Host manipulation by Ligula intestinalis: a cause or consequence of parasite aggregation?

Previous investigations suggest that the infection of the cyprinid roach, Rutilus rutilus, with the larval plerocercoid forms of the cestode, Ligula intestinalis, creates behavioural and morphological changes in the fish host, potentially of adaptive significance to the parasite in promoting transmission to definitive avian hosts. Here we consider whether these behavioural changes are important in shaping the distribution of parasite individuals across the fish population. An examination of field data illustrates that fish infected with a single parasite were more scarce than expected under the negative binomial distribution, and in many months were more scarce than burdens of two, three or more, leading to a bimodal distribution of worm counts (peaks at 0 and >1). This scarcity of single-larval worm infections could be accounted for a priori by a predominance of multiple infection. However, experimental infections of roach gave no evidence for the establishment of multiple worms, even when the host was challenged with multiple intermediate crustacean hosts, each multiply infected. A second hypothesis assumes that host manipulation following an initial single infection leads to an increased probability of subsequent infection (thus creating a contagious distribution). If manipulated fish are more likely to encounter infected first-intermediate hosts (through microhabitat change, increased ingestion, or both), then host manipulation could act as a powerful cause of aggregation. A number of scenarios based on contagious distribution models of aggregation are explored, contrasted with alternative compound Poisson models, and compared with the empirical data on L. intestinalis aggregation in their roach intermediate hosts. Our results indicate that parasite-induced host manipulation in this system can function simultaneously as both a consequence and a cause of parasite aggregation. This mutual interaction between host manipulation and parasite aggregation points to a set of ecological interactions that are easily missed in most experimental studies of either phenomenon.     

Genes involved in host–parasite interactions can be revealed by their correlated expression

Molecular interactions between a parasite and its host are key to the ability of the parasite to enter the host and persist. Our understanding of the genes and proteins involved in these interactions is limited. To better understand these processes it would be advantageous to have a range of methods to predict pairs of genes involved in such interactions. Correlated gene expression profiles can be used to identify molecular interactions within a species. Here we have extended the concept to different species, showing that genes with correlated expression are more likely to encode proteins, which directly or indirectly participate in host–parasite interaction. We go on to examine our predictions of molecular interactions between the malaria parasite and both its mammalian host and insect vector. Our approach could be applied to study any interaction between species, for example, between a host and its parasites or pathogens, but also symbiotic and commensal pairings.     

How many pathways for invasion of the red blood cell by the malaria parasite?

Merozoites of the malaria parasite Plasmodium falciparum use several receptors for cellular engagement when they invade human red blood cells. Recently, a merozoite erythrocyte-binding protein, EBA-140, has been identified that specifically binds to glycophorin C on red blood cells. Up to 50% of Melanesians have a deletion in this gene, and the resultant Gerbich-negative red blood cells are relatively resistant to invasion. While discovery of multiple pathways for invasion could confound the search for suitable vaccine targets, they could also be considered in the design of therapeutic interventions that prevent malaria parasites entering red blood cells.     

Diphyllobothrium: Neolithic parasite?

During paleoparasitological analyses on several Neolithic sites in Switzerland (Arbon-Bleiche 3) and southwestern Germany (Hornstaad-H?rnle I, Torwiesen II, and Seekirch-Stockwiesen), numerous eggs of Diphyllobothrium sp. were recovered. This is one of the earliest occurrences of this parasite during the prehistoric period in the Old World. The prevalence of this helminth in the samples studied raises the question as to how important parasitic diseases were during the Neolithic period and what their actual consequences were.     

Host–parasite coevolution beyond the nestling stage? Mimicry of host fledglings by the specialist screaming cowbird

Egg mimicry by obligate avian brood parasites and host rejection of non-mimetic eggs are well-known textbook examples of host-parasite coevolution. By contrast, reciprocal adaptations and counteradaptations beyond the egg stage in brood parasites and their hosts have received less attention. The screaming cowbird (Molothrus rufoaxillaris) is a specialist obligate brood parasite whose fledglings look identical to those of its primary host, the baywing (Agelaioides badius). Such a resemblance has been proposed as an adaptation in response to host discrimination against odd-looking young, but evidence supporting this idea is scarce. Here, we examined this hypothesis by comparing the survival rates of young screaming cowbirds and non-mimetic shiny cowbirds (Molothrus bonariensis) cross-fostered to baywing nests and quantifying the similarity in plumage colour and begging calls between host and cowbird fledglings. Shiny cowbirds suffered higher post-fledging mortality rates (83%) than screaming cowbirds (0%) owing to host rejection. Visual modelling revealed that screaming cowbirds, but not shiny cowbirds, were indistinguishable from host young in plumage colour. Similarly, screaming cowbirds matched baywings' begging calls more closely than shiny cowbirds. Our results strongly support the occurrence of host fledgling mimicry in screaming cowbirds and suggest a role of visual and vocal cues in fledgling discrimination by baywings.     

Why should parasite resistance be costly?

Parasite resistance is sometimes associated with fitness costs. Costs of resistance are fundamentally important in epidemiology, and in the ecology and evolution of host-parasite interactions. The cost of resistance is often envisioned as the cost of re-allocating limiting resources to resistance machinery from other traits. This popular paradigm has resulted in a spate of research that assumes a fitness cost to resistance. We comment on this trend and propose a working framework of various resistance means and mechanisms. Within these means and mechanisms, we suggest that many are not likely to incur significant fitness costs.     

How adaptive is parasite species diversity?

Has species diversity in parasites evolved as a by-product of adaptive diversification driven by competition for limited resources? Or is it a result of gradual genetic drift in isolation? One can move closer to answering these questions by evaluating the ubiquity of host switching, the key stage of adaptive diversification. Studies dealing with evolutionary role of host switching suggest that this process is extremely common in the wild, thus pointing at adaptive nature of parasite species diversity. However, most of these studies are focused on the evidence that may or may not have emerged as a consequence of host switching, – an approach potentially associated with a degree of uncertainty. After an overview of the data I am making an attempt to get a clearer view on host switching by focusing on factors that cause this phenomenon. In particular, I review theoretical work and field observations in order to identify the type of genetic host-use variance and the type of dispersal that underpin host switching. I show that host switching is likely to require generalist modifier alleles which increase the host range of individual genotypes and is likely to be promoted by wave-like patterns of dispersal. Both factors appear to be common in parasites. I conclude by outlining key areas for future research, including: (i) direct testing for divergence with gene flow, the main “footprint” of adaptive speciation; (ii) investigating the association between demography, dispersal potential and the potential to colonise novel habitats; and (iii) determining the genetic mechanisms underpinning host range variance in parasites.     

When will rejection of parasite nestlings by hosts of nonevicting avian brood parasites be favored? A misimprinting-equilibrium model

It has been suggested that discrimination and rejection of thenestlings of avian brood parasites are most likely to evolvewhen the parasite nestling is raised alongside the host nestlings,for example, many cowbird-host systems. Under these circumstances,the benefits of discrimination are high because the host parentsmay save most of their brood. However, there is a general absenceof nestling rejection behavior among hosts of nonevicting parasites.In a cost-benefit equilibrium model, based on the premise thathost species learn to recognize their offspring through imprintingon first breeding, we show that nestling recognition can beadaptive for hosts of cowbirds, but only under strict conditions.Namely, when host nestling survival alongside the parasite islow, rates of parasitism are high and the average clutch sizeis large. All of these conditions are seldom simultaneouslyachieved in real systems. Most importantly, the parasite nestling,on average, does not sufficiently depress host nestling survivalto outweigh the costs of nestling recognition and rejectionerrors. Thus, we argue that nestling acceptance behaviors byhosts of nonevicting brood parasites may be explained as anevolutionary equilibrium in which recognition costs act as astabilizing selection pressure against rejection when most ofthe host's offspring survive parasitism.     

The scaling of parasite biomass with host biomass in lake ecosystems: are parasites limited by host resources?

The standing crop biomass of different populations or trophic levels reflects patterns of energy flow through an ecosystem. The contribution of parasites to total biomass is often considered negligible; recent evidence suggests otherwise, although it comes from a narrow range of natural systems. Quantifying how local parasite biomass, whether that of a single species or an assemblage of species sharing the same host, varies across localities with host population biomass, is critical to determine what constrains parasite populations. We use an extensive dataset on all free‐living and parasitic metazoan species from multiple sites in New Zealand lakes to measure parasite biomass and test how it covaries with host biomass. In all lakes, trematodes had the highest combined biomass among parasite taxa, ranging from about 0.01 to 0.25 g m^?2, surpassing the biomass of minor free‐living taxa. Unlike findings from other studies, the life stage contributing the most to total trematode biomass was the metacercarial stage in the second intermediate host, and not sporocysts or rediae within snail first intermediate hosts, possibly due to low prevalence and small snail sizes. For populations of single parasite species, we found no relationship between host and parasite biomass for either juvenile or adult nematodes. In contrast, all life stages of trematodes had local biomasses that correlated positively with those of their hosts. For assemblages of parasite species sharing the same host, we found strong relationships between local host population biomass and the total biomass of parasites supported. In these host–parasite biomass relationships, the scaling factor (slope in log‐log space) suggests that parasites may not be making full use of available host resources. Host populations appear capable of supporting a little more parasite biomass, and may be open to expansion of existing parasites or invasion by new ones.     

Carcinogenic liver fluke Opisthorchis viverrini oxysterols detected by LC–MS/MS survey of soluble fraction parasite extract

Liquid chromatography in tandem mass spectrometry (LC–MS/MS) has emerged as an informative tool to investigate oxysterols (oxidized derivatives of cholesterol) in helminth parasite associated cancers. Here, we used LC–MS/MS to investigate in soluble extracts of the adult developmental stage of Opisthorchis viverrini from experimentally infected hamsters. Using comparisons with known bile acids and the metabolites of estrogens, the LC–MS data indicated the existence of novel oxysterol derivatives in O. viverrini. Most of these derivatives were ramified at C-17, in similar fashion to bile acids and their conjugated salts. Several were compatible with the presence of an estrogen core, and/or hydroxylation of the steroid aromatic ring A, hydroxylation of both C-2 and C-3 of the steroid ring and further oxidation into an estradiol-2,3-quinone.     

Understanding parasite strategies: a state-dependent approach?

Understanding and predicting parasite strategies is of interest not only for parasitologists, but also for anyone interested in epidemiology, control strategies and evolutionary medicine. From an ecological and evolutionary perspective, parasites are an important feature of their hosts' selective environment, and may have diverse roles, ranging from the evolution of host sex to host-sexual selection behavior. Generally, it is the hosts and their biology that have been the focus of these evolutionary investigations, but we approach the subject from the parasites' perspective, illustrating the sophistication of parasite strategies in dealing with contrasting and unpredictable environments.     

Is more better? Polyploidy and parasite resistance

Ploidy-level variation is common and can drastically affect organismal fitness. We focus on the potential consequences of this variation for parasite resistance. First, we elucidate connections between ploidy variation and key factors determining resistance, including allelic diversity, gene expression and physiological condition. We then argue that systems featuring both natural and artificially manipulated ploidy variation should be used to evaluate whether ploidy level influences host-parasite interactions.     

Host–parasite interactions in vector-borne protozoan infections

Protists embrace many species, some of which may be either occasional or permanent parasites of vertebrate animals. Between the parasite species, several of medical and veterinary importance are vector-transmitted. The ecology and epidemiology of vector-borne parasitoses, including babesiosis, leishmaniasis and malaria, are particularly complex, as they are influenced by many factors, such as vector reproductive efficiency and geographical spread, vectorial capacity, host immunity, travel and human behaviour and climatic factors. Transmission dynamics are determined by the interactions between pathogen, vector, host and environmental factors and, given their complexity, many different types of mathematical models have been developed to understand them. A good basic knowledge of vector-pathogen relationships and transmission dynamics is thus essential for disease surveillance and control interventions and may help in understanding the spread of epidemics and be useful for public health planning.     

Invaders interfere with native parasite–host interactions

The introduction of species is of increasing concern as invaders often reduce the abundance of native species due to a variety of interactions like habitat engineering, predation and competition. A more subtle and not recognized effect of invaders on their recipient biota is their potential interference with native parasite–host interactions. Here, we experimentally demonstrate that two invasive molluscan filter-feeders of European coastal waters interfere with the transmission of free-living infective trematode larval stages and hereby mitigate the parasite burden of native mussels (Mytilus edulis). In laboratory mesocosm experiments, the presence of Pacific oysters (Crassostrea gigas) and American slipper limpets (Crepidula fornicata) reduced the parasite load in mussels by 65–77% and 89% in single and mixed species treatments, respectively. Both introduced species acted as decoys for the trematodes thus reducing the risk of hosts to become infected. This dilution effect was density-dependent with higher reductions at higher invader densities. Similar effects in a field experiment with artificial oyster beds suggest the observed dilution effect to be relevant in the field. As parasite infections have detrimental effects on the mussel hosts, the presence of the two invaders may elicit a beneficial effect on mussels. Our experiments indicate that introduced species alter native parasite–hosts systems thus extending the potential impacts of invaders beyond the usually perceived mechanisms.