The parasite's long arm: a tapeworm parasite induces behavioural changes in uninfected group members of its social host

Parasites can induce alterations in host phenotypes in order to enhance their own survival and transmission. Parasites of social insects might not only benefit from altering their individual hosts, but also from inducing changes in uninfected group members. Temnothorax nylanderi ant workers infected with the tapeworm Anomotaenia brevis are known to be chemically distinct from nest-mates and do not contribute to colony fitness, but are tolerated in their colonies and well cared for. Here, we investigated how tapeworm- infected workers affect colony aggression by manipulating their presence in ant colonies and analysing whether their absence or presence resulted in behavioural alterations in their nest-mates. We report a parasite-induced shift in colony aggression, shown by lower aggression of uninfected nest-mates from parasitized colonies towards conspecifics, potentially explaining the tolerance towards infected ants. We also demonstrate that tapeworm-infected workers showed a reduced flight response and higher survival, while their presence caused a decrease in survival of uninfected nest-mates. This anomalous behaviour of infected ants, coupled with their increased survival, could facilitate the parasites'' transmission to its definitive hosts, woodpeckers. We conclude that parasites exploiting individuals that are part of a society not only induce phenotypic changes within their individual hosts, but in uninfected group members as well.     

Wolbachia-induced unidirectional cytoplasmic incompatibility and the stability of infection polymorphism in parapatric host populations

Wolbachia are intracellular, maternally inherited bacteria that are widespread among arthropods and commonly induce a reproductive incompatibility between infected male and uninfected female hosts known as unidirectional cytoplasmic incompatibility (CI). If infected and uninfected populations occur parapatrically, CI acts as a post-zygotic isolation barrier. We investigate the stability of such infection polymorphisms in a mathematical model with two populations linked by migration. We determine critical migration rates below which infected and uninfected populations can coexist. Analytical solutions of the critical migration rate are presented for mainland-island models. These serve as lower estimations for a more general model with two-way migration. The critical migration rate is positive if either Wolbachia causes a fecundity reduction in infected female hosts or its transmission is incomplete, and is highest for intermediate levels of CI. We discuss our results with respect to local adaptations of the Wolbachia host, speciation, and pest control.     

Maternal antibodies contribute to sex-based difference in hantavirus transmission dynamics

Individuals often differ in their ability to transmit disease and identifying key individuals for transmission is a major issue in epidemiology. Male hosts are often thought to be more important than females for parasite transmission and persistence. However, the role of infectious females, particularly the transient immunity provided to offspring through maternal antibodies (MatAbs), has been neglected in discussions about sex-biased infection transmission. We examined the effect of host sex upon infection dynamics of zoonotic Puumala hantavirus (PUUV) in semi-natural, experimental populations of bank vole (Myodes glareolus). Populations were founded with either females or males that were infected with PUUV, whereas the other sex was immunized against PUUV infection. The likelihood of the next generation being infected was lower when the infected founders were females, underlying the putative importance of adult males in PUUV transmission and persistence in host populations. However, we show that this effect probably results from transient immunity that infected females provide to their offspring, rather than any sex-biased transmission efficiency per se. Our study proposes a potential contrasting nature of female and male hosts in the transmission dynamics of hantaviruses.     

An empirical model of the optimal timing of reproduction for female amphipods infected by trematodes

Life-history theory predicts that hosts should reproduce when first infected by parasites if hosts are capable and if parasites have a lower cost on current than on future reproduction of hosts. We constructed an empirical model to explore fitness of females of the intertidal amphipod Corophium volutator that reproduced soon versus long after infection by the trematode Gynaecotyla adunca. For uninfected females, the optimal time to reproduce was at their maximum body length. However, for females infected by low or high intensities of trematode metacercariae, reproductive potential (realized fecundity) was highest for females that mated immediately after becoming infected. Even after removing a high cost of delaying reproduction for infected amphipods (high likelihood of depredation by sandpipers, which are final hosts of G. adunca), realized fecundity remained highest if reproduction occurred immediately following infection by trematodes. Results from our model support the view that early reproduction of female amphipods following infection by G. adunca is an adaptive life-history response to parasitism.     

TRADEOFF BETWEEN HORIZONTAL AND VERTICAL MODES OF TRANSMISSION IN BACTERIAL PLASMIDS

It has been hypothesized that there is a fundamental conflict between horizontal (infectious) and vertical (intergenerational) modes of parasite transmission. Activities of a parasite that increase its rate of infectious transmission are presumed to reduce its host's fitness. This reduction in host fitness impedes vertical transmission of the parasite and causes a tradeoff between horizontal and vertical transmission. Given this tradeoff, and assuming no multiple infections (no within-host competition among parasites), a simple model predicts that the density of uninfected hosts in the environment should determine the optimum balance between modes of parasite transmission. When susceptible hosts are abundant, selection should favor increased rates of horizontal transfer, even at the expense of reduced vertical transmission. Conversely, when hosts are rare, selection should favor increased vertical transmission even at the expense of lower horizontal transfer. We tested the tradeoff hypothesis and these evolutionary predictions using conjugative plasmids and the bacteria that they infect. Plasmids were allowed to evolve for 500 generations in environments with different densities of susceptible hosts. The plasmid's rate of horizontal transfer by conjugation increased at the expense of host fitness, indicating a tradeoff between horizontal and vertical transmission. Also, reductions in conjugation rate repeatedly coincided with the loss of a particular plasmid-encoded antibiotic resistance gene. However, susceptible host density had no significant effect on the evolution of horizontal versus vertical modes of plasmid transmission. We consider several possible explanations for the failure to observe such an effect.     

Trypanosoma cruzi-infected Rhodnius prolixus endure increased predation facilitating parasite transmission to mammal hosts

Triatomine bugs aggregate with conspecifics inside shelters during daylight hours. At dusk, they leave their refuges searching for hosts on which to blood feed. After finding a host, triatomines face the threat of being killed, because hosts often prey on them. As it is known that many parasites induce the predation of intermediate hosts to promote transmission, and that ingestion of Trypanosoma cruzi-infected bugs represents a very effective means for mammal infection, we hypothesized that trypanosomes induce infected bugs to take increased risk, and, as a consequence, be predated when approaching a host. Therefore, we evaluated whether the predation risk and predation rates endured by Rhodnius prolixus increase when infected with T. cruzi. Assays were performed in square glass arenas offering one central refuge to infected and uninfected 5^th instar nymphs. A caged mouse was introduced in each arena after a three-day acclimation interval to activate sheltered insects and induce them to approach it. As hypothesized, a significantly higher proportion of infected insects was predated when compared with uninfected ones (36% and 19%, respectively). Indeed, T. cruzi-infected bugs took higher risk (Approximation Index = 0.642) when compared with healthy ones (Approximation Index = 0.302) and remained outside the shelters when the host was removed from the arena. Our results show that infection by T. cruzi induces bugs to assume higher risk and endure higher predation rates. We reveal a hitherto unknown trypanosome-vector interaction process that increases infected bug predation, promoting increased rates of robust oral transmission. The significant consequences of the mechanism revealed here make it a fundamental component for the resilient maintenance of sylvatic, peridomestic and domestic cycles.     

Altered predation susceptibility of mosquitofish infected with Eustrongylides ignotus

Eustrongylides ignotus is a parasitic nematode whose definitive hosts are often piscivorous wading birds (Ciconiiformes). Several species of small fishes are intermediate hosts, while larger predatory fish may be paratenic (transport) hosts. We examined predation susceptibility of infected mosquitofish (Gambusia holbrooki) to three species of predatory fishes, including juvenile largemouth bass (Micropterus salminoides), warmouth (Lepomis gulosus), and bluegill (Lepomis macrochirus). A 250 L aquarium with removable plexiglass divider and remote observation windows was constructed. Aquatic macrophytes were placed in the tank to provide refuge for the fishes. Predatory fish were allowed to acclimate to one half of the tank, while one infected and one uninfected mosquitofish were placed in the other. The divider was removed and an observer recorded the number of capture attempts and time required for capture. Predators were observed for behavioral alterations for 4 days after ingestion of infected mosquitofish, then examined at necropsy. Infected prey were selected preferentially in 31 of 38 (82%) trials. The number of capture attempts was 2.7+/-0.2 (x +/- SE) for infected fish and 3.9+/-0.4 for uninfected fish. Mean time of capture was 12.4+/-1.6 min for infected fish and 21.7+/-2.9 for uninfected fish. Because of these differences, infected mosquitofish were more susceptible to predation (P < 0.01) than uninfected fish. Aberrant behavior including lethargy, convulsions, and buoyancy abnormalities was observed in eight (67%) predatory fish. At necropsy, larvae of E. ignotus were found in the coelomic cavity, viscera, and swim bladders of predators. Parasite-induced behavior modification of intermediate hosts may predispose them to predation by wading birds and thereby facilitate the transmission of this nematode in natural populations.     

Non-Specific Manipulation of Gammarid Behaviour by P. minutus Parasite Enhances Their Predation by Definitive Bird Hosts

Trophically-transmitted parasites often change the phenotype of their intermediate hosts in ways that increase their vulnerability to definitive hosts, hence favouring transmission. As a “collateral damage”, manipulated hosts can also become easy prey for non-host predators that are dead ends for the parasite, and which are supposed to play no role in transmission strategies. Interestingly, infection with the acanthocephalan parasite Polymorphus minutus has been shown to reduce the vulnerability of its gammarid intermediate hosts to non-host predators, whose presence triggered the behavioural alterations expected to favour trophic transmission to bird definitive hosts. Whilst the behavioural response of infected gammarids to the presence of definitive hosts remains to be investigated, this suggests that trophic transmission might be promoted by non-host predation risk. We conducted microcosm experiments to test whether the behaviour of P. minutus-infected gammarids was specific to the type of predator (i.e. mallard as definitive host and fish as non-host), and mesocosm experiments to test whether trophic transmission to bird hosts was influenced by non-host predation risk. Based on the behaviours we investigated (predator avoidance, activity, geotaxis, conspecific attraction), we found no evidence for a specific fine-tuned response in infected gammarids, which behaved similarly whatever the type of predator (mallard or fish). During predation tests, fish predation risk did not influence the differential predation of mallards that over-consumed infected gammarids compared to uninfected individuals. Overall, our results bring support for a less sophisticated scenario of manipulation than previously expected, combining chronic behavioural alterations with phasic behavioural alterations triggered by the chemical and physical cues coming from any type of predator. Given the wide dispersal range of waterbirds (the definitive hosts of P. minutus), such a manipulation whose efficiency does not depend on the biotic context is likely to facilitate its trophic transmission in a wide range of aquatic environments.     

Effects of ultraviolet radiation on the transmission process of an intertidal trematode parasite

The transmission of parasites takes place under exposure to a range of fluctuating environmental factors, one being the changing levels of solar ultraviolet radiation (UVR). Here, we investigated the effects of ecologically relevant levels of UVR on the transmission of the intertidal trematode Maritrema novaezealandensis from its first intermediate snail host (Zeacumantus subcarinatus) to its second intermediate amphipod host (Paracalliope novizealandiae). We assessed the output of parasite transmission stages (cercariae) from infected snail hosts, the survival and infectivity of cercariae, the susceptibility of amphipod hosts to infection (laboratory experiments) and the survival of infected and uninfected amphipod hosts (outdoor experiment) when exposed to photo-synthetically active radiation only (PAR, 400-700 nm; no UV), PAR+UVA (320-700 nm) or PAR+UVA+UVB (280-700 nm). Survival of cercariae and susceptibility of amphipods to infection were the only two steps significantly affected by UVR. Survival of cercariae decreased strongly in a dose-dependent manner, while susceptibility of amphipods increased after exposure to UVR for a prolonged period. Exposure to UVR thus negatively affects both the parasite and its amphipod host, and should therefore be considered an influential component in parasite transmission and host-parasite interactions in intertidal ecosystems.     

The malaria parasite,Plasmodium falciparum,increases the frequency of multiple feeding of its mosquito vector,Anopheles gambiae.

It has often been suggested that vector-borne parasites alter their vector''s feeding behaviour to increase their transmission, but these claims are often based on laboratory studies and lack rigorous testing in a natural situation. We show in this field study that the malaria parasite, Plasmodium falciparum, alters the blood-feeding behaviour of its mosquito vector, Anopheles gambiae s.l., in two ways. First, mosquitoes infected with sporozoited, the parasite stage that is transmitted from the mosquito to a human, took up larger blood meals than uninfected mosquitoes. Whereas 72% of the uninfected mosquitoes had obtained a full blood meal, 82% of the infected ones had engorged fully. Second, mosquitoes harbouring sporozoites were more likely to bite several people per night. Twenty-two per cent of the infected mosquitoes, but only 10% of the uninfected mosquitoes, contained blood from at least two people. We conclude that the observed changes in blood-feeding behaviour allow the parasite to spread more rapidly among human hosts, and thus confirm that the parasite manipulates the mosquito to increase its own transmission.     

The effects of Trichinella spiralis infection on social interactions in mixed groups of infected and uninfected male mice

The presence of Trichinella spiralis infection in groups of male mice caused behavioural changes in both infected and uninfected mice. Also, for some behaviours, the extent of behavioural change in infected mice appeared to be determined by the number of muscle larvae they harboured. Infected mice showed a reduced frequency of exploratory and social behaviours compared with uninfected mice while uninfected mice performed more social investigatory activities towards those that were infected. Social interactions between infected and uninfected mice were also affected by familiarity. Behavioural differences shown to result from infection in mice familiar with each other were similar but more pronounced when the mice were unfamiliar. These results suggest that other factors may influence the behavioural effects of parasites on their hosts. For some behaviours, the greatest alterations in behaviour apparently caused by infection coincided with the period of infectivity to another host. The significance of this in relation to parasite transmission is considered.     

Competitive advantages of Caedibacter-infected Paramecia

Intracellular bacteria of the genus Caedibacter limit the reproduction of their host, the freshwater ciliate Paramecium. Reproduction rates of infected strains of paramecia were significantly lower than those of genetically identical strains that had lost their parasites after treatment with an antibiotic. Interference competition occurs when infected paramecia release a toxic form of the parasitic bacterium that kills uninfected paramecia. In mixed cultures of infected and uninfected strains of either P tetraurelia or of P novaurelia, the infected strains outcompeted the uninfected strains. Infection of new host paramecia seems to be rare. Infection of new hosts was not observed in either mixtures of infected with uninfected strains, or after incubation of paramecia with isolated parasites. The competitive advantages of the host paramecia, in combination with their vegetative reproduction, makes infection of new hosts by the bacterial parasites unnecessary, and could be responsible for the continued existence of "killer paramecia" in nature. Caedibacter parasites are not a defensive adaptation. Feeding rates and reproduction of the predators Didinium nasutum (Ciliophora) and Amoeba proteus (Amoebozoa, Gymnamoebia) were not influenced by whether or not their paramecia prey were infected. Infection of the predators frequently occurred when they preyed on infected paramecia. Caedibacter-infected predators may influence competition between Paramecium strains by release of toxic parasites into the environment that are harmful to uninfected strains.     

Avian malaria infection intensity influences mosquito feeding patterns

Pathogen-induced host phenotypic changes are widespread phenomena that can dramatically influence host–vector interactions. Enhanced vector attraction to infected hosts has been reported in a variety of host–pathogen systems, and has given rise to the parasite manipulation hypothesis whereby pathogens may adaptively modify host phenotypes to increase transmission from host to host. However, host phenotypic changes do not always favour the transmission of pathogens, as random host choice, reduced host attractiveness and even host avoidance after infection have also been reported. Thus, the effects of hosts’ parasitic infections on vector feeding behaviour and on the likelihood of parasite transmission remain unclear. Here, we experimentally tested how host infection status and infection intensity with avian Plasmodium affect mosquito feeding patterns in house sparrows (Passer domesticus). In separate experiments, mosquitoes were allowed to bite pairs containing (i) one infected and one uninfected bird and (ii) two infected birds, one of which treated with the antimalarial drug, primaquine. We found that mosquitoes fed randomly when exposed to both infected and uninfected birds. However, when mosquitoes were exposed only to infected individuals, they preferred to bite the non-treated birds. These results suggest that the malarial parasite load rather than the infection itself plays a key role in mosquito attraction. Our findings partially support the parasite manipulation hypothesis, which probably operates via a reduction in defensive behaviour, and highlights the importance of considering parasite load in studies on host–vector–pathogen interactions.     

Male-biased sex-ratio distortion caused by Octosporea bayeri, a vertically and horizontally-transmitted parasite of Daphnia magna

Female-biased sex-ratio distortion is often observed in hosts infected with vertically-transmitted microsporidian parasites. This bias is assumed to benefit the spread of the parasite, because male offspring usually do not transmit the parasite further. The present study reports on sex-ratio distortion in a host-parasite system with both horizontal and vertical parasite transmission: the microsporidium Octosporea bayeri and its host, the planktonic cladoceran Daphnia magna. In laboratory and field experiments, we found an overall higher proportion of male offspring in infected than in uninfected hosts. In young males, there was no parasite effect on sperm production, but, later in life, infected males produced significantly less sperm than uninfected controls. This shows that infected males are fertile. As males are unlikely to transmit the parasite vertically, an increase in male production could be advantageous to the host during phases of sexual reproduction, because infected mothers may obtain uninfected grandchildren through their sons. Life-table experiments showed that, overall, sons harboured more parasite spores than their sisters, although they reached a smaller body size and died earlier. Male production may thus be beneficial for the parasite when horizontal transmission has a large pay-off as males may contribute more effectively to parasite spread than females.     

Acephaline gregarine parasites (Monocystis sp.) are not transmitted sexually among their lumbricid earthworm hosts

The precise transmission mode(s) of acephaline gregarines in their earthworm hosts has long been questioned, yet a rigorous experimental evaluation of sexual transmission is currently lacking. That Monocystis sp., a common gregarine parasite of the earthworm Lumbricus terrestris, infects the sexual organs of its host is suggestive of sexual transmission. Considering the divergent evolutionary consequences of various modes of transmission, excluding or proving sexual transmission in this host-parasite system is critical to fully understanding it. We cultured uninfected earthworms from cocoons and subsequently mated them to either an infected or uninfected partner (from the wild). We then compared these individuals with an orally infected group, which were infected using a newly developed gavage (oral injection) method. Our data have unambiguously established that (1) horizontal sexual transmission does not play a significant role in the transmission of Monocystis sp., and (2) oral transmission through the soil is likely the principal mode of transmission between earthworms. This finding is important to models of mate-choice because infection avoidance does not appear to drive mating decisions. Finally, we further report a successful and relatively simple method to obtain infection-free individuals, which can subsequently be infected via oral gavage and used in empirical studies.     

Modeling the Potential Impact of Host Population Survival on the Evolution of M. tuberculosis Latency

Tuberculosis (TB) is an infectious disease with a peculiar feature: Upon infection with the causative agent, Mycobacterium Tuberculosis (MTB), most hosts enter a latent state during which no transmission of MTB to new hosts occurs. Only a fraction of latently infected hosts develop TB disease and can potentially infect new hosts. At first glance, this seems like a waste of transmission potential and therefore an evolutionary suboptimal strategy for MTB. It might be that the human immune response keeps MTB in check in most hosts, thereby preventing it from achieving its evolutionary optimum. Another possible explanation is that long latency and progression to disease in only a fraction of hosts are evolutionary beneficial to MTB by allowing it to persist better in small host populations. Given that MTB has co-evolved with human hosts for millenia or longer, it likely encountered small host populations for a large share of its evolutionary history and had to evolve strategies of persistence. Here, we use a mathematical model to show that indeed, MTB persistence is optimal for an intermediate duration of latency and level of activation. The predicted optimal level of activation is above the observed value, suggesting that human co-evolution has lead to host immunity, which keeps MTB below its evolutionary optimum.     

The transmission and effects of Wolbachia bacteria in parasitoids

Wolbachia bacteria are obligatory intracellular parasites of arthropods and have been detected in about 70 species of parasitic wasps and three parasitoid flies. Wolbachia are transmitted cytoplasmically (maternally) and modify host reproduction in different ways to enhance their own transmission: parthenogenesis induction (PI), cytoplasmic incompatibility (CI), or feminization (F) of genetic males. Only PI and CI are known in parasitoids. PI-Wolbachia cause thelytoky in otherwise arrhenotokous parasitoids by generating diploid (rather than haploid) unfertilized wasp eggs. CI-Wolbachia cause incompatibility of crosses between infected males and uninfected females because the paternally derived chromosomes fail to decondense and are destroyed after syngamy. More complex situations arise when hosts harbor multiple infections, which can lead to bidirectional incompatibility and may be involved in parasitoid speciation. The relative fitness of infected and uninfected hosts is important to the population dynamics of Wolbachia, and more data are needed. Evolutionary conflict should be common between host genes, Wolbachia genes, and other "selfish" genetic elements. Wolbachia-specific PCR primers are now available for several genes with different rates of evolution. These primers will permit rapid screening in future studies of spatial and temporal patterns of single and multiple infection. Molecular phylogenies show that CI- and PI-Wolbachia do not form discrete clades. In combination with experimental transfection data, this result suggests that host reproductive alterations depend on the interaction between attributes of both Wolbachia and host. Moreover, Wolbachia isolates from closely related hosts do not usually cluster together, and phylogenies suggest that Wolbachia may have radiated after their arthropod hosts. Both results support considerable horizontal transmission of Wolbachia between host species over evolutionary time. Natural horizontal transmisson between parasitoids and their hosts, or with entomoparasitic nematodes or ectoparasitic mites, remains a tantalizing but equivocal possibility. Received: November 27, 1998 / Accepted: January 15, 1999     

Hantavirus Transmission in Sylvan and Peridomestic Environments

We developed a compartmental model for hantavirus infection in deer mice (Peromyscus maniculatus) with the goal of comparing relative importance of direct and indirect transmission in sylvan and peridomestic environments. A direct transmission occurs when the infection is mediated by the contact of an infected and an uninfected mouse, while an indirect transmission occurs when the infection is mediated by the contact of an uninfected mouse with, for instance, infected soil. Based on population dynamics data and estimates of hantavirus decay in the two types of environments, our model predicts that direct transmission dominates in the sylvan environment, while both pathways are important in peridomestic environments. The model allows us to compute a basic reproduction number R ₀, which indicates whether the virus will be endemic or eradicated from the mouse population, in both an autonomous and a time-periodic model. Our analysis can be used to evaluate various eradication strategies.     

Host life span and the evolution of resistance characteristics

There is a wide variety of resistance mechanisms that hosts may evolve in response to their parasites. These can be functionally classified as avoidance (lower probability of becoming infected), recovery (faster rate of clearance), tolerance (reduced death rate when infected), or acquired immunity. It is commonly thought that longer lived organisms should invest more in costly resistance. We show that due to epidemiological feedbacks the situation is often more complex. Using evolutionary theory we examine how the optimal investment in costly resistance varies with life span in a broad range of scenarios. In the absence of acquired immunity, longer lived populations do generally invest more in resistance. If hosts have acquired immunity, the optimal resistance may either increase or decrease with increasing life span. In addition, there may be evolutionary bistability with high and low investments in avoidance or tolerance. The optimal investment in the duration of acquired immunity always increases with life span, and due to bistability, shorter lived hosts may commonly not evolve any immunity. In contrast, the optimal investment in the probability of acquiring immunity initially increases and then decreases with life span. Our results have important implications for the evolution of invertebrate and vertebrate immunity, and for the evolution of acquired immunity itself.     

The Intracellular Bacterium Wolbachia Uses Parasitoid Wasps as Phoretic Vectors for Efficient Horizontal Transmission

Facultative bacterial endosymbionts are associated with many arthropods and are primarily transmitted vertically from mother to offspring. However, phylogenetic affiliations suggest that horizontal transmission must also occur. Such horizontal transfer can have important biological and agricultural consequences when endosymbionts increase host fitness. So far horizontal transmission is considered rare and has been difficult to document. Here, we use fluorescence in situ hybridization (FISH) and multi locus sequence typing (MLST) to reveal a potentially common pathway of horizontal transmission of endosymbionts via parasitoids of insects. We illustrate that the mouthparts and ovipositors of an aphelinid parasitoid become contaminated with Wolbachia when this wasp feeds on or probes Wolbachia-infected Bemisia tabaci AsiaII7, and non-lethal probing of uninfected B. tabaci AsiaII7 nymphs by parasitoids carrying Wolbachia resulted in newly and stably infected B. tabaci matrilines. After they were exposed to infected whitefly, the parasitoids were able to transmit Wolbachia efficiently for the following 48 h. Whitefly infected with Wolbachia by parasitoids had increased survival and reduced development times. Overall, our study provides evidence for the horizontal transmission of Wolbachia between insect hosts by parasitic wasps, and the enhanced survival and reproductive abilities of insect hosts may adversely affect biological control programs.