Effects of antagonistic coevolution on parasite‐mediated host coexistence

Parasites can promote diversity by mediating coexistence between a poorer and superior competitor, if the superior competitor is more susceptible to parasitism. However, hosts and parasites frequently undergo antagonistic coevolution. This process may result in the accumulation of pleiotropic fitness costs associated with host resistance, and could breakdown coexistence. We experimentally investigated parasite‐mediated coexistence of two genotypes of the bacterium Pseudomonas fluorescens, where one genotype underwent coevolution with a parasite (a virulent bacteriophage), whereas the other genotype was resistant to the evolving phages at all time points, but a poorer competitor. In the absence of phages, the resistant genotype was rapidly driven extinct in all populations. In the presence of the phages, the resistant genotype persisted in four of six populations and eventually reached higher frequencies than the sensitive genotype. The coevolving genotype showed a reduction in the growth rate, consistent with a cost of resistance, which may be responsible for a decline in its relative fitness. These results demonstrate that the stability of parasite‐mediated coexistence of resistant and susceptible species or genotypes is likely to be affected if parasites and susceptible hosts coevolve.     

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.     

Brood‐parasite‐induced female‐biased mortality affects songbird demography: negative implications for conservation

Parasites, of all sorts, can profoundly affect host population dynamics. Parasites commonly cause sex‐biased mortality and this can add to their impact. Female‐biased mortality in particular can destabilize dynamics and promote population collapse. We previously reported in a correlative study that brown‐headed cowbird Molothrus ater brood parasitism of song sparrows Melospiza melodia appears to cause female‐biased host nestling mortality. Here, we report results from ‘infestation’ and ‘de‐infestation’ experiments designed to test whether brood parasitism causes female‐biased mortality, and we document the resulting demographic impact using a simulation model. Experimental cowbird infestation of song sparrow nests halved the proportion of female host nestlings (0.31±0.07 vs 0.59±0.06; infested vs unparasitized nests at day 6) replicating the halving reported in naturally cowbird‐parasitized nests (0.28±0.01 vs 0.57±0.05; parasitized vs unparasitized). De‐infestation of naturally cowbird‐parasitized nests in turn wholly eliminated any effect on the proportion of female host nestlings (0.53±0.13 vs 0.54±0.06; de‐infested vs unparasitized) confirming that brood parasitism is the cause. This halving of the proportion of females fledging is likely to be as significant as nest predation in affecting population dynamics, based on the elasticities derived from our demographic model (–0.50 vs –0.59). Experimental infestation reduced the testosterone levels, begging behaviour, and body mass of six day old female host nestlings, whereas males were largely unaffected, suggesting that it is the exacerbation of intra‐brood competition that may be primarily responsible for the resulting female‐biased mortality. The brown‐headed cowbird is invasive in most of North America and has been implicated in regional population declines of many native species. We suggest that female‐biased host offspring mortality is likely to be commonplace among the 144 host species the cowbird successfully parasitizes, and we discuss the negative implications for songbird conservation, given the projected demographic impact.     

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.     

Experimental evidence for parasite‐induced over‐winter mortality in juvenile Rhodeus amarus

In this study, the effects of the eye fluke Diplostomum pseudospathaceum (Trematoda) infection on over‐winter survival of young‐of‐the‐year (YOY) European bitterling Rhodeus amarus (Cyprinidae) were examined between September 2010 and April 2011. The fish were reared in semi‐natural conditions to ensure that results were not confounded by other parasite infections. The cumulative mortality of R. amarus from November until April was significantly higher in D. pseudospathaceum‐infected fish (57·3%) compared to controls (42·1%). Infection of the parental generation did not have any effect on the mortality of juveniles. The results indicate that D. pseudospathaceum infection increases over‐winter mortality of YOY R. amarus. The possible mechanisms causing mortality are discussed.     

Signs of a vector's adaptive choice: on the evasion of infectious hosts and parasite‐induced mortality

Laboratory and field experiments have demonstrated in many cases that malaria vectors do not feed randomly, but show important preferences either for infected or non‐infected hosts. These preferences are likely in part shaped by the costs imposed by the parasites on both their vertebrate and dipteran hosts. However, the effect of changes in vector behaviour on actual parasite transmission remains a debated issue. We used the natural associations between a malaria‐like parasite Polychromophilus murinus, the bat fly Nycteribia kolenatii and a vertebrate host the Daubenton's bat Myotis daubentonii to test the vector's feeding preference based on the host's infection status using two different approaches: 1) controlled behavioural assays in the laboratory where bat flies could choose between a pair of hosts; 2) natural bat fly abundance data from wild‐caught bats, serving as an approximation of realised feeding preference of the bat flies. Hosts with the fewest infectious stages of the parasite were most attractive to the bat flies that did switch in the behavioural assay. In line with the hypothesis of costs imposed by parasites on their vectors, bat flies carrying parasites had higher mortality. However, in wild populations, bat flies were found feeding more based on the bat's body condition, rather than its infection level. Though the absolute frequency of host switches performed by the bat flies during the assays was low, in the context of potential parasite transmission they were extremely high. The decreased survival of infected bat flies suggests that the preference for less infected hosts is an adaptive trait. Nonetheless, other ecological processes ultimately determine the vector's biting rate and thus transmission. Inherent vector preferences therefore play only a marginal role in parasite transmission in the field. The ecological processes rather than preferences per se need to be identified for successful epidemiological predictions.     

Host phenology regulates parasite–host demographic cycles and eco‐evolutionary feedbacks

Parasite–host interactions can drive periodic population dynamics when parasites overexploit host populations. The timing of host seasonal activity, or host phenology, determines the frequency and demographic impact of parasite–host interactions, which may govern whether parasites sufficiently overexploit hosts to drive population cycles. We describe a mathematical model of a monocyclic, obligate‐killer parasite system with seasonal host activity to investigate the consequences of host phenology on host–parasite dynamics. The results suggest that parasites can reach the densities necessary to destabilize host dynamics and drive cycling as they adapt, but only in some phenological scenarios such as environments with short seasons and synchronous host emergence. Furthermore, only parasite lineages that are sufficiently adapted to phenological scenarios with short seasons and synchronous host emergence can achieve the densities necessary to overexploit hosts and produce population cycles. Host‐parasite cycles also generate an eco‐evolutionary feedback that slows parasite adaptation to the phenological environment as rare advantageous phenotypes can be driven extinct due to a population bottleneck depending on when they are introduced in the cycle. The results demonstrate that seasonal environments can drive population cycling in a restricted set of phenological patterns and provide further evidence that the rate of adaptive evolution depends on underlying ecological dynamics.     

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.     

Patterns of diversity and abundance of fleas and mites in the Neotropics: host‐related,parasite‐related and environment‐related factors

The effects of host‐related, parasite‐related and environmental factors on the diversity and abundance of two ectoparasite taxa, fleas (Insecta: Siphonaptera) and mites (Acari: Mesostigmata), parasitic on small mammals (rodents and marsupials), were studied in different localities across Brazil. A stronger effect of host‐related factors on flea than on mite assemblages, and a stronger effect of environmental factors on mite than on flea assemblages were predicted. In addition, the effects of parasite‐related factors on flea and mite diversity and abundance were predicted to manifest mainly at the scale of infracommunities, whereas the effects of host‐related and environmental factors were predicted to manifest mainly at the scale of component and compound communities. This study found that, in general, diversity and abundance of flea and mite assemblages at two lower hierarchical levels (infracommunities and component communities) were affected by host‐related, parasite‐related and environmental factors, and compound communities were affected mainly by host‐related and environmental factors. The effects of factors differed between fleas and mites: in fleas, community structure and abundance depended on host diversity to a greater extent than in mites. In addition, the effects of factors differed among parasite assemblages harboured by different host species.     

Sex differences in host defence interfere with parasite‐mediated selection for outcrossing during host–parasite coevolution

The Red Queen hypothesis proposes that coevolving parasites select for outcrossing in the host. Outcrossing relies on males, which often show lower immune investment due to, for example, sexual selection. Here, we demonstrate that such sex differences in immunity interfere with parasite‐mediated selection for outcrossing. Two independent coevolution experiments with Caenorhabditis elegans and its microparasite Bacillus thuringiensis produced decreased yet stable frequencies of outcrossing male hosts. A subsequent systematic analysis verified that male C. elegans suffered from a direct selective disadvantage under parasite pressure (i.e. lower resistance, decreased sexual activity, increased escape behaviour), which can reduce outcrossing and thus male frequencies. At the same time, males offered an indirect selective benefit, because male‐mediated outcrossing increased offspring resistance, thus favouring male persistence in the evolving populations. As sex differences in immunity are widespread, such interference of opposing selective constraints is likely of central importance during host adaptation to a coevolving parasite.     

Habitat heterogeneity drives the host‐diversity‐begets‐parasite‐diversity relationship: evidence from experimental and field studies

Despite a century of research into the factors that generate and maintain biodiversity, we know remarkably little about the drivers of parasite diversity. To identify the mechanisms governing parasite diversity, we combined surveys of 8100 amphibian hosts with an outdoor experiment that tested theory developed for free‐living species. Our analyses revealed that parasite diversity increased consistently with host diversity due to habitat (i.e. host) heterogeneity, with secondary contributions from parasite colonisation and host abundance. Results of the experiment, in which host diversity was manipulated while parasite colonisation and host abundance were fixed, further reinforced this conclusion. Finally, the coefficient of host diversity on parasite diversity increased with spatial grain, which was driven by differences in their species–area curves: while host richness quickly saturated, parasite richness continued to increase with neighbourhood size. These results offer mechanistic insights into drivers of parasite diversity and provide a hierarchical framework for multi‐scale disease research.     

Magnitude and direction of parasite‐induced phenotypic alterations: a meta‐analysis in acanthocephalans

Several parasite species have the ability to modify their host's phenotype to their own advantage thereby increasing the probability of transmission from one host to another. This phenomenon of host manipulation is interpreted as the expression of a parasite extended phenotype. Manipulative parasites generally affect multiple phenotypic traits in their hosts, although both the extent and adaptive significance of such multidimensionality in host manipulation is still poorly documented. To review the multidimensionality and magnitude of host manipulation, and to understand the causes of variation in trait value alteration, we performed a phylogenetically corrected meta‐analysis, focusing on a model taxon: acanthocephalan parasites. Acanthocephala is a phylum of helminth parasites that use vertebrates as final hosts and invertebrates as intermediate hosts, and is one of the few parasite groups for which manipulation is predicted to be ancestral. We compiled 279 estimates of parasite‐induced alterations in phenotypic trait value, from 81 studies and 13 acanthocephalan species, allocating a sign to effect size estimates according to the direction of alteration favouring parasite transmission, and grouped traits by category. Phylogenetic inertia accounted for a low proportion of variation in effect sizes. The overall average alteration of trait value was moderate and positive when considering the expected effect of alterations on trophic transmission success (signed effect sizes, after the onset of parasite infectivity to the final host). Variation in the alteration of trait value was affected by the category of phenotypic trait, with the largest alterations being reversed taxis/phobia and responses to stimuli, and increased vulnerability to predation, changes to reproductive traits (behavioural or physiological castration) and immunosuppression. Parasite transmission would thereby be facilitated mainly by changing mainly the choice of micro‐habitat and the anti‐predation behaviour of infected hosts, and by promoting energy‐saving strategies in the host. In addition, infection with larval stages not yet infective to definitive hosts (acanthella) tends to induce opposite effects of comparable magnitude to infection with the infective stage (cystacanth), although this result should be considered with caution due to the low number of estimates with acanthella. This analysis raises important issues that should be considered in future studies investigating the adaptive significance of host manipulation, not only in acanthocephalans but also in other taxa. Specifically, the contribution of phenotypic traits to parasite transmission and the range of taxonomic diversity covered deserve thorough attention. In addition, the relationship between behaviour and immunity across parasite developmental stages and host–parasite systems (the neuropsychoimmune hypothesis of host manipulation), still awaits experimental evidence. Most of these issues apply more broadly to reported cases of host manipulation by other groups of parasites.     

Analysis of solitariness in a parasite—host system (Muscidifurax raptor,Hymenoptera: Pteromalidae—Ceratitis capitata,Diptera: Tephritidae)*

Abstract. 1. The behaviour of the parasite Muscidifurax raptor Girault and Sanders was studied when searching for hosts, puparia of the Mediterranean fruit fly, Ceratitis capitata (Wiedemann). At low density females tend to avoid encountering parasitized hosts. This tendency decreases as density of searching females increases. 2. The proportional avoidance of superparasitism was calculated and the effect of increasing number of encounters per host on this parameter was analysed. 3. The mechanisms of solitariness were studied. These mechanisms include: outer marking of the hosts by the female parasite and deliberate physical attack of the newly hatched larvae to eliminate as yet unhatched eggs. 4. In cases of intraspecific competition between larvae, young first or second instar larvae usually have the advantage over older larvae.     

Interpreting multidimensionality in parasite‐induced phenotypic alterations: panselectionism versus parsimony

The purpose of this note is to provide an alternative to the interpretation of multidimensionality in parasite‐induced phenotypic alterations as a set of effectively‐independent traits produced by adaptive evolution. We propose here that infection with so‐called ‘manipulative parasites’ typically results in an ‘infection syndrome’, characterized by several distinctive symptoms corresponding to the alteration of particular phenotypic traits in infected hosts. Based on the available physiological evidence, we argue that symptoms might actually be the consequence of the dysregulation of some key neuromodulator, arising as a byproduct of the subversion of the host's immune system by the parasite. In that respect, it might be inadequate, from a functional point of view, to separate phenotypic effects that appear to increase trophic transmission from those that do not. We suggest that future research should test the validity of the ‘infection syndrome’ hypothesis through focusing on the mechanisms involved in multidimensionality at the intraspecific level, and through looking for the existence of non‐random associations between symptoms at the interspecific level, across host‐parasite associations.     

Cascading trait‐mediation: disruption of a trait‐mediated mutualism by parasite‐induced behavioral modification

Trait‐mediated indirect interactions (TMII) are important driving‐forces causing trophic cascades in aquatic and terrestrial food webs. Furthermore, since most biological communities are not simple food chains but complex networks of interactions, one TMII within a community might easily be influenced by another TMII. In other words, TMII themselves can be cascades with potential implications for community dynamics. Here we report on one of such cascade, where a parasitic fly induces behavioral changes that disrupt a trait‐mediated ant–hemipteran mutualism. We show that during parasite‐induced low‐activity periods, the ant Azteca instabilis fails to protect its mutualistic scale‐insect partner against predatory ladybeetles. Thus, in the presence of the parasite, ladybeetles ate as many scales in ant‐patrolled plants as they did in ant‐free plants. These results demonstrate how, through a cascade of trait‐mediated interactions, associations between members of a community can be drastically altered.     

Sexual,habitat‐constrained and parasite‐induced dimorphism in the shell of a freshwater mussel (Anodonta anatina,Unionidae)

Intraspecific trends in freshwater mussel (unionoid) shells that are consistently associated with differences in the mussels' sex and/or parasitic infestation can potentially be used to reconstruct sex ratios or parasitic levels of modern and ancient unionoid populations. In contrast to morphological patterns within mammal species, such dimorphic trends within unionoid species are, however, poorly understood. This study investigates, for the first time, to what extent sex, trematode infection and indirect habitat effects determine shell morphology in the freshwater mussel Anodonta anatina. Three of the five study populations displayed significant sexual shell width dimorphism. Here, shells of females were significantly wider than males, probably as a result of altered shell growth to accommodate marsupial gills. In two of these populations, female shells were additionally significantly thinner than those of males, which could be a result of resource depletion by offspring production. Two other A. anatina populations showed no significant dimorphic patterns, and our results indicate that this interpopulational difference in the degree of sexual dimorphism may reflect the overarching effect of habitat on morphology. Thus, populations in the most favourable habitats exhibit faster growth rates, attain larger maximum sizes and produce more offspring, which results in more swollen gills and consequently more inflated shells of gravid females compared to less fecund populations. None of the populations showed any evidence for sexual dimorphism in overall size, growth rate, sagittal shape and density of shells. In addition to sexual dimorphisms, infestation by bucephalid trematode parasites (Rhipidocotyle sp.) significantly altered sagittal and lateral shell shape of A. anatina in one of the populations, with infected specimens growing wider and more elongated. J. Morphol. 2011. © 2011 Wiley‐Liss, Inc.     

Dynamic flux of microvesicles modulate parasite–host cell interaction of Trypanosoma cruzi in eukaryotic cells

Extracellular vesicles released from pathogens may alter host cell functions. We previously demonstrated the involvement of host cell‐derived microvesicles (MVs) during early interaction between Trypanosoma cruzi metacyclic trypomastigote (META) stage and THP‐1 cells. Here, we aim to understand the contribution of different parasite stages and their extracellular vesicles in the interaction with host cells. First, we observed that infective host cell‐derived trypomastigote (tissue culture‐derived trypomastigote [TCT]), META, and noninfective epimastigote (EPI) stages were able to induce different levels of MV release from THP‐1 cells; however, only META and TCT could increase host cell invasion. Fluorescence resonance energy transfer microscopy revealed that THP‐1‐derived MVs can fuse with parasite‐derived MVs. Furthermore, MVs derived from the TCT–THP‐1 interaction showed a higher fusogenic capacity than those from META– or EPI–THP‐1 interaction. However, a higher presence of proteins from META (25%) than TCT (12%) or EPI (5%) was observed in MVs from parasite–THP‐1 interaction, as determined by proteomics. Finally, sera from patients with chronic Chagas disease at the indeterminate or cardiac phase differentially recognized antigens in THP‐1‐derived MVs resulting only from interaction with infective stages. The understanding of intracellular trafficking and the effect of MVs modulating the immune system may provide important clues about Chagas disease pathophysiology.     

Host‐associated genetic divergence and taxonomy in the Rhinusa pilosa Gyllenhal species complex: an integrative approach

A combined taxonomic, morphological, molecular and biological study revealed that stem‐galling weevils from the genus Rhinusa associated with toadflaxes from the genus Linaria (Plantaginaceae) are composed of three different species: Rhinusa pilosa, Rhinusa brondelii and Rhinusa rara sp.n. The authentic field host plants are respectively, Linaria vulgaris, Linaria purpurea and Linaria genistifolia/ Linaria dalmatica. These weevil species can be distinguished from each other by a few subtle morphological characteristics, mainly in the shape of the rostrum and of the integument. An analysis of the mitochondrial [cytochrome oxidase subunit II gene (COII) and 16S ribosomal RNA gene (16S)] and nuclear (elongation factor‐1α, EF‐1α) sequence data revealed high genetic divergence among these species. Uncorrected pairwise distances on mtCOII gene were 14.3% between R. pilosa and R. brondelii, 15.7% between R. pilosa and R. rara, while R. brondelii and R. rara were approximately 11% divergent from each other. Divergences obtained on 16S and nuclear EF‐1α genes were congruent. However, substantial intraspecific mitochondrial divergence was recorded for all studied populations of R. pilosa s.s. showing two mtDNA lineages, with estimated COII and 16S divergences of 4% and 1.6%, respectively. Nuclear pseudogenes (Numts) and Wolbachia influence, although recorded within both lineages, were excluded as possible causatives of the mtDNA divergence, while EF‐1α indicated absence of lineage sorting. Species from the R. pilosa complex are estimated to have diverged from each other approximately 7.2 million years ago (mya; late Miocene), while R. brondelii and R. rara diverged from each other about 4.7 mya (early Pliocene). This published work has been registered in ZooBank, http://zoobank.org/urn:lsid:zoobank.org:pub:EEDD6248‐01DB‐4B4A‐B79D‐C5606393E3AA .