Two different strategies of host manipulation allow parasites to persist in intermediate–definitive host systems

Trophically transmitted parasites start their development in an intermediate host, before they finish the development in their definitive host when the definitive host preys on the intermediate host. In intermediate–definitive host systems, two strategies of host manipulation have been evolved: increasing the rate of transmission to the definitive host by increasing the chance that the definitive host will prey on the intermediate host, or increasing the lifespan of the parasite in the intermediate host by decreasing the predation chance when the intermediate host is not yet infectious. As the second strategy is less well studied than the first, it is unknown under what conditions each of these strategies is prevailed and evolved. We analysed the effect of both strategies on the presence of parasites in intermediate–definitive host systems with a structured population model. We show that the parasite can increase the parameter space where it can persist in the intermediate–definitive host system using one of these two strategies of host manipulation. We found that when the intermediate host or the definitive host has life‐history traits that allow the definitive host to reach large population densities, that is high reproduction rate of the intermediate host or high conversion efficiency of the definitive host (efficiency at which the uninfected definitive host converts caught intermediate hosts into offspring), respectively, evolving manipulation to decrease the predation chance of the intermediate host will be more beneficial than manipulation to increase the predation chance to enhance transmission. Furthermore, manipulation to decrease the predation chance of the intermediate host results in higher population densities of infected intermediate hosts than manipulation that increases the predation chance to enhance transmission. Our study shows that host manipulation in early stages of the parasite development to decrease predation might be a more frequently evolved way of host manipulation than is currently assumed.     

Global patterns in helminth host specificity: phylogenetic and functional diversity of regional host species pools matter

Host specificity has a major influence on a parasite's ability to shift between human and animal host species. Yet there is a dearth of quantitative approaches to explore variation in host specificity across biogeographical scales, particularly in response to the varying community compositions of potential hosts. We built a global dataset of intermediate host associations for nine of the world's most widespread helminth parasites (all of which infect humans). Using hierarchical models, we asked if realised parasite host specificity varied in response to regional variation in the phylogenetic and functional diversities of potential host species. Parasites were recorded in 4–10 zoogeographical regions, with some showing considerable geographical variation in observed versus expected host specificity. Parasites generally exhibited the lowest phylogenetic host specificity in regions with the greatest variation in prospective host phylogenetic diversity, namely the Neotropical, Saharo‐Arabian and Australian regions. Globally, we uncovered notable variation in parasite host shifting potential. Observed host assemblages for Hydatigera taeniaeformis and Hymenolepis diminuta were less phylogenetically diverse than expected, suggesting limited potential to spillover into unrelated hosts. Host assemblages for Echinococcus granulosus, Mesocestoides lineatus and Trichinella spiralis were less functionally diverse than expected, suggesting limited potential to shift across host ecological niches. By contrast, Hyd. taeniaeformis infected a higher functional diversity of hosts than expected, indicating strong potential to shift across hosts with different ecological niches. We show that the realised phylogenetic and functional diversities of infected hosts are determined by biogeographical gradients in prospective host species pools. These findings emphasise the need to account for underlying species diversity when assessing parasite host specificity. Our framework to identify variation in realised host specificity is broadly applicable to other host–parasite systems and will provide key insights into parasite invasion potential at regional and global scales.     

植食性昆虫的寄主选择机理及行为调控策略

害虫是影响农作物生产的重要因素,过度使用化学农药已带来严重的“3R”问题。为了长期有效地控制害虫的危害,基于植食性昆虫寄主选择机制的行为调控策略已成为害虫治理研究的重要方向。天然植物资源（如驱避植物、诱集植物与诱集枝把）、物理模拟材料（如诱集色、驱避色与诱集模型）和人工合成物质（如引诱剂、驱避剂、刺激剂与抑制剂）等研发工作皆取得了突破性的进展。除单一措施的使用外,多种诱集措施协同利用的“诱集＋诱集”策略、诱集措施与趋避措施结合使用的“排斥-诱集”策略也已被广泛应用。     

Effectively vertical transmission of a Drosophila‐parasitic nematode: mechanism and consequences

1. Long‐term control of insects by parasites is possible only if the parasite populations persist. Because parasite transmission rate depends on host density, parasite populations may go extinct during periods of low host density. Vertical transmission of parasites, however, is independent of host density and may therefore provide a demographic bridge through times when their insect hosts are rare. 2. The nematode Howardula aoronymphium, which parasitises mycophagous species of Drosophila, can experience both horizontal and effectively vertical transmission, relative rates of which depend, in theory at least, on the density of hosts at breeding sites. 3. A nine‐generation experiment was carried out in which nematodes were transmitted either exclusively vertically or primarily horizontally. This experiment revealed that these parasites can persist and exhibit positive population growth even when there is only vertical transmission. 4. Assays at the end of the experiment revealed that the vertically transmitted nematodes had suffered no inbreeding depression and that they were similar to the horizontally transmitted nematodes in terms of virulence, infectivity, within‐host growth rate, and fecundity. Thus, vertical transmission of H. aoronymphium did not appear to compromise the ability of these parasites to control Drosophila populations.     

Baculovirus‐induced tree‐top disease: how extended is the role of egt as a gene for the extended phenotype?

Many parasites alter host behaviour to enhance their chance of transmission. Recently, the ecdysteroid UDP‐glucosyl transferase (egt) gene from the baculovirus Lymantria dispar multiple nucleopolyhedrovirus (LdMNPV) was identified to induce tree‐top disease in L. dispar larvae. Infected gypsy moth larvae died at elevated positions (hence the term tree‐top disease), which is thought to promote dissemination of the virus to lower foliage. It is, however, unknown whether egt has a conserved role among baculoviruses in inducing tree‐top disease. Here, we studied tree‐top disease induced by the baculovirus Autographa californica multiple nucleopolyhedrovirus (AcMNPV) in two different host insects, Trichoplusia ni and Spodoptera exigua, and we investigated the role of the viral egt gene therein. AcMNPV induced tree‐top disease in both T. ni and S. exigua larvae, although in S. exigua a moulting‐dependent effect was seen. Those S. exigua larvae undergoing a larval moult during the infection process died at elevated positions, while larvae that did not moult after infection died at low positions. For both T. ni and S. exigua, infection with a mutant AcMNPV lacking egt did not change the position where the larvae died. We conclude that egt has no highly conserved role in inducing tree‐top disease in lepidopteran larvae. The conclusion that egt is a ‘gene for an extended phenotype’ is therefore not generally applicable for all baculovirus–host interactions. We hypothesize that in some baculovirus–host systems (including LdMNPV in L. dispar), an effect of egt on tree‐top disease can be observed through indirect effects of egt on moulting‐related climbing behaviour.     

Survival of the feces: Does a nematode lungworm adaptively manipulate the behavior of its cane toad host?

Parasites can enhance their fitness by modifying the behavior of their hosts in ways that increase rates of production and transmission of parasite larvae. We used an antihelminthic drug to experimentally alter infections of lungworms (Rhabdias pseudosphaerocephala) in cane toads (Rhinella marina). We then compared subsequent behaviors of dewormed toads versus toads that retained infections. Both in the laboratory and in the field, the presence of parasites induced hosts to select higher body temperatures (thereby increasing rates of lungworm egg production), to defecate in moister sites, and to produce feces with higher moisture content (thereby enhancing survival of larvae shed in feces). Because those behavioral modifications enhance rather than decrease parasite fitness, they are likely to have arisen as adaptive manipulations of host behavior rather than as host adaptations to combat infection or as nonadaptive consequences of infection on host physiology. However, the mechanisms by which lungworms alter cane toad thermal preference and defecation are not known. Although many examples of host manipulation by parasites involve intermediate hosts facilitating their own demise, our findings indicate that manipulation of definitive hosts can be as subtle as when and where to defecate.     

Assessment of correlational selection on tolerance and resistance traits in a host plant–parasitic plant interaction

Resistance and tolerance are considered to be different plant strategies against disease. While resistance traits prevent hosts becoming parasitized or reduce the extent of parasitism, tolerance traits reduce the fitness-impact of parasitism on infected hosts. Theoretical considerations predict that in some circumstances mutual redundancy will give hosts with either high resistance or high tolerance a fitness advantage over hosts that exhibit both of these traits together. However, empirical evidence has provided mixed results. In this paper, I describe the pattern of phenotypic selection imposed by the holoparasitic mistletoe Tristerix aphyllus upon resistance (spine length) and tolerance (branching) traits in the cactus Echinopsis chilensis. Results indicate that branching was an efficient compensatory mechanism, reducing 75.5% of the fitness-impact attributable to parasitism. Even though both traits showed a negative correlation, as expected from the presence of allocation costs between strategies, no correlational selection coefficient was significant indicating that selection did not favor alternative combinations of traits. Consequently, I did not find evidence for selection promoting mutually exclusive defense strategies against the mistletoe, which suggests that tolerance and resistance traits may coexist stably in populations of E. chilensis.     

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.     

Mistletoe macroecology: spatial patterns in species diversity and host use across Australia

Mistletoes are parasitic plants, the spatial distributions of which are poorly understood on macroecological scales. Because of their highly unusual life history, investigating mistletoe macroecology may provide new insight into broad‐scale patterns in species distributions. We collated data on the spatial distribution and host use of 65 species of Loranthaceous mistletoes across the continent of Australia, and tested two predictions. First, we predicted mistletoe diversity would be unrelated to productivity (i.e. evapotranspiration and precipitation), as the parasitic lifestyle might relax environmental constraints on their distributions. Second, we predicted that mistletoe host ranges (number of infected host species) would increase in areas with more potential host species. The basis of this prediction is that greater host generality is likely to evolve in regions with greater host diversity because of greater unpredictability in encounter rates with particular host species. Conversely, in regions with fewer potential hosts, randomly dispersing mistletoe propagules are likely to repeatedly encounter particular host species, thus favouring the evolution of host specialization. The results were generally consistent with these predictions. Mistletoe diversity across Australia was weakly associated with environmental conditions, whereas mistletoe host ranges increased significantly with total plant diversity. Macroecological patterns in mistletoes are unusual. In contrast to non‐parasitic plants, mistletoe diversity is poorly correlated with productivity. Host ranges varied predictably across Australia, providing the first quantitative support for the hypothesis that mistletoes in diverse regions tend to be host generalists, whereas mistletoes in depauperate regions tend to be host specialists. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 106 , 459–468.     

Parasite host range and the evolution of host resistance

Parasite host range plays a pivotal role in the evolution and ecology of hosts and the emergence of infectious disease. Although the factors that promote host range and the epidemiological consequences of variation in host range are relatively well characterized, the effect of parasite host range on host resistance evolution is less well understood. In this study, we tested the impact of parasite host range on host resistance evolution. To do so, we used the host bacterium Pseudomonas fluorescens SBW25 and a diverse suite of coevolved viral parasites (lytic bacteriophage Φ2) with variable host ranges (defined here as the number of host genotypes that can be infected) as our experimental model organisms. Our results show that resistance evolution to coevolved phages occurred at a much lower rate than to ancestral phage (approximately 50% vs. 100%), but the host range of coevolved phages did not influence the likelihood of resistance evolution. We also show that the host range of both single parasites and populations of parasites does not affect the breadth of the resulting resistance range in a naïve host but that hosts that evolve resistance to single parasites are more likely to resist other (genetically) more closely related parasites as a correlated response. These findings have important implications for our understanding of resistance evolution in natural populations of bacteria and viruses and other host–parasite combinations with similar underlying infection genetics, as well as the development of phage therapy.     

Priming of host resistance to protect cultured rainbow trout Oncorhynchus mykiss against eye flukes and parasite‐induced cataracts

In the present study, immunologically naive rainbow trout Oncorhynchus mykiss were experimentally exposed to a low‐level Diplostomum spathaceum (Trematoda) infection to stimulate acquired resistance and, along with unexposed controls, were subsequently exposed to natural infection for 8 weeks. The priming of the host resistance, designed to simulate a procedure applicable in aquaculture, decreased the number of establishing parasites compared to untreated controls by the end of the experiment. This effect was slow and did not protect the fish against the parasite‐induced cataracts. The results suggest that this type of priming of host resistance is probably inefficient in preventing the deleterious effects of D. spathaceum infection in aquaculture conditions.     

Brood parasitism causes female‐biased host nestling mortality regardless of parasite species

Inequality in male and female numbers may affect population dynamics and extinction probabilities and so has significant conservation implications. We previously demonstrated that Brown‐headed Cowbird Molothrus ater brood parasitism of Song Sparrows Melospiza melodia results in a 50% reduction in the proportion of female host offspring by day 6 post‐hatch and at fledging, which modelling demonstrated is as significant as nest predation in affecting demography. Many avian brood parasites possess special adaptations to parasitize specific hosts so this sex‐ratio effect could be specific to the interaction between these two species. Alternatively, perturbations associated with brood parasitism per se (e.g. the addition of an extra, larger, unrelated nestling), rather than a Cowbird nestling specifically, may be responsible. We experimentally eliminated the effects of Cowbird‐specific traits by parasitizing nests with a conspecific nestling rather than a Cowbird, while otherwise emulating the circumstances of Cowbird parasitism by adding an extra, larger (2‐day‐older), unrelated Song Sparrow nestling to Song Sparrow nests. Our parasitism treatment led to few host offspring deaths and no evidence of male‐biased sex ratios by day 6 post‐hatch. However, after day 6, female nestling mortality rates increased significantly in experimentally parasitized nests, resulting in a 60% reduction in the proportion of females fledging. Cowbird‐specific traits are thus not necessary to cause female‐biased host nestling mortality and far more general features associated with Cowbird parasitism instead appear responsible. Our results suggest, however, that Cowbird‐specific traits may help accelerate the pace of female host deaths. The conservation implications of our results could be wide reaching. Cowbirds are unrelated to all their hosts, are larger than the great majority, and a Cowbird nestling's presence can mean there is an extra mouth to feed. Thus, sex‐biased mortality in parasitized nests could be occurring across a range of host species.     

A combined parasitological molecular approach for noninvasive characterization of parasitic nematode communities in wild hosts

Most hosts are concurrently or sequentially infected with multiple parasites; thus, fully understanding interactions between individual parasite species and their hosts depends on accurate characterization of the parasite community. For parasitic nematodes, noninvasive methods for obtaining quantitative, species‐specific infection data in wildlife are often unreliable. Consequently, characterization of gastrointestinal nematode communities of wild hosts has largely relied on lethal sampling to isolate and enumerate adult worms directly from the tissues of dead hosts. The necessity of lethal sampling severely restricts the host species that can be studied, the adequacy of sample sizes to assess diversity, the geographic scope of collections and the research questions that can be addressed. Focusing on gastrointestinal nematodes of wild African buffalo, we evaluated whether accurate characterization of nematode communities could be made using a noninvasive technique that combined conventional parasitological approaches with molecular barcoding. To establish the reliability of this new method, we compared estimates of gastrointestinal nematode abundance, prevalence, richness and community composition derived from lethal sampling with estimates derived from our noninvasive approach. Our noninvasive technique accurately estimated total and species‐specific worm abundances, as well as worm prevalence and community composition when compared to the lethal sampling method. Importantly, the rate of parasite species discovery was similar for both methods, and only a modest number of barcoded larvae (n = 10) were needed to capture key aspects of parasite community composition. Overall, this new noninvasive strategy offers numerous advantages over lethal sampling methods for studying nematode–host interactions in wildlife and can readily be applied to a range of study systems.     

Parasite‐induced alterations of host behaviour in a riverine fish: the effects of glochidia on host dispersal

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Mistletoe species richness patterns are influenced more by host geographic range than nitrogen content

Mistletoes are hemiparasites that access water and nutrients from their hosts. Previous studies have suggested that host genera with high nitrogen are parasitized by more mistletoe species but these studies failed to take into account phylogenetic relationships among host genera. Our main question was whether more mistletoe species parasitize host genera with high nitrogen content when phylogenetic relationships were controlled. We also asked whether patterns in mistletoe parasitism were related to host geographic range size, host fruit type and host spinescence. Overall, we found no difference between conventional and phylogenetically controlled analyses. We also found no evidence for higher mistletoe species richness on host genera with high nitrogen, fleshy fruits or spinescence. However, similar to findings for animal parasites, we found that host genera with large geographic range had higher mistletoe species richness. This is likely because a greater number of mistletoe species will encounter hosts that have a greater geographic distribution. Mistletoe studies frequently assume that nitrogen status drives patterns in mistletoe parasitism but our study suggests that macroecological patterns in mistletoe assemblages are primarily determined by host geographic range.     

When parasites disagree: Evidence for parasite‐induced sabotage of host manipulation

Host manipulation is a common parasite strategy to alter host behavior in a manner to enhance parasite fitness usually by increasing the parasite's transmission to the next host. In nature, hosts often harbor multiple parasites with agreeing or conflicting interests over host manipulation. Natural selection might drive such parasites to cooperation, compromise, or sabotage. Sabotage would occur if one parasite suppresses the manipulation of another. Experimental studies on the effect of multi‐parasite interactions on host manipulation are scarce, clear experimental evidence for sabotage is elusive. We tested the effect of multiple infections on host manipulation using laboratory‐bred copepods experimentally infected with the trophically transmitted tapeworm Schistocephalus solidus. This parasite is known to manipulate its host depending on its own developmental stage. Coinfecting parasites with the same aim enhance each other's manipulation but only after reaching infectivity. If the coinfecting parasites disagree over host manipulation, the infective parasite wins this conflict: the noninfective one has no effect. The winning (i.e., infective) parasite suppresses the manipulation of its noninfective competitor. This presents conclusive experimental evidence for both cooperation in and sabotage of host manipulation and hence a proof of principal that one parasite can alter and even neutralize manipulation by another.     

From one host to another: tracking vector movements using microsatellite markers

In principle, the solution to stopping the spread of any vectorborne pathogen is a simple one – just stop infected vectors from biting new hosts and the pathogen cannot spread. Importantly, this does not necessarily require killing all vectors, or protecting all hosts. Transmission only occurs when an infected vector moves to a new host, and so knowing how vectors move between hosts in nature and how they choose hosts is crucial to understanding transmission. For example, the infection status of a potential vector or that of a potential host would have a huge influence on pathogen transmission if it affected vector movement or host choice. Remarkably little is known about how vectors move between and choose hosts in nature, in part because of the logistical difficulties of tracking vector movement. This is why the article by Levin and Parker ( 2014 ) in this issue of Molecular Ecology is so exciting.     

Sexually transmitted diseases of insects: distribution, evolution, ecology and host behaviour

Sexually transmitted diseases (STDs) of insects are known from the mites, nematodes, fungi, protists and viruses. In total 73 species of parasite and pathogen from approximately 182 species of host have been reported. Whereas nearly all vertebrate STDs are viruses or bacteria, the majority of insect STDs are multicellular ectoparasites, protistans or fungi. Insect STDs display a range of transmission modes, with 'pure' sexual transmission only described from ectoparasites, all of which are mites, fungi or nematodes, whereas the microparasitic endo-parasites tend to show vertical as well as sexual transmission. The distribution of STDs within taxa of insect hosts appears to be related to the life histories of the hosts. In particular, STDs will not be able to persist if host adult generations do not overlap unless they are also transmitted by some alternative route. This explains the observation that the Coleoptera seem to suffer from more STDs than other insect orders, since they tend to diapause as adults and are therefore more likely to have overlapping generations of adults in temperate regions. STDs of insects are often highly pathogenic, and are frequently responsible for sterilizing their hosts, a feature which is also found in mammalian STDs. This, combined with high prevalences indicates that STDs can be important in the evolution and ecology of their hosts. Although attempts to demonstrate mate choice for uninfected partners have so far failed it is likely that STDs have other effects on host mating behaviour, and there is evidence from a few systems that they might manipulate their hosts to cause them to mate more frequently. STDs may also play a part in sexual conflict, with males in some systems possibly gaining a selective advantage from transmitting certain STDs to females. STDs may well be important factors in host population dynamics, and some have the potential to be useful biological control agents, but empirical studies on these subjects are lacking.     

Host traits associated with species roles in parasite sharing networks

The community of host species that a parasite infects is often explained by functional traits and phylogeny, predicting that closely related hosts or those with particular traits share more parasites with other hosts. Previous research has examined parasite community similarity by regressing pairwise parasite community dissimilarity between two host species against host phylogenetic distance. However, pairwise approaches cannot target specific host species responsible for disproportionate levels of parasite sharing. To better identify why some host species contribute differentially to parasite diversity patterns, we represent parasite sharing using ecological networks consisting of host species connected by instances of shared parasitism. These networks can help identify host species and traits associated with high levels of parasite sharing that may subsequently identify important hosts for parasite maintenance and transmission within communities. We used global‐scale parasite sharing networks of ungulates, carnivores, and primates to determine if host importance – encapsulated by the network measures degree, closeness, betweenness, and eigenvector centrality – was predictable based on host traits. Our findings suggest that host centrality in parasite sharing networks is a function of host population density and range size, with range size reflecting both species geographic range and the home range of those species. In the full network, host taxonomic family became an important predictor of centrality, suggesting a role for evolutionary relationships between host and parasite species. More broadly, these findings show that trait data predict key properties of ecological networks, thus highlighting a role for species traits in understanding network assembly, stability, and structure.