Corrigendum to Streicker et al. (2013) Differential sources of host species heterogeneity influence the transmission and control of multi‐host parasites

In a recent article, we described a conceptual and analytical model to identify the key host species for parasite transmission in multi‐host communities and used data from 11 gastro‐intestinal parasites infecting up to five small mammal host species as an illustrative example of how the framework could be applied. A limitation of these empirical data was uncertainty in the identification of parasite species using egg/oocyst morphology, which could overestimate parasite sharing between host species. Here, we show that the key results of the original analysis, namely that (1) parasites naturally infect multiple host species, but typically rely on a small subset of infected host species for long‐term maintenance, (2) that different mechanisms underlie how particular host species dominate transmission and (3) that these different mechanisms influence the predicted efficiency of disease control measures, are robust to analysis of a smaller subset of host–parasite combinations that we have greatest confidence in identifying. We further comment briefly on the need for accurate parasite identification, ideally using molecular techniques to quantify cross‐species transmission and differentiate covert host specificity from true host generalism.     

Infection dynamics of endemic malaria in a wild bird population: parasite species-dependent drivers of spatial and temporal variation in transmission rates

1.?Investigating the ecological context in which host-parasite interactions occur and the roles of biotic and abiotic factors in forcing infection dynamics is essential to understanding disease transmission, spread and maintenance. 2.?Despite their prominence as model host-pathogen systems, the relative influence of environmental heterogeneity and host characteristics in influencing the infection dynamics of avian blood parasites has rarely been assessed in the wild, particularly at a within-population scale. 3.?We used a novel multievent modelling framework (an extension of multistate mark-recapture modelling) that allows for uncertainty in disease state, to estimate transmission parameters and assess variation in the infection dynamics of avian malaria in a large, longitudinally sampled data set of breeding blue tits infected with two divergent species of Plasmodium parasites. 4.?We found striking temporal and spatial heterogeneity in the disease incidence rate and the likelihood of recovery within this single population and demonstrate marked differences in the relative influence of environmental and host factors in forcing the infection dynamics of the two Plasmodium species. 5.?Proximity to a permanent water source greatly influenced the transmission rates of P.?circumflexum, but not of P.?relictum, suggesting that these parasites are transmitted by different vectors. 6.?Host characteristics (age/sex) were found to influence infection rates but not recovery rates, and their influence on infection rates was also dependent on parasite species: P.?relictum infection rates varied with host age, whilst P.?circumflexum infection rates varied with host sex. 7.?Our analyses reveal that transmission of endemic avian malaria is a result of complex interactions between biotic and abiotic components that can operate on small spatial scales and demonstrate that knowledge of the drivers of spatial and temporal heterogeneity in disease transmission will be crucial for developing accurate epidemiological models and a thorough understanding of the evolutionary implications of pathogens.     

Sources and sinks: revisiting the criteria for identifying reservoirs for American cutaneous leishmaniasis

Molecular-based approaches might be misleading for assessing the 'potential importance' of possible reservoirs for parasites unless used in conjunction with population dynamics and ecological studies that provide an understanding of the linkages between the enzootic transmission cycle (in wild animals) and that in domestic animals. Better understanding of ecological constraints on Leishmania transmission is needed to assess fully the passage of the parasite between its sandfly vector and different mammalian host species. We use a straightforward mathematical framework to illustrate that misuse of association patterns, as guidance for implementation of control measures, can in fact increase the endemism of leishmaniasis.     

Ruminating on complexity: macroparasites of wildlife and livestock

Recent advances in ecology have improved our understanding of the role of parasites in the dynamics of wildlife populations. However, conditions that prevail in many wildlife systems, such as host movement, contact with livestock, and heterogeneity in the environment of the parasite outside of the host, have largely been ignored in existing models of macroparasite transmission. We need to refine these models if we are to stand a chance of developing effective parasite control strategies. New quantitative approaches enable us to address key complexities and make better use of scarce data, and these should enhance our efforts to understand and control emerging problems of interspecific parasite transmission.     

Interspecific associations among larval helminths in fish

Various processes can generate associations between the larvae of different helminth species in their fish intermediate or paratenic host. We investigated the pairwise associations among larval helminth species in eight different fish populations, using two different coefficients of associations, in order to determine in what situations they are strongest. All helminth species included use the fish studied as either their second intermediate host or their paratenic host, and are acquired by the fish when it ingests an infected first intermediate host. The intensity of infection correlated positively with fish length for most helminth species. Pairs of species which both exhibited positive correlations with fish length tended to be more strongly associated with one another, although this tendency was not pronounced. Similarity in life cycle had a more important influence on pairwise associations. Among the 62 pairwise associations that could be computed, pairs of helminth species that shared both first intermediate hosts and definitive hosts were the most strongly associated, followed by pairs that shared only one other host, and finally by pairs that did not share other hosts. The results suggest that assemblages of larval helminth parasites in fish are not random collections of locally available species, but rather structured packets of larval parasites that travel together along common transmission routes.     

The dynamics of parasite incidence across host species

Whilst it is well known that many parasites occasionally switch from one host species to another and thus spread within a host clade, the patterns of spread and the observed heterogeneity in parasite incidence between host taxa are not well understood. Here, we develop a simple stochastic model as a first attempt to understand these ‘incidence dynamics’. Based on the empirically supported assumption that the probability of successful transmission from an infected to a new host species declines with increasing genetic distance between them, we study the impact of different phylogenetic histories of the host clade on the pattern of spread and the average incidence of the parasites. Our results suggest that host phylogeny alone can lead to heterogeneous parasite incidence.     

Parasite and host assemblages: embracing the reality will improve our knowledge of parasite transmission and virulence

Interactions involving several parasite species (multi-parasitized hosts) or several host species (multi-host parasites) are the rule in nature. Only a few studies have investigated these realistic, but complex, situations from an evolutionary perspective. Consequently, their impact on the evolution of parasite virulence and transmission remains poorly understood. The mechanisms by which multiple infections may influence virulence and transmission include the dynamics of intrahost competition, mediation by the host immune system and an increase in parasite genetic recombination. Theoretical investigations have yet to be conducted to determine which of these mechanisms are likely to be key factors in the evolution of virulence and transmission. In contrast, the relationship between multi-host parasites and parasite virulence and transmission has seen some theoretical investigation. The key factors in these models are the trade-off between virulence across different host species, variation in host species quality and patterns of transmission. The empirical studies on multi-host parasites suggest that interspecies transmission plays a central role in the evolution of virulence, but as yet no complete picture of the phenomena involved is available. Ultimately, determining how complex host–parasite interactions impact the evolution of host–parasite relationships will require the development of cross-disciplinary studies linking the ecology of quantitative networks with the evolution of virulence.     

Parasite species richness in carnivores: effects of host body mass, latitude, geographical range and population density

Aim  Comparative studies have revealed strong links between ecological factors and the number of parasite species harboured by different hosts, but studies of different taxonomic host groups have produced inconsistent results. As a step towards understanding the general patterns of parasite species richness, we present results from a new comprehensive data base of over 7000 host–parasite combinations representing 146 species of carnivores (Mammalia: Carnivora) and 980 species of parasites.
Methods  We used both phylogenetic and non-phylogenetic comparative methods while controlling for unequal sampling effort within a multivariate framework to ascertain the main determinants of parasite species richness in carnivores.
Results  We found that body mass, population density, geographical range size and distance from the equator are correlated with overall parasite species richness in fissiped carnivores. When parasites are classified by transmission mode, body mass and home range area are the main determinants of the richness of parasites spread by close contact between hosts, and population density, geographical range size and distance from the equator account for the diversity of parasites that are not dependent on close contact. For generalist parasites, population density, geographical range size and latitude are the primary predictors of parasite species richness. We found no significant ecological correlates for the richness of specialist or vector-borne parasites.
Main conclusions  Although we found that parasite species richness increases instead of decreases with distance from the equator, other comparative patterns in carnivores support previous findings in primates, suggesting that similar ecological factors operate in both these independent evolutionary lineages.     

Come with me if you want to live: sympatric parasites follow different transmission routes through aquatic host communities

Community composition, including the relative density of each host species, plays a vital role in the transmission of parasites or disease in freshwater ecosystems. Whereas some host species can effectively transmit parasites, others can act as dead ends (non-viable transmission routes), accumulating large numbers of parasites throughout their life, thus becoming important sinks for parasite populations. Although population sinks have been identified in certain host-parasite systems, robust field estimates of the proportions of parasites that are lost to these hosts are lacking. Here, we quantified the distribution of encysted larval hairworms (phylum Nematomorpha), common parasites in lotic ecosystems, in two subalpine stream communities of New Zealand. With parasite and host population densities calculated per m², we identified which host species most likely contributed to the transmission of three sympatric hairworm morphotypes identified in both streams, and which species acted as population sinks. We also tested for seasonal patterns and peaks in the abundance of each morphotype in the two communities over the sampling season. Finally, we tested whether hosts emerging from the streams had comparable abundances of hairworm morphotypes throughout the sampling period. For each morphotype, different key sets of host species harboured more hairworms on average (abundance) than others, depending on the stream. For one morphotype in particular, two species of hosts were found to be important population sinks that inhibited over a third of these parasites from completing their life cycle. We also observed a clear peak in abundance for another hairworm morphotype during summer. Our data suggest that hosts emerging from the streams matched their aquatic counterparts with respect to hairworm abundance, indicating no infection-dependent reduction in emergence success. Our findings suggest that, depending on relative community composition, sympatric parasites follow different host transmission pathways, some of which lead to dead ends that potentially impact overall infection dynamics. In turn, this information can help us understand the spread or emergence of disease in both freshwater and terrestrial environments, since hairworms infect terrestrial arthropods to complete their life cycle.     

Fitness effects of endemic malaria infections in a wild bird population: the importance of ecological structure

1.?Parasites can have important effects on host populations influencing either fecundity or mortality, but understanding the magnitude of these effects in endemic host-parasite systems is challenging and requires an understanding of ecological processes affecting both host and parasite. 2.?Avian blood parasites (Haemoproteus and Plasmodium) have been much studied, but the effects of these parasites on hosts in areas where they are endemic remains poorly known. 3.?We used a multistate modelling framework to explore the effects of chronic infection with Plasmodium on survival and recapture probability in a large data set of breeding blue tits, involving 3424 individuals and 3118 infection diagnoses over nine years. 4.?We reveal strong associations between chronic malaria infection and both recapture and survival, effects that are dependent on the clade of parasite, on host traits and on the local risk of infection. 5.?Infection with Plasmodium relictum was associated with reduced recapture probability and increased survival, compared to P.?circumflexum, suggesting that these parasites have differing virulence and cause different types of selection on this host. 6.?Our results suggest a large potential survival cost of acute infections revealed by modelling host survival as a function of the local risk of infection. 7.?Our analyses suggest not only that endemic avian malaria may have multiple fitness effects on their hosts and that these effects are species dependent, but also that adding ecological structure (in this case parasite species and spatial variation in disease occurrence) to analyses of host-parasite interactions is an important step in understanding the ecology and evolution of these systems.     

Quantifying Transmission Investment in Malaria Parasites

Many microparasites infect new hosts with specialized life stages, requiring a subset of the parasite population to forgo proliferation and develop into transmission forms. Transmission stage production influences infectivity, host exploitation, and the impact of medical interventions like drug treatment. Predicting how parasites will respond to public health efforts on both epidemiological and evolutionary timescales requires understanding transmission strategies. These strategies can rarely be observed directly and must typically be inferred from infection dynamics. Using malaria as a case study, we test previously described methods for inferring transmission stage investment against simulated data generated with a model of within-host infection dynamics, where the true transmission investment is known. We show that existing methods are inadequate and potentially very misleading. The key difficulty lies in separating transmission stages produced by different generations of parasites. We develop a new approach that performs much better on simulated data. Applying this approach to real data from mice infected with a single Plasmodium chabaudi strain, we estimate that transmission investment varies from zero to 20%, with evidence for variable investment over time in some hosts, but not others. These patterns suggest that, even in experimental infections where host genetics and other environmental factors are controlled, parasites may exhibit remarkably different patterns of transmission investment.     

Vector-borne parasites decrease host mobility: a field test of freeze or flee behaviour of willow ptarmigan

Transmission mode has been suggested to be a strong predictor of virulence. According to theory, the transmission of vector-borne parasites should be less dependent on host mobility than directly transmitted parasites. This could select for increased exploitation of host resources in parasites transmitted by vectors, which may be manifested as higher virulence. Here, we test the prediction that there is an association between transmission mode and the effect on host mobility by comparing parasite infection levels and mobility in willow ptarmigan (Lagopus lagopus L.). We examined the endoparasite infracommunities of individual hosts to obtain annual, quantitative data on four vector-transmitted species (Leucocytozoon lovati, Trypanosoma avium, Haemoproteus mansoni and microfilaria), two directly transmitted species (Trichostrongylus tenuis and Eimeria sp.) and two species with indirect life cycles (Hymenolepis microps and Parionella urogalli). We then used observed variations in freeze-or-flee responses of individual willow ptarmigan to assess whether parasite intensities were related to scored freezing responses. From a field data set covering a period of 9 years from a single area, we found that stronger freezing responses were associated with higher intensities of vector-borne parasites, especially with higher intensities of the haemosporidian L. lovati. Freezing responses were not associated with parasites transmitted in other ways. Thus, high intensities of vector-borne parasites tended to reduce host movements, while parasites with other transmission modes did not.     

Simultaneously reconstructing viral cross-species transmission history and identifying the underlying constraints

The factors that determine the origin and fate of cross-species transmission events remain unclear for the majority of human pathogens, despite being central for the development of predictive models and assessing the efficacy of prevention strategies. Here, we describe a flexible Bayesian statistical framework to reconstruct virus transmission between different host species based on viral gene sequences, while simultaneously testing and estimating the contribution of several potential predictors of cross-species transmission. Specifically, we use a generalized linear model extension of phylogenetic diffusion to perform Bayesian model averaging over candidate predictors. By further extending this model with branch partitioning, we allow for distinct host transition processes on external and internal branches, thus discriminating between recent cross-species transmissions, many of which are likely to result in dead-end infections, and host shifts that reflect successful onwards transmission in the new host species. Our approach corroborates genetic distance between hosts as a key determinant of both host shifts and cross-species transmissions of rabies virus in North American bats. Furthermore, our results indicate that geographical range overlap is a modest predictor for cross-species transmission, but not for host shifts. Although our evolutionary framework focused on the multi-host reservoir dynamics of bat rabies virus, it is applicable to other pathogens and to other discrete state transition processes.     

Host population density and body mass as determinants of species richness in parasite communities: comparative analyses of directly transmitted nematodes of mammals

Epidemiological theory predicts positive correlations between host population density or body mass and species richness among parasite communities. Here I test these predictions by a comparative study of communities of directly transmitted mammalian parasites, gastrointestinal strongylid nematodes. I use data from 45 species of mammals, representing examination of 17 200 individual hosts. The variable studied was the average number of gastrointestinal strongylid nematode species per host population, and three different methods were used to obtain estimates of parasite species richness that are unbiased by number of host individuals examined. Analyses were done using the phylogenetically independent contrast method. Host population density and parasite species richness were strongly positively correlated when the effects of host body weight had been controlled for. Controlling for other variables did not change this, and the relationship was found regardless of method used to correct for uneven sampling effort among host species. A positive relationship between parasite species richness and host body weight was also found, but the effect of host densities had to be controlled for to see this. These relationships between host traits and species richness of directly transmitted parasites are stronger than patterns found using data on indirectly transmitted mammalian parasites, and suggests that links between host traits and parasite species richness are stronger than previously suggested. The results are consistent with parasite species richness being positively linked to pathogen transmission rates and reductions in transmission rates possibly increasing extinction probabilities in parasite populations. The results also suggest that parasites may exert a cost of increases in rate of population energy usage, and thus show that pathogens may be important in generating independence between body mass and rate of population energy usage among host species.     

Parasite establishment in host communities

Many pathogens and parasites attack multiple host species, so their ability to invade a host community can depend on host community composition. We present a graphical isocline framework for studying disease establishment in systems with two host species, based on treating host species as resources. The isocline approach provides a natural generalization to multi‐host systems of two related concepts in disease ecology – the basic reproductive rate of a parasite, and threshold host density. Qualitative isocline shape characterizes the threshold community configurations that permit parasite establishment. In general, isocline shape reflects the relative forces of inter‐ and intraspecific transmission of shared parasites. We discuss the qualitative implications of parasite isocline shape for issues of mounting concern in conservation ecology.     

Determinants of distribution and prevalence of avian malaria in blue tit populations across Europe: separating host and parasite effects

Although avian malarial parasites are globally distributed, the factors that affect the geographical distribution and local prevalence of different parasite lineages across host populations or species are still poorly understood. Based on the intense screening of avian malarial parasites in nine European blue tit populations, we studied whether distribution ranges as well as local adaptation, host specialization and phylogenetic relationships can determine the observed prevalences within populations. We found that prevalence differed consistently between parasite lineages and host populations, indicating that the transmission success of parasites is lineage specific but is partly shaped by locality-specific effects. We also found that the lineage-specific estimate of prevalence was related to the distribution range of parasites: lineages found in more host populations were generally more prevalent within these populations. Additionally, parasites with high prevalence that were also widely distributed among blue tit populations were also found to infect more host species. These findings suggest that parasites reaching high local prevalence can also realize wide distribution at a global scale that can have further consequences for host specialization. Although phylogenetic relationships among parasites did not predict prevalence, we detected a close match between a tree based on the geographic distance of the host populations and the parasite phylogenetic tree, implying that neighbouring host populations shared a related parasite fauna.     

Within-host population dynamics and the evolution of microparasites in a heterogeneous host population

Abstract Why do parasites harm their hosts? The general understanding is that if the transmission rate and virulence of a parasite are linked, then the parasite must harm its host to maximize its transmission. The exact nature of such trade‐offs remains largely unclear, but for vertebrate hosts it probably involves interactions between a microparasite and the host immune system. Previous results have suggested that in a homogeneous host population in the absence of super‐ or coinfection, within‐host dynamics lead to selection of the parasite with an intermediate growth rate that is just being controlled by the immune system before it kills the host (Antia et al. 1994). In this paper, we examine how this result changes when heterogeneity is introduced to the host population. We incorporate the simplest form of heterogeneity–random heterogeneity in the parameters describing the size of the initial parasite inoculum, the immune response of the host, and the lethal density at which the parasite kills the host. We find that the general conclusion of the previous model holds: parasites evolve some intermediate growth rate. However, in contrast with the generally accepted view, we find that virulence (measured by the case mortality or the rate of parasite‐induced host mortality) increases with heterogeneity. Finally, we link the within‐host and between‐host dynamics of parasites. We show how the parameters for epidemiological spread of the disease can be estimated from the within‐host dynamics, and in doing so examine the way in which trade‐offs between these epidemiological parameters arise as a consequence of the interaction of the parasite and the immune response of the host.     

Patterns of host specificity and transmission among parasites of wild primates

Multihost parasites have been implicated in the emergence of new diseases in humans and wildlife, yet little is known about factors that influence the host range of parasites in natural populations. We used a comprehensive data set of 415 micro- and macroparasites reported from 119 wild primate hosts to investigate broad patterns of host specificity. The majority (68%) of primate parasites were reported to infect multiple host species, including animals from multiple families or orders. This pattern corresponds to previous studies of parasites found in humans and domesticated animals. Within three parasite groups (viruses, protozoans and helminths), we examined parasite taxonomy and transmission strategy in relation to measures of host specificity. Relative to other parasite groups, helminths were associated with the greatest levels of host specificity, whereas most viruses were reported to infect hosts from multiple families or orders. Highly significant associations between the degree of host specificity and transmission strategy arose within each parasite group, but not always in the same direction, suggesting that unique constraints influence the host range of parasites within each taxonomic group. Finally characteristics of over 100 parasite species shared between wild primates and humans, including those recognised as emerging in humans, revealed that most of these shared parasites were reported from multiple host orders. Furthermore, nearly all viruses that were reported to infect both humans and non-human primates were classified as emerging in humans.