Tropics,trophics and taxonomy: the determinants of parasite‐associated host mortality

Empirical studies often reveal deleterious effects of parasites on host survival, but the ecological and environmental processes modulating parasite‐associated host mortality are not well understood. We conducted meta‐analysis of experimental studies assessing parasite‐associated mortality (n = 52) to evaluate broad‐scale patterns in host mortality risk relative to host or parasite taxon, parasite life cycle, or local environmental conditions. Overall, likelihood of host mortality was ～2.6 times higher among infected individuals when compared with hosts that either lacked parasites or had experimentally‐reduced parasite burdens. Parasites with complex life cycles reliant on predation‐mediated transmission generally were associated with higher mortality risk than those exploiting other transmission strategies. We also detected a negative relationship between parasite‐associated host mortality and latitude; host mortality risk declined by ～2.6% with each degree increase in latitude. This result indicated the likely importance of abiotic factors in determining parasite effects. Host taxonomy further influenced parasite‐associated mortality risk, with amphibian, fish, and mollusc hosts generally having higher hazard than arthropod, mammal, and bird hosts. Our results suggest patterns that conform to the predicted link between host mortality and parasite transmissibility, and pathogenicity. The relationship between host mortality and latitude in particular may portend marked shifts in host–parasite relationships pursuant to ongoing and projected global climate change.     

Trade-offs in the evolution of virulence in an indirectly transmitted macroparasite

The adaptive trade-off theory for the evolution and maintenance of parasite virulence requires that virulence be genetically correlated with other fitness characteristics of the parasite. Many theoretical models rely on a positive correlation between virulence and transmissibility. They assume that high parasite replication rates are associated with a high probability of transmission (and, hence, increased parasite fitness), but also with high levels of damage to the host (high virulence). Schistosomes are macroparasites with an indirect life cycle involving a mammalian and a molluscan host. Here we demonstrate, through the development of five substrains, a genetic basis for schistosome virulence. We used these substrains further in order to investigate the presence of parasite fitness traits that were genetically correlated with virulence. High virulence in the (mouse) definitive host was, as predicted, positively correlated with parasite replication. In contrast, in the (snail) intermediate host high virulence was associated with low parasite replication rates. Variation in infectivity to and parasite replication in the definitive host was suggested as a compensating mechanism for the maintenance of virulence in the snail host. This is the first report of a trade-off in parasite reproductive success across hosts in an indirectly transmitted macroparasite.     

Rosetting is associated with increased Plasmodium falciparum in vivo multiplication rate in the Saimiri sciureus monkey

Severe Plasmodium falciparum malaria in African children is associated with high peripheral parasite densities and high rate of rosette-forming parasites. To explore the relationship between rosette formation and parasite density in vivo, we compared the multiplication rate of a rosette-forming variant (varO) of the Palo Alto line with a sibling non-rosetting variant (varR) in splenectomized Saimiri monkeys. The multiplication rate of varO parasites was 1.5-fold higher than that of the varR variant. This indicates that rosetting is indeed associated with high parasite multiplication efficiency in vivo and, as such, may contribute to the high parasite densities observed in severe malaria.     

Patterns of parasite species richness of Western Palaeartic micro-mammals: island effects

We investigate the patterns of parasite species richness of small mammals of the Western Palaearctic, and the effects of insularity. We compiled 28 studies dealing with 16 species of mammals. There was a significant effect of area size on the total parasite species richness, controlling for host sample size. Four mammal species were sufficiently sampled. Two are associated with humans: Mus musculus, and Rattus rattus , and two are not associated with humans, Apodemus sylvaticus and Clethrionomys glaerolus. We show that there is an effect of insularity on parasite species richness of A. sylvaticus . Rodents associated with humans show no effect of insularity on parasite species richness. These rodents appear to reflect a more complex pattern of parasite species richness, probably because of their close association with humans. Host specificity of parasites significantly decreases on islands, with the exception of Rattus rattus . We use parasitological data in order to explore the geographical connections between host populations. We show that parasites may help to resolve these connections but we emphasise that parasites are better geographic than phylogenetic markers.     

TgM2AP participates in Toxoplasma gondii invasion of host cells and is tightly associated with the adhesive protein TgMIC2

Like other members of the medically important phylum Apicomplexa, Toxoplasma gondii is an obligate intracellular parasite that secretes several classes of proteins involved in the active invasion of target host cells. Proteins in apical secretory organelles known as micronemes have been strongly implicated in parasite attachment to host cells. TgMIC2 is a microneme protein with multiple adhesive domains that bind target cells and is mobilized onto the parasite surface during parasite attachment. Here, we describe a novel parasite protein, TgM2AP, which is physically associated with TgMIC2. TgM2AP complexes with TgMIC2 within 15 min of synthesis and remains associated with TgMIC2 in the micronemes, on the parasite surface during invasion and in the culture medium after release from the parasite plasma membrane. TgM2AP is proteolytically processed initially when its propeptide is removed during transit through the golgi and later while it occupies the parasite surface after discharge from the micronemes. We show that TgM2AP is a member of a protein family expressed by coccidian parasites including Neospora caninum and Eimeria tenella. This phylogenic conservation and association with a key adhesive protein suggest that TgM2AP is a fundamental component of the T. gondii invasion machinery.     

Insights into fish host-parasite trophic relationships revealed by stable isotope analysis

Trophic relationships between 10 species of fish host and their associated nematode, cestode, and copepod parasites were investigated using stable isotopes of carbon and nitrogen. Nematodes and cestodes were consistently depleted in 15N with respect to their host, and such fractionation patterns are unlike those conventionally observed between consumers and their diets. Species of copepod parasite were sometimes depleted and sometimes enriched in 15N with respect to fish hosts, and this confirms earlier reports that the nature and magnitude of ectoparasite-host fractionations can vary. Significant differences in delta15N and delta13C were observed among fish tissues, and the isotopic signature of parasites did not always closely correspond to that of the tissue with which the parasite was found most closely associated, or on which the parasite was thought to be feeding. Several possible explanations are considered for such discrepancies, including selective feeding on specific amino acids or lipids, migration of the parasite among different fish tissues, changes in the metabolism of the parasite associated with life history and migration between different host animals.     

Transcriptomic profiling of Alexandrium fundyense during physical interaction with or exposure to chemical signals from the parasite Amoebophrya

Toxic microalgae have their own pathogens, and understanding the way in which these microalgae respond to antagonistic attacks may provide information about their capacity to persist during harmful algal bloom events. Here, we compared the effects of the physical presence of the parasite Amoebophrya sp. and exposure to waterborne cues from cultures infected with this parasite, on gene expression by the toxic dinoflagellates, Alexandrium fundyense. Compared with control samples, a total of 14 882 Alexandrium genes were differentially expressed over the whole‐parasite infection cycle at three different time points (0, 6 and 96 h). RNA sequencing analyses indicated that exposure to the parasite and parasitic waterborne cues produced significant changes in the expression levels of Alexandrium genes associated with specific metabolic pathways. The observed upregulation of genes associated with glycolysis, the tricarboxylic acid cycle, fatty acid β‐oxidation, oxidative phosphorylation and photosynthesis suggests that parasite infection increases the energy demand of the host. The observed upregulation of genes correlated with signal transduction indicates that Alexandrium could be sensitized by parasite attacks. This response might prime the defence of the host, as indicated by the increased expression of several genes associated with defence and stress. Our findings provide a molecular overview of the response of a dinoflagellate to parasite infection.     

Host ecology and life-history traits associated with blood parasite species richness in birds

Identifying host traits associated with the number of different parasite species or strains harboured by a particular host species can have important implications for understanding the impact of parasitism on hosts. We investigated associations between host ecology and life history, and parasite richness and prevalence of the four major avian blood parasite genera. We used an extensive data on blood parasite infections and host ecology in 263 bird species from the Western Palearctic, combining species-specific data with a comparative approach to control for similarity in phenotype among host species due to the effects of common phylogenetic descent. Adult survival rate negatively correlated with the number of parasite species infecting a host species when controlling for similarity due to common descent and body mass. In addition, the prevalence of Haemoproteus, Plasmodium and Leucocytozoon was higher in species harbouring a richer parasite assemblage. These results suggest that the impact on host fitness caused by avian haematozoa may be underestimated in natural populations if the exacerbated virulence associated with exposure to multiple parasites is not taken into account.     

Parasite‐associated mortality in a long‐lived mammal: Variation with host age,sex, and reproduction

Parasites can cause severe host morbidity and threaten survival. As parasites are generally aggregated within certain host demographics, they are likely to affect a small proportion of the entire population, with specific hosts being at particular risk. However, little is known as to whether increased host mortality from parasitic causes is experienced by specific host demographics. Outside of theoretical studies, there is a paucity of literature concerning dynamics of parasite‐associated host mortality. Empirical evidence mainly focuses on short‐lived hosts or model systems, with data lacking from long‐lived wild or semi‐wild vertebrate populations. We investigated parasite‐associated mortality utilizing a multigenerational database of mortality, health, and reproductive data for over 4,000 semi‐captive timber elephants (Elephas maximus), with known causes of death for mortality events. We determined variation in mortality according to a number of host traits that are commonly associated with variation in parasitism within mammals: age, sex, and reproductive investment in females. We found that potentially parasite‐associated mortality varied significantly across elephant ages, with individuals at extremes of lifespan (young and old) at highest risk. Mortality probability was significantly higher for males across all ages. Female reproducers experienced a lower probability of potentially parasite‐associated mortality than females who did not reproduce at any investigated time frame. Our results demonstrate increased potentially parasite‐associated mortality within particular demographic groups. These groups (males, juveniles, elderly adults) have been identified in other studies as susceptible to parasitism, stressing the need for further work investigating links between infection and mortality. Furthermore, we show variation between reproductive and non‐reproductive females, with mothers being less at risk of potentially parasite mortality than nonreproducers.     

Microparasite assemblages of conspecific shrew populations in southern California

The microparasite component communities of 2 species of shrews, Notiosorex crawfordi and Sorex ornatus, were investigated for the first time in 2 isolated and 3 continuous landscapes in southern California. With microscopical examination, a total of 6 parasite species was found in N. crawfordi and 8 species in S. ornatus. The highest number (5) of parasite species was detected in the lungs. The corrected estimate of parasite species richness did not significantly correlate with the host abundance in either shrew species. Altitude, and also latitude in N. crawfordi, appeared to be significantly positively associated with the parasite species richness, but this could be due to a false association because of the rare occurrence of some of the parasites or the small altitude range (or both). No other landscape variable analyzed (location, size of the study site, disturbance) was significantly associated with the parasite species richness of the shrews. The parasite assemblages of the 2 shrew species were similar despite the fact that N. crawfordi has a lower metabolic rate than S. ornatus.     

Parasite recruitment and oceanographic regime: evidence suggesting a relationship on a global scale

We here investigate the relationship between oceanographic processes and variability in parasite recruitment to host populations using existing data from host-parasite systems encountering differing hydrographic conditions. Combined epidemiological data obtained from both exploited fish and cephalopod populations indicate that variability in recruitment of parasite infracommunities tends to be associated with major current systems of the World's oceans. It appears that instability in water masses caused by physical perturbations (e.g. water mass convergence and turbulent mixing in upwelling systems) is associated with instability of trophic interactions over time, which in turn leads to a paucity of parasite communities in that area. The likely relationship between parasite recruitment and oceanographic regime should be extremely useful to the fishing industry and also as an indicator of ecosystem health.     

Vesicle-mediated transport of membrane and proteins in malaria-infected erythrocytes

Malaria parasites during intraerythrocytic development change the ultrastructure, biophysics, and the antigens of the host red blood cell membrane. Parasite-encoded proteins are associated with, inserted into, or secreted across the infected erythrocyte membrane. Since parasites of the genus Plasmodium are eukaryotic cells, it must be assumed that they possess essentially eukaryotic modes of vesicle-mediated transport and translocation of proteins and membranes. Numerous studies have demonstrated vesicular structures in the cytoplasm of malaria-infected red blood cells and an assortment of parasite proteins associated with the different vesicles, membranes, and membrane-defined compartments. Some parasite polypeptides remain trapped between the parasite and the parasitophorous vacuole membranes PVM, whereas others are associated with morphologically distinct membrane-limited vesicles and vacuoles. Some of these same parasite protein antigens also associate with the erythrocyte membrane or with parasite-induced ultrastructural modifications in the membrane of the parasitized red blood cells. This implies that intracellular transport occurs in malaria-infected erythrocytes, a capacity that uninfected red blood cells normally lose upon enucleation. The specific locations of parasite antigens within the infected cell also implys the existence of targeting signals in the translocated parasite polypeptides and perhaps transport-mediating proteins. The genes corresponding to some of these translocated proteins have been sequenced. Typical (and in some cases atypical) signal peptide sequences occur, as well as a number of sequences that may result in posttranslational modifications. How or if these features figure in to the translocation across, and targeting to a particular membrane compartment of the intraerythrocytic parasite remains unknown.(ABSTRACT TRUNCATED AT 250 WORDS)     

Drug-induced death of the asexual blood stages of Plasmodium falciparum occurs without typical signs of apoptosis

There is clear evidence that most antimalarial drugs, while acting through different mechanisms, are associated with parasite growth/development inhibition and eventual parasite death. However, the exact mode of parasite death remains unclear. In the present study, we investigated the ability of various drugs, including two antimalarial drugs (chloroquine and atovaquone), a topoisemerase II inhibitor (etoposide) and a nitric oxide donor (S-nitro-N-acetyl-D, L-penicillamine), to induce apoptosis in a laboratory strain of Plasmodium falciparum. Results obtained from flow cytometric analysis showed a significant reduction in the percent of parasitemia and parasite growth in all drug-treated parasite cultures, including those treated with etoposide and S-nitro-N-acetyl-D, L-penicillamine. For further investigation, we used various biochemical approaches including the terminal dUTP nick-end labeling assay, determination of mitochondrial membrane integrity and DNA degradation/fragmentation, to analyze the changes occurring during parasite-drug interactions and eventual death. We observed that loss of membrane potential was induced in parasite cultures treated with atovaquone, while S-nitro-N-acetyl-D, L-penicillamine induced abnormal parasite forms, "crisis forms", and minor DNA degradation. However, these features were not observed in the parasite cultures treated with chloroquine nor were other features of apoptosis-like death associated with any of the drugs used in this study. The death resulting from the various drug treatments is atypical of apotosis. More studies will be needed to define the precise mode of death exhibited by P. falciparum.     

Life history and virulence are linked in the ectoparasitic salmon louse Lepeophtheirus salmonis

Models of virulence evolution for horizontally transmitted parasites often assume that transmission rate (the probability that an infected host infects a susceptible host) and virulence (the increase in host mortality due to infection) are positively correlated, because higher rates of production of propagules may cause more damages to the host. However, empirical support for this assumption is scant and limited to microparasites. To fill this gap, we explored the relationships between parasite life history and virulence in the salmon louse, Lepeophtheirus salmonis, a horizontally transmitted copepod ectoparasite on Atlantic salmon Salmo salar. In the laboratory, we infected juvenile salmon hosts with equal doses of infective L. salmonis larvae and monitored parasite age at first reproduction, parasite fecundity, area of damage caused on the skin of the host, and host weight and length gain. We found that earlier onset of parasite reproduction was associated with higher parasite fecundity. Moreover, higher parasite fecundity (a proxy for transmission rate, as infection probability increases with higher numbers of parasite larvae released to the water) was associated with lower host weight gain (correlated with lower survival in juvenile salmon), supporting the presence of a virulence–transmission trade‐off. Our results are relevant in the context of increasing intensive farming, where frequent anti‐parasite drug use and increased host density may have selected for faster production of parasite transmission stages, via earlier reproduction and increased early fecundity. Our study highlights that salmon lice, therefore, are a good model for studying how human activity may affect the evolution of parasite virulence.     

Divergent sexual signals reflect costs of local parasites*

Many closely related populations are distinguished by variation in sexual signals and this variation is hypothesized to play an important role in reproductive isolation and speciation. Within populations, there is considerable evidence that sexual signals provide information about the incidence and severity of parasite infections, but it remains unclear if variation in parasite communities across space could play a role in initiating or maintaining sexual trait divergence. To test for variation in parasite-associated selection, we compared three barn swallow subspecies with divergent sexual signals. We found that parasite community structure and host tolerance to ecologically similar parasites varied between subspecies. Across subspecies we also found that different parasites were costly in terms of male survival and reproductive success. For each subspecies, the preferred sexual signal(s) were associated with the most costly local parasite(s), indicating that divergent signals are providing relevant information to females about local parasite communities. Across subspecies, the same traits were often associated with different parasites, indicating that parasite-sexual signal links are quite flexible and may evolve relatively quickly. This study provides evidence for (1) variation in parasite communities and (2) different parasite-sexual signal links among three closely related subspecies with divergent sexual signal traits, suggesting that parasites may play an important role in initiating and/or maintaining the divergence of sexual signals among these closely related, yet geographically isolated populations.     

Lung lesions in an opossum (Didelphis virginiana) associated with Capillaria didelphis

An opossum (Didelphis virginiana) live-trapped on Parramore Island, Virginia was infected with the lung parasite Capillaria didelphis. Lung lesions associated with this parasite were extensive and consisted of numerous areas with central necrosis deep within the parenchyma. Necrotic foci were present around airways and consisted of a mixture of inflammatory cells and cellular debris, adult nematodes and many bipolar eggs. This parasite causes severe verminous pneumonia in the opossum.     

Relative importance of host environment,transmission potential and host phylogeny to the structure of parasite metacommunities

Identification of mechanisms that shape parasite community and metacommunity structures have important implications to host health, disease transmission, and the understanding of community assembly in general. Using a long‐term dataset on parasites from desert rodents, we examined the relative contributions of host traits that represent important aspects of parasite environment, transmission probability between host species, and host phylogeny to the structure of a parasite metacommunity as well as for taxonomically restricted parasite metacommunities (coccidians, ectoparasites and helminths). This was done using a combination of metacommunity analysis and variance partitioning based on canonical correspondence analysis. Coccidian and ectoparasite metacommunities did not exhibit coherent structure. In contrast, helminths and the full parasite metacommunity had Clementsian and quasi‐Clementsian structure, respectively, indicating that parasite species distributions for these metacommunities were compartmentalized along a dominant gradient. Variance decomposition indicated that characteristics associated with the host environment consistently explained more variation than did host traits associated with transmission opportunities or host phylogeny, indicating that the host environment is primary in shaping parasite species distributions among host species. Moreover, the importance of different types of host traits in structuring parasite metacommunities was consistent among taxonomic groups (i.e. full metacommunity, coccidians, and helminths) despite manifest differences in emergent structures (i.e. Clementsian, quasi‐Clementsian, and random) that arose in response to variation in host environment.     

Host and parasite morphology influence congruence between host and parasite phylogenies

Comparisons of host and parasite phylogenies often show varying degrees of phylogenetic congruence. However, few studies have rigorously explored the factors driving this variation. Multiple factors such as host or parasite morphology may govern the degree of phylogenetic congruence. An ideal analysis for understanding the factors correlated with congruence would focus on a diverse host–parasite system for increased variation and statistical power. In this study, we focused on the Brueelia-complex, a diverse and widespread group of feather lice that primarily parasitise songbirds. We generated a molecular phylogeny of the lice and compared this tree with a phylogeny of their avian hosts. We also tested for the contribution of each host–parasite association to the overall congruence. The two trees overall were significantly congruent, but the contribution of individual associations to this congruence varied. To understand this variation, we developed a novel approach to test whether host, parasite or biogeographic factors were statistically associated with patterns of congruence. Both host plumage dimorphism and parasite ecomorphology were associated with patterns of congruence, whereas host body size, other plumage traits and biogeography were not. Our results lay the framework for future studies to further elucidate how these factors influence the process of host–parasite coevolution.