The role of phylogeny and ecology in experimental host specificity: insights from a eugregarine-host system

The degree to which parasites use hosts is fundamental to host-parasite coevolution studies, yet difficult to assess and interpret in an evolutionary manner. Previous assessments of parasitism in eugregarine-host systems suggest high degrees of host specificity to particular host stages and host species; however, rarely have the evolutionary constraints on host specificity been studied experimentally. A series of experimental infections were conducted to determine the extent of host stadium specificity (larval vs. adult stage) and host specificity among 6 tenebrionid host species and 5 eugregarine parasite species. Eugregarines from all host species infected both the larva and adult stages of the host, and each parasite taxa colonized several host species (Tribolium spp. and Palorus subdepressus). Parasite infection patterns were not congruent with host phylogeny, suggesting that host phylogeny is not a significant predictor of host-parasite interactions in this system. However, the 2 host stages produced significantly different numbers of parasite propagules, indicating that ecological factors may be important determinants of host specificity in this host-parasite system. While field infections reflect extant natural infection patterns of parasites, experimental infections can demonstrate potential host-parasite interactions, which aids in identifying factors that may be significant in shaping future host-parasite interactions.     

Coevolution in host-parasite systems: behavioural strategies of slave-making ants and their hosts

Recently, avian brood parasites and their hosts have emerged as model systems for the study of host-parasite coevolution. However, empirical studies of the highly analogous social parasites, which use the workers of another eusocial species to raise their own young, have never explicitly examined the dynamics of these systems from a coevolutionary perspective. Here, we demonstrate interpopulational variation in behavioural interactions between a socially parasitic slave-maker ant and its host that is consistent with the expectations of host-parasite coevolution. Parasite pressure, as inferred by the size, abundance and raiding frequency of Protomognathus americanus colonies, was highest in a New York population of the host Leptothorax longispinosus and lowest in a West Virginia population. As host-parasite coevolutionary theory would predict, we found that the slave-makers and the hosts from New York were more effective at raiding and defending against raiders, respectively, than were conspecifics from the West Virginia population. Some of these variations in efficacy were brought about by apparently simple shifts in behaviour. These results demonstrate that defence mechanisms against social parasites can evolve, and they give the first indications of the existence of a coevolutionary arms race between a social parasite and its host.     

Geographic and within-population structure in variable resistance to parasite species and strains in a vertebrate host

Host resistance to parasites and parasite infectivity may be subject to significant genetically determined variation within species. However, relatively little is known of how this variability is structured in natural vertebrate populations and their macroparasites. A laboratory experiment on host susceptibility-parasite infectivity variation in a wildlife host-parasite system (subspecies of the anuran X. laevis and their polystome flatworms), including 33 pairwise allopatric and sympatric host-parasite combinations (three parasite geographical isolates x 11 host full-sibling families, n=600), revealed a complex pattern of infection success. Results amongst host sibships from different localities suggested that infection success was subject to a highly significant locality x parasite isolate interaction. Within localities, a highly significant sibship x isolate interaction also occurred in one of two groups of sibships examined. The existence of such interactions suggests a potential for frequency-dependent, Red Queen-like selection. Interaction between locality and isolate was partly due to higher infection levels in sympatric combinations, consistent with a general pattern of host-specific adaptation. However, some allopatric combinations produced unpredictably high infection levels, resulting in very asymmetrical cross-infectivity patterns (where the reciprocal cross-infections produced negligible infection). This phylogeographically structured host-parasite system may, therefore, sometimes generate local parasite strains with high infectivity to allopatric hosts. Secondary contact between populations could thus result in significant, and unequal, transfer of parasites.     

Drivers of parasite community structure in fishes of the continental shelf of the Western Mediterranean: the importance of host phylogeny and autecological traits

We explored the relationships between features of host species and their environment, and the diversity, composition and structure of parasite faunas and communities using a large taxonomically consistent dataset of host-parasite associations and host-prey associations, and original environmental and host trait data (diet, trophic level, population density and habitat depth vagility) for the most abundant demersal fish species off the Catalonian coast of the Western Mediterranean. Altogether 98 species/taxa belonging to seven major parasite groups were recovered in 683 fish belonging to 10 species from seven families and four orders. Our analyses revealed that (i) the parasite fauna of the region is rich and dominated by digeneans; (ii) the host parasite faunas and communities exhibited wide variations in richness, abundance and similarity due to a strong phylogenetic component; (iii) the levels of host sharing were low and involved host generalists and larval parasites; (iv) the multivariate similarity pattern of prey samples showed significant associations with hosts and host trophic guilds; (v) prey compositional similarity was not associated with the similarity of trophically transmitted parasite assemblages; and (vi) phylogeny and fish autecological traits were the best predictors of parasite community metrics in the host-parasite system studied.     

Forest fragmentation, the decline of an endangered primate, and changes in host-parasite interactions relative to an unfragmented forest

Forest fragmentation may alter host-parasite interactions in ways that contribute to host population declines. We tested this prediction by examining parasite infections and the abundance of infective helminths in 20 forest fragments and in unfragmented forest in Kibale National Park, Uganda. Over 4 years, the endangered red colobus (Procolobus rufomitratus) declined by 20% in fragments, whereas the black-and-white colobus (Colobus guereza) in fragments and populations of both colobines in unfragmented forest remained relatively stable. Seven nematodes (Strongyloides fulleborni, Strongyloides stercoralis, Oesophagostomum sp., an unidentified strongyle, Trichuris sp., Ascaris sp., and Colobenterobius sp.), one cestode (Bertiella sp.), and three protozoans (Entamoeba coli, Entamoeba histolytica/dispar, and Giardia sp.) were detected. Infection prevalence and the magnitude of multiple infections were greater for red colobus in fragmented than in unfragmented forest, but these parameters did not differ between forests for black-and-white colobus. Infective-stage colobus parasites occurred at higher densities in fragmented compared with unfragmented forest, demonstrating greater infection risk for fragmented populations. There was little evidence that the nature of the infection was related to the size of the fragment, the density of the host, or the nature of the infection in the other colobine, despite the fact that many of the parasites are considered generalists. This study suggests that forest fragmentation can alter host-parasite dynamics and demonstrates that such changes can correspond with changes in host population size in forest fragments.     

The host specificity of Gyrodactylus salaris Malmberg (Platyhelminthes, Monogenea): susceptibility of Oncovhynchus mykiss (Walbaum) under experimental conditions

An experimental epidemiological approach was chosen to study the survival and infection dynamics of Gyrodactylus salaris on juvenile rainbow trout, Oncorhynchus mykiss , in the laboratory. A marked heterogeneity in the host stock was apparent. The rainbow trout could be divided into three groups on the basis of parasite survival and infection pattern on individually isolated fish: (1) hosts receptive to initial parasite attachment, but unreceptive to parasite establishment and reproduction; (2) hosts moderately susceptible to parasite establishment and reproduction, but which, after a period of restricted parasite population growth, responded, recovered and eliminated the parasites; and (3) hosts very susceptible to parasite infection and reproduction, but which, after a period of significant parasite population growth, responded, recovered and eliminated the parasites. These different patterns are considered to reflect genetic differences between host individuals. Parasite aggregation was also shown to be an important factor in the outcome of the host-parasite association. The parasites were finally eliminated on the individually isolated hosts, but not on hosts maintained in batches and so host population size and immigration of fresh. previously unexposed, hosts appeared to be important for growth and maintenance of the parasite population. The parasite was not found to cause host mortality. Rainbow trout was a suitable host for G. salaris , capable of transmitting the parasite to new localities as a consequence of stocking programmes or migratory behaviour.     

Effect of sexual segregation on host-parasite interaction: Model simulation for abomasal parasite dynamics in alpine ibex (Capraibex)

We investigated whether sexual segregation might affect parasite transmission and host dynamics, hypothesising that if males are the more heavily infected sex and more responsible for the transmission of parasite infections, female avoidance of males and the space they occupy could reduce infection rates. A mathematical model, simulating the interaction between abomasal parasites and a hypothetical alpine ibex (Capraibex) host population composed of its two sexes, was developed to predict the effect of different degrees of sexual segregation on parasite intensity and on host abundance. The results showed that when females tended to be segregated from males, and males were distributed randomly across space, the impact of parasites was the lowest, resulting in the highest host abundance, with each sex having the lowest parasite intensity. The predicted condition that minimises the impact of parasites in our model was the one closest to that observed in nature where females actively seek out the more segregated sites while males are less selective in their ranging behaviour. The overlapping of field observation with the predicted optimal strategy lends support to our idea that there might be a connection between parasite transmission and sexual segregation. Our simulations provide the biological boundaries of host-parasite interaction needed to determine a parasite-mediated effect on sexual segregation and a formalised null hypothesis against which to test future field experiments.     

Comparative proteomic analysis of Fasciola hepatica juveniles and Schistosoma bovis schistosomula

Protein interactions between host and parasites can influence the infection success and severity. The aim of this investigation was to identify the proteins from two trematodes potentially localized at the host-parasite interface. We performed the proteomic profiles from in vivo obtained immature lung stage Schistosoma bovis schistosomula and in vitro excysted juveniles from Fasciola hepatica, parasites of ruminants and man usually giving rise to chronic infections. Proteomes from those parasites were obtained after digestion with trypsin and the peptides generated were identified by mass spectrometry, both before and after parasites' treatment with 70% methanol. The comparison of the two proteome sets from each parasite and between them, the analysis of their relative abundance and of their potential exposure to the host from living parasites, together with the specific immunolocalization of two of the identified molecules, show that this approach could assist in the identification of parasite exposed proteins and in the definition of molecules common for the two parasites with potential interaction with the host. Further characterization of these molecules could guide to define new common anti-parasitic targets and potential vaccine candidates.     

Chance or choice? Understanding parasite selection and infection in multi-host communities

Ongoing debate over the relationship between biodiversity and disease risk underscores the need to develop a more mechanistic understanding of how changes in host community composition influence parasite transmission, particularly in complex communities with multiple hosts. A key challenge involves determining how motile parasites select among potential hosts and the degree to which this process shifts with community composition. Focusing on interactions between larval amphibians and the pathogenic trematode Ribeiroia ondatrae, we designed a novel, large-volume set of choice chambers to assess how the selectivity of free-swimming infectious parasites varied among five host species and in response to changes in assemblage composition (four different permutations). In a second set of trials, cercariae were allowed to contact and infect hosts, allowing comparison of host-parasite encounter rates (parasite choice) with infection outcomes (successful infections). Cercariae exhibited consistent preferences for specific host species that were independent of the community context; large-bodied amphibians, such as larval bullfrogs (Rana catesbeiana), exhibited the highest level of parasite attraction. However, because host attractiveness was decoupled from susceptibility to infection, assemblage composition sharply affected both per-host infection as well as total infection (summed among co-occurring hosts). Species such as the non-native R. catesbeiana functioned as epidemiological ‘sinks’ or dilution hosts, attracting a disproportionate fraction of parasites relative to the number that established successfully, whereas Taricha granulosa and especially Pseudacris regilla supported comparatively more metacercariae relative to cercariae selection. These findings provide a framework for integrating information on parasite preference in combination with more traditional factors such as host competence and density to forecast how changes within complex communities will affect parasite transmission.     

Population biology of Schistosoma mansoni in the black rat: host regulation and basic transmission rate.

A simple mathematical model was built to investigate the population biology of Schistosoma mansoni in its natural definitive host, the black rat (Rattus rattus). Prevalence and parasite abundance over 13 years from field studies and data from laboratory experiments were used to set up the model. Sensitivity analysis showed that the abundance of parasites is strongly influenced by variation in the values of infection parameters. The model shows that the parasite is able to control populations of definitive hosts. We discuss the factors that may explain the long-term persistence of S. mansoni among its natural definitive host, R. rattus and its intermediate host, the snail Biomphalaria glabrata in Guadeloupe (French West Indies). The impact of the parasite does not appear to explain the apparent persistence of the host-parasite association over a 13 year period. Our results seem to support the influence of environmental factors, which may act on the infection process by reducing, or increasing, the rate of encounters between hosts and free-living stages of the parasite.     

Parasite-driven extinction in spatially explicit host-parasite systems

General host-parasite theory suggests that parasites may be implicated in the extinction of their hosts by causing instability that leads to increased risk of stochastic extinction. In contrast, spatially explicit models suggest that the parasite may directly drive the host population to extinction. Here we examine the ecological characteristics of host-parasite interactions that favor parasite-driven host extinction. Pair approximations and simulations show that parasites only drive their hosts to extinction when they significantly reduce host reproduction. As a matter of interest, parasites that have a relatively small effect on host death rate are more likely to cause host extinction. Parasite-driven host extinction occurs at any population size, whereas extinction caused by stochastic effects is less likely to occur in large host populations. Populations may therefore be under threat from parasites that stop host reproduction, and this type of parasite may prove to be the most effective biological pesticide.     

THE EFFECTS OF HOST GENOTYPE AND SPATIAL DISTRIBUTION ON TREMATODE PARASITISM IN A BIVALVE POPULATION

A basic assumption underlying models of host-parasite coevolution is the existence of additive genetic variation among hosts for resistance to parasites. However, estimates of additive genetic variation are lacking for natural populations of invertebrates. Testing this assumption is especially important in view of current models that suggest parasites may be responsible for the evolution of sex, such as the Red Queen hypothesis. This hypothesis suggests that the twofold reproductive disadvantage of sex relative to parthenogenesis can be overcome by the more rapid production of rare genotypes resistant to parasites. Here I present evidence of significant levels of additive genetic variance in parasite resistance for an invertebrate host-parasite system in nature. Using families of the bivalve mollusc, Transennella tantilla, cultured in the laboratory, then exposed to parasites in the field, I quantified heritable variation in parasite resistance under natural conditions. The spatial distribution of outplanted hosts was also varied to determine environmental contributions to levels of parasite infection and to estimate potential interactions of host genotype with environment. The results show moderate but significant levels of heritability for resistance to parasites (h² = 0.36). The spatial distribution of hosts also significantly influenced parasite prevalence such that increased host aggregation resulted in decreased levels of parasite infection. Family mean correlations across environments were positive, indicating no genotype-environment interaction. Therefore, these results provide support for important assumptions underlying coevolutionary models of host-parasite systems.     

Ecological and genetic determinants of multiple infection and aggregation in a microbial host-parasite system

The number of parasites colonizing a host (termed 'multiple infection') is an important determinant of host-parasite interactions. In theory, multiple infection is determined by random mass action in genetically and spatially homogeneous populations of host and parasite. In real populations, deviations from these assumptions may strongly influence levels of multiple infection. We carried out inoculation experiments in microcosms of the freshwater protozoan Paramecium caudatum and its bacterial parasite Holospora undulata. Increasing parasite dose produced higher levels of (multiple) infection; more susceptible host genotypes also were more multiply infected. An overall pattern of parasite aggregation (excess of uninfected individuals and of individuals carrying larger numbers of parasites) indicated deviations from random mass-action transmission. Homogenizing spatial distributions of parasite and host in our microcosms did not affect aggregation, whereas aggregation was more pronounced in old than in new host clones. Thus, variation in susceptibility may arise over time within clonal populations. When sequentially inoculated, already established infections increased the probability of additional infection in generally resistant host clones, but decreased it in more susceptible clones. Hence, the role of multiple infection as a driver of epidemiological or evolutionary processes may vary among populations, depending on their precise genetic composition or infection history.     

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.     

Consistent pattern of local adaptation during an experimental heat wave in a pipefish-trematode host-parasite system

Extreme climate events such as heat waves are expected to increase in frequency under global change. As one indirect effect, they can alter magnitude and direction of species interactions, for example those between hosts and parasites. We simulated a summer heat wave to investigate how a changing environment affects the interaction between the broad-nosed pipefish (Syngnathus typhle) as a host and its digenean trematode parasite (Cryptocotyle lingua). In a fully reciprocal laboratory infection experiment, pipefish from three different coastal locations were exposed to sympatric and allopatric trematode cercariae. In order to examine whether an extreme climatic event disrupts patterns of locally adapted host-parasite combinations we measured the parasite's transmission success as well as the host's adaptive and innate immune defence under control and heat wave conditions. Independent of temperature, sympatric cercariae were always more successful than allopatric ones, indicating that parasites are locally adapted to their hosts. Hosts suffered from heat stress as suggested by fewer cells of the adaptive immune system (lymphocytes) compared to the same groups that were kept at 18°C. However, the proportion of the innate immune cells (monocytes) was higher in the 18°C water. Contrary to our expectations, no interaction between host immune defence, parasite infectivity and temperature stress were found, nor did the pattern of local adaptation change due to increased water temperature. Thus, in this host-parasite interaction, the sympatric parasite keeps ahead of the coevolutionary dynamics across sites, even under increasing temperatures as expected under marine global warming.     

Migratory behavior of birds affects their coevolutionary relationship with blood parasites

Host traits, such as migratory behavior, could facilitate the dispersal of disease-causing parasites, potentially leading to the transfer of infections both across geographic areas and between host species. There is, however, little quantitative information on whether variation in such host attributes does indeed affect the evolutionary outcome of host-parasite associations. Here, we employ Leucocytozoon blood parasites of birds, a group of parasites closely related to avian malaria, to study host-parasite coevolution in relation to host behavior using a phylogenetic comparative approach. We reconstruct the molecular phylogenies of both the hosts and parasites and use cophylogenetic tools to assess whether each host-parasite association contributes significantly to the overall congruence between the two phylogenies. We find evidence for a significant fit between host and parasite phylogenies in this system, but show that this is due only to associations between nonmigrant parasites and their hosts. We also show that migrant bird species harbor a greater genetic diversity of parasites compared with nonmigrant species. Taken together, these results suggest that the migratory habits of birds could influence their coevolutionary relationship with their parasites, and that consideration of host traits is important in predicting the outcome of coevolutionary interactions.     

Host sexual dimorphism and parasite adaptation

In species with separate sexes, parasite prevalence and disease expression is often different between males and females. This effect has mainly been attributed to sex differences in host traits, such as immune response. Here, we make the case for how properties of the parasites themselves can also matter. Specifically, we suggest that differences between host sexes in many different traits, such as morphology and hormone levels, can impose selection on parasites. This selection can eventually lead to parasite adaptations specific to the host sex more commonly encountered, or to differential expression of parasite traits depending on which host sex they find themselves in. Parasites adapted to the sex of the host in this way can contribute to differences between males and females in disease prevalence and expression. Considering those possibilities can help shed light on host-parasite interactions, and impact epidemiological and medical science.     

Climatic effects and phenological mismatch in cuckoo–host interactions: a role for host phenotypic plasticity in laying date?

Climatic effects on breeding phenology vary across organisms and therefore might promote a phenological mismatch in ecologically interacting species, including those engaged in coevolutionary interactions such as brood parasites and their hosts. Recent studies suggest that climatic induced changes in migration phenology may have mismatched cuckoos and their hosts in Europe. However, it is currently unknown whether cuckoo–host phenological mismatch results from different degrees of phenotypic plasticity or to different speeds of microevolutionary processes affecting hosts and parasites. Here we performed 1) cross‐sectional correlations between climate conditions and population level of phenological mismatch between the migratory brood parasite great spotted cuckoo Clamator glandarius and its main resident host in Europe, the magpie Pica pica; and 2) a longitudinal analysis to study within‐individual variation in breeding phenology for individual hosts experiencing different climate conditions over a period of nine years (2005–2013). Cross‐sectional analyses revealed independent and contrary effects of winter and spring temperature on magpie phenology: magpie hosts tend to breed earlier those years with lower February temperatures, however, high temperature in the first half of April spur individuals to lay eggs. Breeding phenology of cuckoos was tuned to that of their magpie host in time and duration. However, annual phenological mismatch between cuckoos and magpie hosts increased with NAO index and January temperature. Longitudinal analyses revealed high individual consistency in magpie host phenology, but a low influence of climate, suggesting that the climatic‐driven phenological mismatch between cuckoos and magpies at the population‐level cannot be explained by a host plastic response to climatic conditions.     

New technologies to study helminth development and host-parasite interactions

How parasites develop and survive, and how they stimulate or modulate host immune responses are important in understanding disease pathology and for the design of new control strategies. Microarray analysis and bulk RNA sequencing have provided a wealth of data on gene expression as parasites develop through different life-cycle stages and on host cell responses to infection. These techniques have enabled gene expression in the whole organism or host tissue to be detailed, but do not take account of the heterogeneity between cells of different types or developmental stages, nor the spatial organisation of these cells. Single-cell RNA-seq (scRNA-seq) adds a new dimension to studying parasite biology and host immunity by enabling gene profiling at the individual cell level. Here we review the application of scRNA-seq to establish gene expression cell atlases for multicellular helminths and to explore the expansion and molecular profile of individual host cell types involved in parasite immunity and tissue repair. Studying host-parasite interactions in vivo is challenging and we conclude this review by briefly discussing the applications of organoids (stem-cell derived mini-tissues) to examine host-parasite interactions at the local level, and as a potential system to study parasite development in vitro. Organoid technology and its applications have developed rapidly, and the elegant studies performed to date support the use of organoids as an alternative in vitro system for research on helminth parasites.     

Island and taxon effects in parasitism revisited: avian malaria in the Lesser Antilles

We identify and describe the distribution of 12 genetically distinct malaria parasite lineages over islands and hosts in four common passerine birds in the Lesser Antilles. Combined parasite prevalence demonstrates strong host effects, little or no island effect, and a significant host-times-island interaction, indicating independent outcomes of host-parasite infections among island populations of the same host species. Host- and/or island-specific parasite lineages do not explain these host-parasite associations; rather, individual lineages themselves demonstrate the same type of independent interactions. Unlike overall prevalence, individual parasite lineages show considerable geographic structure (i.e., island effects) as well as species effects indicating that parasite lineages are constrained in their ability to move between hosts and locations. Together, our results suggest an upper limit to the number of host individuals that malaria parasites, as a community, can infect. Within this limit, however, the relative frequency of the different lineages varies reflecting fine scale interactions between host and parasite populations. Patterns of host-parasite associations within this system suggest both historical co-evolution and ecologically dynamic and independent host-parasite interactions.