, elevation, host body mass, migratory behavior, and climate were also predictors of Leucocytozoon lineage richness across the New World avian communities, with decreasing parasite richness at higher elevations, rainy and warmer localities, and in heavier and resident host species. Increased parasite richness was found farther from the equator, confirming a reverse Latitudinal Diversity Gradient pattern for this parasite group. The increased rates of Leucocytozoon co-infection and lineage richness with increased latitude are in opposition with the pervasive assumption that pathogen infection rates and diversity are higher in tropical host communities.

Host phylogeny and seasonality shapes avian haemosporidian prevalence in a Brazilian biodiverse and dry forest: the Caatinga.

The relationships between host phylogenetics, functional traits and parasites in wildlife remain poorly understood in the Neotropics, especially in habitats with marked seasonal variation. Here, we examined the effect of seasonality and host functional traits on the prevalence of avian haemosporidians (Plasmodium and Haemoproteus) in the Brazilian Caatinga, a seasonally dry tropical forest. 933 birds were evaluated for haemosporidian infections. We found a high parasitism prevalence (51.2%), which was correlated with phylogenetic relatedness among avian species. Prevalence varied drastically among the 20 well-sampled species, ranging from 0 to 70%. Seasonality was the main factor associated with infections, but how this abiotic condition influenced parasite prevalence varied according to the host-parasite system. Plasmodium prevalence increased during the rainy season and, after excluding the large sample size of Columbiformes (n = 462/933), Plasmodium infection rate was maintained high in the wet season and showed a negative association with host body mass. No association was found between non-Columbiform bird prevalence and seasonality or body mass when evaluating both Plasmodium and Haemoproteus or only Haemoproteus infections. Parasite community was composed of 32 lineages including 7 new lineages. We evidenced that even dry domains can harbour a high prevalence and diversity of vector-borne parasites and pointed out seasonality as a ruling factor.

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.

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.

Functional and sex-specific dynamics of ectoparasite size evolution in marine isopod-fish interactions: Harrison's rule and increasing variance.

Harrison's rule, a pattern predicting that the body size of parasites correlates positively with the size of their hosts, is well-supported. However, its interaction with highly distinct "guilds" of closely related parasites warrants further exploration. The increasing variance hypothesis predicts that the variance in parasite size should also increase with the size of their hosts. Though untested, in parasite taxa with differential sex-dependent pressures on body size, this relationship should also be divergent across sexes due to differential size-fecundity relationships. We compiled global data on sequentially hermaphroditic isopods (Isopoda: Cymothoidae) parasitic on fish from published literature. With a data set comprising of 204 marine cymothoid species and their hosts, we used Bayesian hierarchical models to primarily test (1) Harrison's rule and its scaling across three functionally distinct guilds (mouth, gill, external); (2) the increasing variance hypothesis and sex-specific patterns. Our results revealed a strong positive association between parasite and host body sizes, but with uniform scaling across guilds. Host size exerted divergent, sex-specific effects on the relative intraspecific variation in parasite size, where this association was positive in males and absent in females. Here, we show that Harrison's rule is independent of guild, suggesting body size evolution across all cymothoids is equally underpinned by the size of their hosts. The sex-specificity of the increasing variance hypothesis can be explained by female fecundity being tightly bound to body size, whereas the dependency of reproductive success on size is inherently more relaxed in males.

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.

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.

Evolutionary consequences of vector-borne transmission: how using vectors shapes host, vector and pathogen evolution.

Transmission mode is a key factor that influences host­parasite coevolution. Vector-borne pathogens are among the most important disease agents for humans and wildlife due to their broad distribution, high diversity, prevalence and lethality. They comprise some of the most important and widespread human pathogens, such as yellow fever, leishmania and malaria. Vector-borne parasites (in this review, those transmitted by blood-feeding Diptera) follow unique transmission routes towards their vertebrate hosts. Consequently, each part of this tri-partite (i.e. parasite, vector and host) interaction can influence co- and counter-evolutionary pressures among antagonists. This mode of transmission may favour the evolution of greater virulence to the vertebrate host; however, pathogen­vector interactions can also have a broad spectrum of fitness costs to the insect vector. To complete their life cycle, vector-borne pathogens must overcome immune responses from 2 unrelated organisms, since they can activate responses in both vertebrate and invertebrate hosts, possibly creating a trade-off between investments against both types of immunity. Here, we assess how dipteran vector-borne transmission shapes the evolution of hosts, vectors and the pathogens themselves. Hosts, vectors and pathogens co-evolve together in a constant antagonistic arms race with each participant's primary goal being to maximize its performance and fitness.

Short and sweet: an analysis of the length of parasite species names.

In its advice to taxonomists, the International Commission on Zoological Nomenclature (ICZN) recommends that scientific species names should be compact, memorable, and easy to pronounce. Here, using a dataset of over 3000 species of parasitic helminths described in the past two decades, we investigate trends in the length of Latin specific names (=epithets) chosen by taxonomists. Our results reveal no significant temporal change in the length of species epithets as a function of year of description, with annual averages fluctuating around the overall average length of just over 9 letters. We also found that lengths of species epithets did not differ among the various host taxa from which the parasites were recovered, however acanthocephalan species have been given longer species epithets than other helminth taxa. Finally, although species epithets were shorter than genus names for three-quarters of the species in our dataset, we detected no relationship between the length of species epithets and that of genus names across all species included, i.e., there was no evidence that shorter species epithets are chosen to compensate for long genus names. We conclude by encouraging parasite taxonomists to follow the recommendations of the ICZN and choose species epithets that are, as much as possible, compact and easy to remember, pronounce and spell.

Prevalence and richness of malaria and malaria-like parasites in wild birds from different biomes in South America.

South America has different biomes with a high richness of wild bird species and Diptera vectors, representing an ideal place to study the influence of habitat on vector-borne parasites. In order to better understand how different types of habitats do or do not influence the prevalence of haemosporidians, we performed a new analysis of two published datasets comprising wild birds from the Brazilian Savanna (Cerrado) as well as wild birds from the Venezuelan Arid Zone. We investigated the prevalence and genetic diversity of haemosporidian parasites belonging to two genera: Plasmodium and Haemoproteus. We evaluated data from 676 wild birds from the Cerrado and observed an overall prevalence of 49%, whereas, in the Venezuelan Arid Zone, we analyzed data from 527 birds and found a similar overall prevalence of 43%. We recovered 44 lineages, finding Plasmodium parasites more prevalent in the Cerrado (15 Plasmodium and 12 Haemoproteus lineages) and Haemoproteus in the Venezuelan Arid Zone (seven Plasmodium and 10 Haemoproteus lineages). No difference was observed on parasite richness between the two biomes. We observed seven out of 44 haemosporidian lineages that are shared between these two distinct South American biomes. This pattern of parasite composition and prevalence may be a consequence of multiple factors, such as host diversity and particular environmental conditions, especially precipitation that modulate the vector's dynamics. The relationship of blood parasites with the community of hosts in large and distinct ecosystems can provide more information about what factors are responsible for the variation in the prevalence and diversity of these parasites in an environment.

Migratory behaviour does not alter cophylogenetic congruence between avian hosts and their haemosporidian parasites.

Parasites display various degrees of host specificity, reflecting different coevolutionary histories with their hosts. Avian hosts follow multiple migration patterns representing short but also long distances. As parasites infecting migratory birds are subjected to multiple environmental and biotic changes through their flyways, migration may disrupt or strengthen cophylogenetic congruence between hosts and parasites. On the one hand, parasites might adapt to a single migratory host, evolving to cope with the specific challenges associated with the multiple habitats occupied by the host. On the other, as migrants can introduce parasites into new habitats, higher rates of host switching could also disrupt cophylogenetic patterns. We analysed whether migratory behaviour shapes avian haemosporidian parasite­host cophylogenetic congruence by testing if contributions of host­parasite links to overall congruence differ among resident and short-, variable- and long-distance migrants globally and within South America only. On both scales, we found significant overall cophylogenetic congruence by testing whether overall congruence differed between haemosporidian lineages and bird species. However, we found no difference in contribution towards congruence among links involving resident vs migratory hosts in both models. Thus, migratory behaviour neither weakens nor strengthens bird­haemosporidian cophylogenetic congruence, suggesting that other avian host traits are more influential in generating phylogenetic congruence in this host­parasite system.

The rise of big data in disease ecology.

Big data have become readily available to explore patterns in large-scale disease ecology. However, the rate at which these public databases are exploited remains unknown. We highlight trends in big data usage in disease ecology during the past decade and encourage researchers to integrate big data into their study framework.

Haemosporidian taxonomic composition, network centrality and partner fidelity between resident and migratory avian hosts.

Migration can modify interaction dynamics between parasites and their hosts with migrant hosts able to disperse parasites and impact local community transmission. Thus, studying the relationships among migratory hosts and their parasites is fundamental to elucidate how migration shapes host-parasite interactions. Avian haemosporidians are some of the most prevalent and diverse group of wildlife parasites and are also widely studied as models in ecological and evolutionary research. Here, we contrast partner fidelity, network centrality and parasite taxonomic composition among resident and non-resident avian hosts using presence/absence data on haemosporidians parasitic in South American birds as study model. We ran multilevel Bayesian models to assess the role of migration in determining partner fidelity (i.e., normalized degree) and centrality (i.e., weighted closeness) in host-parasite networks of avian hosts and their respective haemosporidian parasites. In addition, to evaluate parasite taxonomic composition, we performed permutational multivariate analyses of variance to quantify dissimilarity in haemosporidian lineages infecting different host migratory categories. We observed similar partner fidelity and parasite taxonomic composition among resident and migratory hosts. Conversely, we demonstrate that migratory hosts play a more central role in host-parasite networks than residents. However, when evaluating partially and fully migratory hosts separately, we observed that only partially migratory species presented higher network centrality when compared to resident birds. Therefore, migration does not lead to differences in both partner fidelity and parasite taxonomic composition. However, migratory behavior is positively associated with network centrality, indicating migratory hosts play more important roles in shaping host-parasite interactions and influence local transmission.

The people vs science: can passively crowdsourced internet data shed light on host-parasite interactions?

Every internet search query made out of curiosity by anyone who observed something in nature, as well as every photo uploaded to the internet, constitutes a data point of potential use to scientists. Researchers have now begun to exploit the vast online data accumulated through passive crowdsourcing for studies in ecology and epidemiology. Here, we demonstrate the usefulness of iParasitology, i.e. the use of internet data for tests of parasitological hypotheses, using hairworms (phylum Nematomorpha) as examples. These large worms are easily noticeable by people in general, and thus likely to generate interest on the internet. First, we show that internet search queries (collated with Google Trends) and photos uploaded to the internet (specifically, to the iNaturalist platform) point to parts of North America with many sightings of hairworms by the public, but few to no records in the scientific literature. Second, we demonstrate that internet searches predict seasonal peaks in hairworm abundance that accurately match scientific data. Finally, photos uploaded to the internet by non-scientists can provide reliable data on the host taxa that hairworms most frequently parasitize, and also identify hosts that appear to have been neglected by scientific studies. Our findings suggest that for any parasite group likely to be noticeable by non-scientists, information accumulating through internet search activity, photo uploads, social media or any other format available online, represents a valuable source of data that can complement traditional scientific data sources in parasitology.

Migratory birds have higher prevalence and richness of avian haemosporidian parasites than residents.

Individuals of migratory species may be more likely to become infected by parasites because they cross different regions along their route, thereby being exposed to a wider range of parasites during their annual cycle. Conversely, migration may have a protective effect since migratory behaviour allows hosts to escape environments presenting a high risk of infection. Haemosporidians are one of the best studied, most prevalent and diverse groups of avian parasites, however the impact of avian host migration on infection by these parasites remains controversial. We tested whether migratory behaviour influenced the prevalence and richness of avian haemosporidian parasites among South American birds. We used a dataset comprising ~ 11,000 bird blood samples representing 260 bird species from 63 localities and Bayesian multi-level models to test the impact of migratory behaviour on prevalence and lineage richness of two avian haemosporidian genera (Plasmodium and Haemoproteus). We found that fully migratory species present higher parasite prevalence and higher richness of haemosporidian lineages. However, we found no difference between migratory and non-migratory species when evaluating prevalence separately for Plasmodium and Haemoproteus, or for the richness of Plasmodium lineages. Nevertheless, our results indicate that migratory behaviour is associated with an infection cost, namely a higher prevalence and greater variety of haemosporidian parasites.

Animal migrations and parasitism: reciprocal effects within a unified framework.

Migrations, i.e. the recurring, roundtrip movement of animals between distant and distinct habitats, occur among diverse metazoan taxa. Although traditionally linked to avoidance of food shortages, predators or harsh abiotic conditions, there is increasing evidence that parasites may have played a role in the evolution of migration. On the one hand, selective pressures from parasites can favour migratory strategies that allow either avoidance of infections or recovery from them. On the other hand, infected animals incur physiological costs that may limit their migratory abilities, affecting their speed, the timing of their departure or arrival, and/or their condition upon reaching their destination. During migration, reduced immunocompetence as well as exposure to different external conditions and parasite infective stages can influence infection dynamics. Here, we first explore whether parasites represent extra costs for their hosts during migration. We then review how infection dynamics and infection risk are affected by host migration, thereby considering parasites as both causes and consequences of migration. We also evaluate the comparative evidence testing the hypothesis that migratory species harbour a richer parasite fauna than their closest free-living relatives, finding general support for the hypothesis. Then we consider the implications of host migratory behaviour for parasite ecology and evolution, which have received much less attention. Parasites of migratory hosts may achieve much greater spatial dispersal than those of non-migratory hosts, expanding their geographical range, and providing more opportunities for host-switching. Exploiting migratory hosts also exerts pressures on the parasite to adapt its phenology and life-cycle duration, including the timing of major developmental, reproduction and transmission events. Natural selection may even favour parasites that manipulate their host's migratory strategy in ways that can enhance parasite transmission. Finally, we propose a simple integrated framework based on eco-evolutionary feedbacks to consider the reciprocal selection pressures acting on migratory hosts and their parasites. Host migratory strategies and parasite traits evolve in tandem, each acting on the other along two-way causal paths and feedback loops. Their likely adjustments to predicted climate change will be understood best from this coevolutionary perspective.

iParasitology: Mining the Internet to Test Parasitological Hypotheses.

Digital data (internet queries, page views, social media posts, images) are accumulating online at increasing rates. Tools for compiling these data and extracting their metadata are now readily available. We highlight the possibilities and limitations of internet data to reveal patterns in host-parasite interactions and encourage parasitologists to embrace iParasitology.

Higher infection probability of haemosporidian parasites in Blue-black Grassquits (Volatinia jacarina) inhabiting native vegetation across Brazil.

Human induced changes on landscape can alter the biotic and abiotic factors that influence the transmission of vector-borne parasites. To examine how infection rates of vector-transmitted parasites respond to changes on natural landscapes, we captured 330 Blue-black Grassquits (Volatinia jacarina) in Brazilian biomes and assessed the prevalence and diversity of avian haemosporidian parasites (Plasmodium and Haemoproteus) across avian host populations inhabiting environment under different disturbance and climatic conditions. Overall prevalence in Blue-black Grassquits was low (11%) and infection rates exhibited considerable spatial variation, ranging from zero to 39%. Based on genetic divergence of cytochrome b gene, we found two lineages of Haemoproteus (Parahaemoproteus) and 10 of Plasmodium. We showed that Blue-black Grassquit populations inhabiting sites with higher proportion of native vegetation cover were more infected across Brazil. Other landscape metrics (number of water bodies and distance to urban areas) and climatic condition (temperature and precipitation) known to influence vector activity and promote avian malaria transmission did not explain infection probability in Blue-black Grassquit populations. Moreover, breeding season did not explain prevalence across avian host populations. Our findings suggest that avian haemosporidian prevalence and diversity in Blue-black Grassquit populations are determined by recent anthropogenic changes in vegetation cover that may alter microclimate, thus influencing vector activity and parasite transmission.

First record of haemosporidian parasites infecting swifts (Aves: Apodidae).

Avian malaria is a widespread infection caused by parasites from the Order Haemosporida. Indeed, Neotropical swifts are interesting models for host-parasite coevolution studies due to their unique life history that may allow them to escape parasitism. Considering this, we evaluated haemosporidians from Neotropical swifts. We collected blood and prepared smears from 277 individuals from waterfalls in Brazil. Despite low parasitemia or absence of parasites detected by microscopy haemosporidian infection was detected in 44 swifts (15.8%) using a screening PCR that amplifies a 154-nucleotide segment of ribosomal RNA coding sequence within the mitochondrial DNA (mtDNA) of Plasmodium and Haemoproteus. Although previous studies reported absence of these parasites in European and North American swifts our data suggest that Neotropical swifts are susceptible to haemosporidians. Further studies will add information about evolutionary and ecological aspects of avian haemosporidia in Neotropical Cypseloidinae swifts.