Synchronous attack is advantageous: mixed genotype infections lead to higher infection success in trematode parasites

Co-infecting parasite genotypes typically compete for host resources limiting their fitness. The intensity of such competition depends on whether parasites are reproducing in a host, or using it primarily as a transmission vehicle while not multiplying in host tissues (referred to as 'competition hypothesis'). Alternatively, simultaneous attack and co-infection by several parasite genotypes might facilitate parasite infection because such a diverse attack could present an additional challenge to host immune defence (referred to as 'facilitation hypothesis'). We tested the competition hypothesis by comparing the production of transmission stages (cercariae) from snails infected with one or two genotypes of the trematode Diplostomum pseudospathaceum. We found that cercarial production did not differ between the two groups of snails, suggesting lower per genotype production in double infections, and competition for host resources. Second, we tested the facilitation hypothesis by comparing parasite infection success on fishes (proportion of parasites establishing in the host) using cercariae originating from single-infected snails, double-infected snails and artificial mixtures of the single genotypes. In both cases, we found higher infection success when fishes were challenged with two parasite genotypes instead of one, supporting the facilitation hypothesis. Our results suggest that constraints defining the success of multiple genotype infections in parasites with multiple host life cycles include both between-genotype resource competition in the host and performance of host immune defences against a diverse parasite challenge.     

Host specificity shapes population structure of pinworm parasites in Caribbean reptiles

Host specificity is one of the potential factors affecting parasite diversification because gene flow may be facilitated or constrained by the number of host species that a parasite can exploit. We test this hypothesis using a costructure approach, comparing two sympatric pinworm parasites that differ in host specificity – Parapharyngodon cubensis and Spauligodon anolis – on the Puerto Rican Bank and St. Croix in the Caribbean. Spauligodon anolis specializes on Anolis lizards, whereas P. cubensis parasitizes Anolis lizards as well as many other species of lizards and snakes. We collected lizards from across the Puerto Rican Bank and St. Croix, sampled them for S. anolis and P. cubensis and generated nuclear and mitochondrial sequence data from the parasites. We used these data to show that P. cubensis is comprised of multiple cryptic species that exhibit limited population structure relative to S. anolis, which is consistent with our prediction based on their host specificity. We also provide evidence that the distribution of P. cubensis species is maintained by competitive exclusion, and in contrast to previous theoretical work, the parasites with the greatest number of host species also reach the highest prevalence rates. Overall, our results are consistent with the hypothesis that host specificity shapes parasite diversification, and suggest that even moderate differences in host specificity may contribute to substantial differences in diversification.     

Host associations and beta diversity of fungal endophyte communities in New Guinea rainforest trees

Processes shaping the distribution of foliar fungal endophyte species remain poorly understood. Despite increasing evidence that these cryptic fungal symbionts of plants mediate interactions with pathogens and herbivores, there remain basic questions regarding the extent to which dispersal limitation and host specificity might shape fungal endophyte community composition in rainforests. To assess the relative importance of spatial pattern and host specificity, we isolated fungi from a sample of mapped trees in lowland Papua New Guinea. Sequences of the internal transcribed spacer (ITS) region were obtained for 2079 fungal endophytes from three sites and clustered into molecular operational taxonomic units (MOTUs) at 95% similarity. Multivariate analyses suggest that host affinity plays a significant role in structuring endophyte community composition whereas there was no evidence of endophyte spatial pattern at the scale of tens to hundreds of metres. Differences in endophyte communities between sampled trees were weakly correlated with variation in foliar traits but not with tree species relatedness. The dominance of relatively few generalist endophytes and the presence of a large number of rare MOTUs was a consistent observation at three sites separated by hundreds of kilometres and regional turnover was low. Host specificity appears to play a relatively weak but more important role than dispersal limitation in shaping the distribution of fungal endophyte communities in New Guinea forests. Our results suggest that in the absence of strong ecological gradients and host turnover, beta diversity of endophyte communities could be low in large areas of contiguous forest.     

Relative importance of chemical attractiveness to parasites for susceptibility to trematode infection

While the host immune system is often considered the most important physiological mechanism against parasites, precontact mechanisms determining exposure to parasites may also affect infection dynamics. For instance, chemical cues released by hosts can attract parasite transmission stages. We used the freshwater snail Lymnaea stagnalis and its trematode parasite Echinoparyphium aconiatum to examine the role of host chemical attractiveness, physiological condition, and immune function in determining its susceptibility to infection. We assessed host attractiveness through parasite chemo‐orientation behavior; physiological condition through host body size, food consumption, and respiration rate; and immune function through two immune parameters (phenoloxidase‐like and antibacterial activity of hemolymph) at an individual level. We found that, although snails showed high variation in chemical attractiveness to E. aconiatum cercariae, this did not determine their overall susceptibility to infection. This was because large body size increased attractiveness, but also increased metabolic activity that reduced overall susceptibility. High metabolic rate indicates fast physiological processes, including immune activity. The examined immune traits, however, showed no association with susceptibility to infection. Our results indicate that postcontact mechanisms were more likely to determine snail susceptibility to infection than variation in attractiveness to parasites. These may include localized immune responses in the target tissue of the parasite. The lack of a relationship between food consumption and attractiveness to parasites contradicts earlier findings that show food deprivation reducing snail attractiveness. This suggests that, although variation in resource level over space and time can alter infection dynamics, variation in chemical attractiveness may not contribute to parasite‐induced fitness variation within populations when individuals experience similar environmental conditions.     

Small worms, big appetites: ratios of different functional morphs in relation to interspecific competition in trematode parasites

Animals living in colonies or collectives composed of highly-related individuals often produce morphs that are physically and behaviourally specialised to perform specific tasks. Because such morphs are often sterile, their production represents a fitness cost for the colony and there should be an optimal ratio of the numbers of sterile specialists and reproductive members that may be adjustable to environmental conditions. Trematode parasites undergo asexual multiplication within their snail intermediate host, resulting in large numbers of clonal stages known as rediae or sporocysts, depending on the trematode species. In areas with high prevalences of infection, the host can be infected by multiple species, which can lead to intense competition for limited resources. Here, we describe the existence of specialised ‘mini-rediae’ in the trematode Philophthalmus sp. that are morphologically and functionally specialised for interspecific competition. Mini-rediae were observed feeding on the sporocysts of a co-occurring trematode species - Maritrema novaezealandensis. In addition, in larger snails - which are less likely to have M. novaezealandensis infections - Philophthalmus sp. produces relatively fewer mini-rediae than expected. Our findings support results from a prior study which demonstrated the existence of morphs that perform specialised functions in antagonistic interspecific interactions in trematodes, and additionally shows that the number of these morphs in each host is associated with the likelihood of encountering other species within the same host. Trematodes may thus provide interesting models for studying morphological specialisation in colonial organisms.     

The effects of gregarine parasites on longevity, weight loss, fecundity and developmental time in the field crickets Gryllus veletis and G.pennsylvanicus

ABSTRACT. 1. Gregarines, debilitating gut parasites, significantly reduced longevity and increased weight loss in the field cricket Gryllus pennsylvanicus Burmeiser when adults were kept on suboptimal diets, but in G.pennsylvanicus and G.veletis (Alexander and Bigelow) fed ad libitum , weight change, longevity, and fecundity were not significantly different in infected and control individuals.
2. Adults harbouring gregarines at eclosion took significantly longer to develop from the second and third instars than did uninfected adults.
3. Longevity of nymphs kept in the laboratory without food was decreased in infected individuals compared with uninfected ones, but not significantly so.
4. The evolutionary and ecological implications of nonlethal parasites are discussed.     

Contrasting mtDNA diversity and population structure in a direct-developing marine gastropod and its trematode parasites

The comparative genetic structure of hosts and their parasites has important implications for their coevolution, but has been investigated in relatively few systems. In this study, we analysed the genetic structure and diversity of the New Zealand intertidal snail Zeacumantus subcarinatus ( n  =   330) and two of its trematode parasites, Maritrema novaezealandensis ( n  =   269) and Philophthalmus sp. ( n  =   246), using cytochrome c oxidase subunit I gene ( COI ) sequences. Snails and trematodes were examined from 11 collection sites representing three regions on the South Island of New Zealand. Zeacumantus subcarinatus displayed low genetic diversity per geographic locality, strong genetic structure following an isolation by distance pattern, and low migration rates at the scale of the study. In contrast, M. novaezealandensis possessed high genetic diversity, genetic homogeneity among collection sites and high migration rates. Genetic diversity and migration rates were typically lower for Philophthalmus sp. compared to M. novaezealandensis and it displayed weak to moderate genetic structure. The observed patterns likely result from the limited dispersal ability of the direct developing snail and the utilization of bird definitive hosts by the trematodes. In addition, snails may occasionally experience long-distance dispersal. Discrepancies between trematode species may result from differences in their effective population sizes and/or life history traits.     

Analysis of a summary network of co-infection in humans reveals that parasites interact most via shared resources

Simultaneous infection by multiple parasite species (viruses, bacteria, helminths, protozoa or fungi) is commonplace. Most reports show co-infected humans to have worse health than those with single infections. However, we have little understanding of how co-infecting parasites interact within human hosts. We used data from over 300 published studies to construct a network that offers the first broad indications of how groups of co-infecting parasites tend to interact. The network had three levels comprising parasites, the resources they consume and the immune responses they elicit, connected by potential, observed and experimentally proved links. Pairs of parasite species had most potential to interact indirectly through shared resources, rather than through immune responses or other parasites. In addition, the network comprised 10 tightly knit groups, eight of which were associated with particular body parts, and seven of which were dominated by parasite–resource links. Reported co-infection in humans is therefore structured by physical location within the body, with bottom-up, resource-mediated processes most often influencing how, where and which co-infecting parasites interact. The many indirect interactions show how treating an infection could affect other infections in co-infected patients, but the compartmentalized structure of the network will limit how far these indirect effects are likely to spread.     

Evidence of an interannual effect of maternal immunization on the immune response of juveniles in a long-lived colonial bird

Little is known about the maternal transfer of antibodies in natural host-parasite systems despite its possible evolutionary and ecological implications. In domestic animals, the maternal transfer of antibodies can enhance offspring survival via a temporary protection against parasites, but it can also interfere with the juvenile immune response to antigens. We tested the functional role of maternal antibodies in a natural population of a long-lived colonial seabird, the kittiwake (Rissa tridactyla), using a vaccine (Newcastle disease virus vaccine) to mimic parasite exposure combined with a cross-fostering design. We first investigated the role of prior maternal exposure on the interannual transmission of Ab to juveniles. We then tested the effect of these antibodies on the juvenile immune response to the same antigen. The results show that specific maternal antibodies were transferred to chicks 1 year after maternal exposure and that these antibodies were functional, i.e. they affected juvenile immunity. These results suggest that the role of maternal antibodies may depend on the timing and pattern of offspring exposure to parasites, along with the patterns of maternal exposure and the dynamics of her immune response. Overall, our approach underlines that although the transgenerational transfer of antibodies in natural populations is likely to have broad implications, the nature of these effects may vary dramatically among host-parasite systems, depending on the physiological mechanisms involved and the ecological context.     

Cowpox virus infection in natural field vole Microtus agrestis populations: delayed density dependence and individual risk

1. Little is known about the dynamics of pathogen (microparasite) infection in wildlife populations, and less still about sources of variation in the risk of infection. Here we present the first detailed analysis of such variation. 2. Cowpox virus is an endemic sublethal pathogen circulating in populations of wild rodents. Cowpox prevalence was monitored longitudinally for 2 years, in populations of field voles exhibiting multiannual cycles of density in Kielder Forest, UK. 3. The probability that available susceptible animals seroconverted in a given trap session was significantly positively related to host density with a 3-month time lag. 4. Males were significantly more likely to seroconvert than females. 5. Despite most infection being found in young animals (because transmission rates were generally high) mature individuals were more likely to seroconvert than immature ones, suggesting that behavioural or physiological changes associated with maturity contribute to variation in infection risk. 6. Hence, these analyses confirm that there is a delayed numerical response of cowpox infection to vole density, supporting the hypothesis that endemic pathogens may play some part in shaping vole cycles.     

Direct non-insect-vector transmission of Leishmania parasites in mice

Animal to animal non-vector transmission of Leishmania major was investigated in Balb/c mice, a strain known for its susceptibility to this parasite. Both overt or inapparent infection (documented by positive spleen cultures) was possible after prolonged contact with infected animals. Similarly transmission of infection from infected mothers to their offspring was documented.     

Population structure and the co-evolution between social parasites and their hosts

Co-evolutionary trajectories of host-parasite interactions are strongly affected by the antagonists' evolutionary potential, which in turn depends on population sizes as well as levels of recombination, mutation, and gene flow. Under similar selection pressures, the opponent with the higher evolutionary rate is expected to lead the co-evolutionary arms race and to develop local adaptations. Here, we use mitochondrial DNA sequence data and microsatellite markers to assess the amount of genetic variability and levels of gene flow in two host-parasite systems, each consisting of an ant social parasite--the European slavemaker Harpagoxenus sublaevis and the North American slavemaker Protomognathus americanus--and its two main host species. Our population genetic analyses revealed limited gene flow between individual populations of both host and parasite species, allowing for a geographic mosaic of co-evolution. In a between-system comparison, we found less genetic variability and more pronounced structure in Europe, where previous behavioural studies demonstrated strong local adaptation. Within the European host-parasite system, the larger host species Leptothorax acervorum exhibited higher levels of both genetic variability and gene flow, and previous field data showed that it is less affected by the social parasite H. sublaevis than the smaller host Leptothorax muscorum, which has genetically depleted and isolated populations. In North America, the parasite P. americanus showed higher levels of gene flow between sites, but overall less genetic diversity than its hyper-variable main host species, Temnothorax longispinosus. Interestingly, recent ecological and chemical studies demonstrated adaptation of P. americanus to local host populations, indicating the importance of migration in co-evolutionary interactions.     

Competition and host size mediate larval anuran interactions with trematode parasites

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Host specificity and incidence of Trypanosoma in some African rainforest birds: a molecular approach

Studies of host-parasite interactions in birds have contributed greatly to our understanding of the evolution and ecology of disease. Here we employ molecular techniques to determine the incidence and study the host-specificity of parasitic trypanosomes in the African avifauna. We developed a polymerase chain reaction (PCR)-based diagnostic test that amplified the small subunit ribosomal RNA gene (SSU rRNA) of Trypanosoma from avian blood samples. This nested PCR assay complements and corroborates information obtained by the traditional method of blood smear analysis. The test was used to describe the incidence of trypanosomes in 479 host individuals representing 71 rainforest bird species from Cameroon, the Ivory Coast and Equatorial Guinea. Forty-two (59%) of these potential host species harboured trypanosomes and 189 individuals (35%) were infected. To examine host and geographical specificity, we examined the morphology and sequenced a portion of the SSU rRNA gene from representative trypanosomes drawn from different hosts and collecting locations. In traditional blood smear analyses we identified two trypanosome morphospecies, T. avium and T. everetti. Our molecular and morphological results were congruent in that these two morphospecies had highly divergent SSU rRNA sequences, but the molecular assay also identified cryptic variation in T. avium, in which we found seven closely allied haplotypes. The pattern of sequence diversity within T. avium provides evidence for widespread trypanosome mixing across avian host taxa and across geographical locations. For example, T. avium lineages with identical haplotypes infected birds from different families, whereas single host species were infected by T. avium lineages with different haplotypes. Furthermore, some conspecific hosts from geographically distant sampling locations were infected with the same trypanosome lineage, but other individuals from those locations harboured different trypanosome lineages. This apparent lack of host or geographical specificity may have important consequences for the evolutionary and ecological interactions between parasitic trypanosomes and their avian hosts.     

Host preference and specialization in Gnathia sp., a common parasitic isopod of coral reef fishes

A gnathiid species (Crustacea: Isopoda; one of the most common ectoparasites of coral reef fishes) from the Great Barrier Reef, Australia, was allowed to choose among fishes from three different families to feed on (using two species of fishes per family). Gnathiids showed a strong preference for labrids, rarely feeding on pomacentrids or apogonids. In a separate experiment, gnathiid host preference did not vary among three labrid fish species. Gnathiids that fed on labrids had higher survival than those that fed on apogonids. Male gnathiids that fed on labrids also moulted to the adult stage more quickly. This suggests that host specialization and local adaptation might be occurring between these ectoparasites and their host fishes at the host fish family level.     

Conflicts over host manipulation between different parasites and pathogens: Investigating the ecological and medical consequences

When parasites have different interests in regard to how their host should behave this can result in a conflict over host manipulation, i.e. parasite induced changes in host behaviour that enhance parasite fitness. Such a conflict can result in the alteration, or even complete suppression, of one parasite's host manipulation. Many parasites, and probably also symbionts and commensals, have the ability to manipulate the behaviour of their host. Non‐manipulating parasites should also have an interest in host behaviour. Given the frequency of multiple parasite infections in nature, potential conflicts of interest over host behaviour and manipulation may be common. This review summarizes the evidence on how parasites can alter other parasite's host manipulation. Host manipulation can have important ecological and medical consequences. I speculate on how a conflict over host manipulation could alter these consequences and potentially offer a new avenue of research to ameliorate harmful consequences of host manipulation.     

Resource predictability and specialization in avian malaria parasites

We tested the hypothesis that avian haemosporidian (malaria) parasites specialize on hosts that can be characterized as predictable resources at a site in Amazonian Ecuador. We incorporated host phylogenetic relationship and relative abundance in assessing parasite specialization, and we examined associations between parasite specialization and three host characteristics – abundance, mass and longevity – using quantile regression, phylogenetic logistic regression and t‐tests. Hosts of specialist malaria parasite lineages were on average more abundant than hosts of generalist parasite lineages, but the relationship between host abundance and parasite specialization was not consistent across analyses. We also found support for a positive association between parasite specialization and host longevity, but this also was not consistent across analyses. Nonetheless, our findings suggest that the predictability of a host resource may play a role in the evolution of specialization. However, we also discuss two alternative explanations to the resource predictability hypothesis for specialization: (i) that interspecific interactions among the parasites themselves might constrain some parasites to a specialist strategy, and (ii) that frequent encounters with multiple host species, mediated by blood‐sucking insects, might promote generalization within this system.