Parasite establishment and host extinction in model communities

Studies of host–parasite dynamics usually consider one, or at most two, host species, neglecting the possible effects of other species on the focal hosts and vice versa. To explore the interaction of community structure with host–parasite dynamics, we model the invasion of stable communities of varying size by a parasite. The communities are generated with random interaction coefficients and connectance 0.5. Each community is invaded by parasites with different values of virulence (disease-induced host mortality rate), specificity and transmission rate. The result of each invasion is determined by numerically simulating the dynamics of the community. We classify the outcomes by whether the parasite successfully establishes in the focal host population(s), and, if so, by the proportion of host and non-host species that go extinct as a result of the parasite's introduction. We discuss how the structure of the community and the interaction between hosts and other species affect several important processes of disease ecology: the density threshold for parasite invasion, extinction cascades caused by the parasite, and the frequency of extinctions of hosts and non-hosts. In our simulated communities, non-host species went extinct more frequently than hosts, suggesting the importance of the community context of disease. In some cases, the parasite's invasion induced regular population cycles in the previously stable community.     

Differential virulence in a multiple‐host parasite of bumble bees: resolving the paradox of parasite survival?

Parasite virulence determines both the impact that parasites have on their hosts and parasite fitness. While most studies of virulence have involved single-species host–parasite interactions, the majority of parasites are likely to use multiple concurrent host species. Our understanding of how this impacts on parasite epidemiology and virulence is limited. Using the bumble bee Bombus lucorum , which exists in sympatry with B. terrestris in multi-species assemblages, and their generalist micosporidian parasite Nosema bombi , we tested whether the apparent paradox of parasite maintenance due to parasite virulence in a single host, B. terrestris , could be resolved through understanding the parasite's virulence in this sympatric host species. Nosema bombi significantly impacted colony growth, individual longevity, and individual development in B. lucorum . However, these effects were different both qualitatively and quantitatively to the parasite's impact in B. terrestris . Infected colonies of B. lucorum successfully produced both male and female reproductives, and infected female reproductives were capable of successful mating. Variation in life-history across host species may explain differences in the virulence, or impact of the parasite in B. terrestris and B. lucorum , with species with shorter life-cycles being more likely to transfer the parasite from one annual generation to the next. These results suggest that to understand the virulence and epidemiology of multi-host parasites we need to examine their ecological interactions across their various host species.     

Relatedness and spatial proximity as determinants of host–parasite interactions in the brood parasitic Barrow's goldeneye (Bucephala islandica)

Recent studies, which have found evidence for kin-biased egg donation, have sparked interest in re-assessing the parasitic nature of conspecific brood parasitism (CBP). Since host–parasite kinship is essential for mutual benefits to arise from CBP, we explored the role of relatedness in determining the behaviour of conspecific nest parasites and their hosts in nesting female Barrow's goldeneyes ( Bucephala islandica ), a duck in which CBP is common. The results revealed that the amount of parasitism increased with host–parasite relatedness, the effect of which was independent of geographical proximity of host and parasite nests. Proximity per se was also positively associated with the amount of parasitism. Furthermore, while hosts appeared to reduce their clutch size as a response to the presence of parasitic eggs, the magnitude of host clutch reduction also tended to increase with increasing relatedness to the parasite. Hence, our results indicate that both relatedness and spatial proximity are important determinants of CBP, and that host clutch reduction may be an adaptation to nest parasitism, modulated by host–parasite relatedness. Taken together, the results provide a demonstration that relatedness influences host and parasite behaviour in Barrow's goldeneyes, resulting in kin-biased egg donation.     

Variation in intensity of a parasitic mite (Spinturnix myoti) in relation to the reproductive cycle and immunocompetence of its bat host (Myotis myotis)

Given the intimate association in host–parasite systems, parasites are expected to initiate their own reproduction when vulnerable hosts become abundant and/or when adult hosts are less resistant. In this study, we examined the variation in the intensities of a blood-sucking mite ( Spinturnix myoti , Acarina) with respect to the reproductive cycle and immunocompetence of its host, the greater mouse-eared bat Myotis myotis . Reproductive, pregnant females were less immunocompetent and harboured more parasites than nonreproductive females, whilst, during lactation, immunocompetence was positively associated with female body mass. There was a dramatic increase in the T-cell response of gravid females with the advancement of gestation, which coincided with a diminution of individual parasite loads and a progressive switch of parasites from adults to juveniles. The latter not only harboured greater numbers of mites than adult female bats, but they also exhibited gravid parasites in higher proportions, indicating that juvenile hosts are more attractive for parasite reproduction than adult females.     

Evolution of tolerance: the genetic basis of a host's resistance against parasite manipulation

Despite considerable theoretical advances in the evolutionary biology of host–parasite systems, our knowledge of host–parasite coevolution in natural systems is often limited. Among the reasons for the lag of experimental insight behind theory is that the parasite's virulence is not a simple trait that is controlled by the parasite's genes. Rather, virulence can be expressed in several traits due to the subtle interactions between the host and the parasite. Furthermore, the host might evolve tolerance to the parasite if there is sufficient genetic variance to reduce the detrimental effect of the parasite on these traits. We studied the traits underlying virulence and the genetic potential to evolve tolerance to infection in the host–parasite system Aedes aegypti – Brachiola algerae . We reared the mosquitoes in a half-sib design, exposed half of the individuals in each full-sib family to the parasite and measured several life history traits – juvenile mortality, age at pupation and adult size – of infected and uninfected individuals. Virulence was due in large part to a delay of the mosquito's age at pupation by about 10%. Although this imposes strong selection pressure on the mosquito to resist the parasite, all of the mosquitoes were infected, implying a lack of resistance. Furthermore, although additive genetic variance was present for other traits, we found no indication of additive genetic variation for the age at pupation, nor for the delay of pupation due to infection, implying no potential for the evolution of tolerance. Overall, the results suggest that in this host–parasite system, the host has little evolutionary control over the expression of the parasite's virulence.     

Host specificity in spinturnicid mites: do parasites share a long evolutionary history with their host?

Host specificity in parasites can be explained by spatial isolation from other potential hosts or by specialization and speciation of specific parasite species. The first assertion is based on allopatric speciation, the latter on differential lifetime reproductive success on different available hosts. We investigated the host specificity and cophylogenetic histories of four sympatric European bat species of the genus Myotis and their ectoparasitic wing mites of the genus Spinturnix. We sampled >40 parasite specimens from each bat species and reconstructed their phylogenetic COI trees to assess host specificity. To test for cospeciation, we compared host and parasite trees for congruencies in tree topologies. Corresponding divergence events in host and parasite trees were dated using the molecular clock approach. We found two species of wing mites to be host specific and one species to occur on two unrelated hosts. Host specificity cannot be explained by isolation of host species, because we found individual parasites on other species than their native hosts. Furthermore, we found no evidence for cospeciation, but for one host switch and one sorting event. Host‐specific wing mites were several million years younger than their hosts. Speciation of hosts did not cause speciation in their respective parasites, but we found that diversification of recent host lineages coincided with a lineage split in some parasites.     

Interactions between the parasite's previous and current environment mediate the outcome of parasite infection

The study of parasite virulence has generally focused on the conditions under which virulence is expected to increase or decrease over time and how the interactions between hosts and their environments may mediate the outcome of infection. Recently, parasite traits such as transmission, offspring production, and development have also been shown to be influenced by environmental variation. What is unclear is how variation in the parasite's environment may impact virulence. Recent theory demonstrates that plasticity can promote the evolution of decreased virulence; thus, understanding whether the parasite's environment can mediate virulence can improve predictions regarding the outcome of parasite infection. Here, an obligate mosquito parasite was reared in hosts fed high or low levels of food. Parasite oocysts (offspring) produced in these two host environments were subsequently fed to uninfected hosts. Parasites originating from well-fed hosts were found to be more virulent to these subsequent hosts compared to parasites originating from poorly fed hosts. Additionally, this effect was apparent only when current hosts were food deprived. These results demonstrate that parasite virulence was mediated by a cross-generational effect of the environment and that the overall outcome of infection was modified by variation in both the parasite's and host's environments.     

Codivergence in heteromyid rodents (Rodentia: heteromyidae) and their sucking lice of the genus Fahrenholzia (Phthiraptera: anoplura)

Although most studies of codivergence rely primarily on topological comparisons of host and parasite phylogenies, temporal assessments are necessary to determine if divergence events in host and parasite trees occurred contemporaneously. A combination of cophylogenetic analyses and comparisons of branch lengths are used in this study to understand the host-parasite association between heteromyid rodents (Rodentia: Heteromyidae) and their sucking lice of the genus Fahrenholzia (Phthiraptera: Anoplura). Cophylogenetic comparisons based on nucleotide substitutions in the mitochondrial COI gene reveal a significant, but not perfect, pattern of cophylogeny between heteromyids and their sucking lice. Regression analyses show a significant functional relationship between the lengths of analogous branches in the host and parasite trees, indicating that divergence events in hosts and parasites were approximately contemporaneous. Thus, the topological similarity observed between heteromyids and their lice is the result of codivergence. These analyses also show that the COI gene in lice is evolving two to three times faster than the same gene in their hosts (similar to the results of studies of other lice and their vertebrate hosts) and that divergence events in lice occurred shortly after host divergence. We recommend that future studies of codivergence include temporal comparisons and, when possible, use the same molecular marker(s) in hosts and parasites to achieve the greatest insight into the history of the host-parasite relationship.     

A macroevolutionary mosaic: episodic host-switching, geographical colonization and diversification in complex host–parasite systems

Aim  To integrate ecological fitting, the oscillation hypothesis and the taxon pulse hypothesis into a coherent null model for the evolution of complex host–parasite associations.
Location  Global.
Methods  This paper reviews and synthesizes literature that focuses on phylogenetic analyses and reciprocal mapping of a model system of hosts and their parasites to determine patterns of host–parasite associations and geographical distributions through time.
Results  Host-switching and geographical dispersal of parasites are common phenomena, occurring on many temporal and spatial scales. Diversification involving both co-evolution and colonization explains complex host–parasite associations. Across the expanse of Earth history, the major radiations in host–parasite assemblages have been preceded by ecological disruption, ecological breakdown and host-switching in a context that can be defined by the concept of ecological fitting. This cyclical process sets the stage for co-diversification during periods of relative stability, punctuated by host-switching during episodes of regional to global environmental disruption and climatological change.
Main conclusions  Most observed host–parasite associations can be explained by an historical interaction between ecological fitting, oscillation (episodes of increasing host range alternating with isolation on particular hosts) and taxon pulses (cyclical episodes of expansion and isolation in geographical range). Major episodes of environmental change appear to be the main drivers for both the persistence and diversification of host–parasite systems, creating opportunities for host-switching during periods of geographical expansion and allowing for co-evolution and co-speciation during periods of geographical isolation.     

Infection success in novel hosts: an experimental and phylogenetic study of Drosophila-parasitic nematodes

Surprisingly little is known about what determines a parasite's host range, which is essential in enabling us to predict the fate of novel infections. In this study, we evaluate the importance of both host and parasite phylogeny in determining the ability of parasites to infect novel host species. Using experimental lab assays, we infected 24 taxonomically diverse species of Drosophila flies (Diptera: Drosophilidae) with five different nematode species (Tylenchida: Allantonematidae: Howardula, Parasitylenchus), and measured parasite infection success, growth, and effects on female host fecundity (i.e., virulence). These nematodes are obligate parasites of mushroom-feeding Drosophila, particularly quinaria and testacca group species, often with severe fitness consequences on their hosts. We show that the potential host ranges of the nematodes are much larger than their actual ranges, even for parasites with only one known host species in nature. Novel hosts that are distantly related from the native host are much less likely to be infected, but among more closely related hosts, there is much variation in susceptibility. Potential host ranges differ greatly between the related parasite species. All nematode species that successfully infected novel hosts produced infective juveniles in these hosts. Most novel infections did not result in significant reductions in the fecundity of female hosts, with one exception: the host specialist Parasitylenchus nearcticus sterilized all quinaria group hosts, only one of which is a host in nature. The large potential host ranges of these parasites, in combination with the high potential for host colonization due to shared mushroom breeding sites, explain the widespread host switching observed in comparisons of nematode and Drosophila phylogenies.     

Virulence reaction norms across a food gradient

Host-parasite interactions involve competition for nutritional resources between hosts and the parasites growing within them. Consuming part of a host's resources is one cause of a parasite's virulence, i.e. part of the fitness cost imposed on the host by the parasite. The influence of a host's nutritional conditions on the virulence of a parasite was experimentally tested using the mosquito Aedes aegypti and the microsporidian parasite Vavraia culicis. A condition-dependent expression of virulence was found and a positive relation between virulence and transmissibility was established. Spore production was positively influenced by host food availability, indicating that the parasite's within-host growth is limited by host condition. We also investigated how the fitness of each partner varied across the nutritional gradient and demonstrated that the sign of the correlation between host fitness and parasite fitness depended on the amount of nutritional resources available to the host.     

Swimming against the current: genetic structure, host mobility and the drift paradox in trematode parasites

Life-cycle characteristics and habitat processes can potentially interact to determine gene flow and genetic structuring of parasitic species. In this comparative study, we analysed the genetic structure of two freshwater trematode species with different life histories using cytochrome c oxidase I gene (COI) sequences and examined the effect of a unidirectional river current on their genetic diversity at 10 sites along the river. We found moderate genetic structure consistent with an isolation-by-distance pattern among subpopulations of Coitocaecum parvum but not in Stegodexamene anguillae. These contrasting parasite population structures were consistent with the relative dispersal abilities of their most mobile hosts (i.e. their definitive hosts). Genetic diversity decreased, as a likely consequence of unidirectional river flow, with increasing distance upstream in C. parvum, which utilizes a definitive host with only restricted mobility. The absence of such a pattern in S. anguillae suggests that unidirectional river flow affects parasite species differently depending on the dispersal abilities of their most mobile host. In conclusion, genetic structure, genetic diversity loss and drift are stronger in parasites whose most mobile hosts have low dispersal abilities and small home ranges. An additional prediction can be made for parasites under unidirectional drift: those parasites that stay longer in their benthic intermediate host or have more than one benthic intermediate hosts would have relatively high local recruitment and hence increased retention of upstream genetic diversity.     

Determinants of host-specificity in parasites of freshwater fishes.

Factors responsible for interspecific variability in host-specificity were investigated within 15 genera (including 176 species) of metazoan parasites found in Canadian freshwater fish. For each species in a genus, the parasite's number of known hosts was determined from published host-parasite records. The effects of the total number and mean size of potential hosts (i.e. all fish species belonging to the family or families that include a parasite's known hosts) on number of hosts of congeneric species were evaluated using multiple regressions. Since parasite species that have been recorded often tend to have greater numbers of known hosts than do seldom-recorded parasites, it was necessary to control for the confounding effect of study intensity. In all parasite genera, whether from highly specific taxa such as monogeneans or from less host-specific ones, there was a positive relationship between the number of potential hosts and the number of known hosts. However, no consistent relationships were observed between the mean size of potential hosts and number of known hosts. These results suggest that the availability of suitable host species may have been a key factor limiting the colonization of new hosts by fish parasites.     

Do mosquitoes filter the access of Plasmodium cytochrome b lineages to an avian host?

Many parasites show fidelity to a set of hosts in ecological time but not evolutionary time and the determinants of this pattern are poorly understood. Malarial parasites use vertebrate hosts for the asexual stage of their life cycle but use Dipteran hosts for the sexual stage. Despite the potential evolutionary importance of Dipteran hosts, little is known of their role in determining a parasite's access to vertebrate hosts. Here, we use an avian malarial system in Panama to explore whether mosquitoes act as an access filter that limits the range of vertebrate hosts used by particular parasite lineages. We amplified and sequenced Plasmodium mitochondrial DNA (mtDNA) from Turdus grayi (clay-coloured robin) and from mosquitoes at the same study site. We trapped and identified to species 123 141 female mosquitoes and completed polymerase chain reaction (PCR) screening for Plasmodium parasites in 435 pools of 20 mosquitoes per pool (8700 individuals total) spanning the 11 most common mosquito species. Our primers amplified nine Plasmodium lineages, whose sequences differed by 1.72%–10.0%. Phylogenetic analyses revealed partial clustering of lineages that co-occurred in mosquito hosts. However PAN3 and PAN6, the two primary parasite lineages of T. grayi , exhibited sequence divergence of 8.59% and did not cluster in the phylogeny. We detected these two lineages exclusively in mosquitoes from different genera — PAN3 was found only in Culex (Melanoconion) ocossa , and PAN6 was found only in Aedeomyia squamipennis . Furthermore, each of these two parasite lineages co-occurred in mosquitoes with other Plasmodium lineages that were not found in the vertebrate host T. grayi . Together, this evidence suggests that parasite–mosquito associations do not restrict the access of parasites to birds but instead may actually facilitate the switching of vertebrate hosts that occurs over evolutionary time.     

Differential reproductive success favours strong host preference in a highly specialized brood parasite

Obligate avian brood parasites show dramatic variation in the degree to which they are host specialists or host generalists. The screaming cowbird Molothrus rufoaxillaris is one of the most specialized brood parasites, using a single host, the bay-winged cowbird (Agelaioides badius) over most of its range. Coevolutionary theory predicts increasing host specificity the longer the parasite interacts with a particular avian community, as hosts evolve defences that the parasite cannot counteract. According to this view, host specificity can be maintained if screaming cowbirds avoid parasitizing potentially suitable hosts that have developed effective defences against parasitic females or eggs. Specialization may also be favoured, even in the absence of host defences, if the parasite's reproductive success in alternative hosts is lower than that in the main host. We experimentally tested these hypotheses using as alternative hosts two suitable but unparasitized species: house wrens (Troglodytes aedon) and chalk-browed mockingbirds (Mimus saturninus). We assessed host defences against parasitic females and eggs, and reproductive success of the parasite in current and alternative hosts. Alternative hosts did not discriminate against screaming cowbird females or eggs. Egg survival and hatching success were similarly high in current and alternative hosts, but the survival of parasitic chicks was significantly lower in alternative hosts. Our results indicate that screaming cowbirds have the potential to colonize novel hosts, but higher reproductive success in the current host may favour host fidelity.     

Partial host fidelity in nest selection by the shiny cowbird (Molothrus bonariensis), a highly generalist avian brood parasite

Obligate avian brood parasites can be host specialists or host generalists. In turn, individual females within generalist brood parasites may themselves be host specialists or generalists. The shiny cowbird Molothrus bonariensis is an extreme generalist, but little is known about individual female host fidelity. We examined variation in mitochondrial control region sequences from cowbird chicks found in nests of four common Argentinean hosts. Haplotype frequency distributions differed among cowbird chicks from nests of these hosts, primarily because eggs laid in nests of house wrens Troglodytes aedon differed genetically from those laid in nests of the other three hosts (chalk-browed mockingbird Mimus saturninus, brown-and-yellow marshbird Pseudoleistes virescens, and rufous-collared sparrow Zonotrichia capensis). These differences in a maternally inherited marker indicate the presence of a nonrandom laying behaviour in the females of this otherwise generalist brood parasite, which may be guided by choice for nest type, as house wrens nest in cavities whereas the other three species are open cup nesters.     

The role of moulting in parasite defence

Parasitic infections consist of a succession of steps during which hosts and parasites interact in specific manners. At each step, hosts can use diverse defence mechanisms to counteract the parasite's attempts to invade and exploit them. Of these steps, the penetration of parasites into the host is a key step for a successful infection and the epithelium is the first line of host defence. The shedding of this protective layer (moulting) is a crucial feature in the life cycle of several invertebrate and vertebrate taxa, and is generally considered to make hosts vulnerable to parasites and predators. Here, we used the crustacean Daphnia magna to test whether moulting influences the likelihood of infection by the castrating bacterium Pasteuria ramosa. This parasite is known to attach to the host cuticula before penetrating into its body. We found that the likelihood of successful parasite infection is greatly reduced if the host moults within 12 h after parasite exposure. Thus, moulting is beneficial for the host being exposed to this parasite. We further show that exposure to the parasite does not induce hosts to moult earlier. We discuss the implications of our findings for host and parasite evolution and epidemiology.     

Phenotypic plasticity of host-parasite interactions in response to the route of infection

The microsporidium Octosporea bayeri can infect its host, the planktonic crustacean Daphnia magna, vertically and horizontally. The two routes differ greatly in the way the parasite leaves the harbouring host (transmission) and in the way it enters a new, susceptible host (infection). Infections resulting from each route may thus vary in the way they affect host and parasite life-histories and, subsequently, host and parasite fitness. We conducted a life-table experiment to compare D. magna infected with O. bayeri either horizontally or vertically, using three different parasite isolates. Both the infection route and the parasite isolate had significant effects on host life-history. Hosts matured at different ages depending on the parasite isolate, and at a size that varied with infection route. The frequency of host sterility and the host's life-time reproductive success were affected by both the infection route and the parasite isolate. The infection route also affected parasite life-history. The production of parasite spores was much higher in vertically than in horizontally infected hosts. We found a trade-off between the production of spores (the parasite's horizontal fitness component) and the production of infected host offspring (the parasite's vertical fitness component). This study shows that hosts and parasites can react plastically to different routes of infection, suggesting that ecological factors that may influence the relative importance of horizontal and vertical transmission can shape the evolution of host and parasite life histories, and, consequently, the evolution of virulence.     

Coevolution of daily activity timing in a host–parasite system

Coevolutionary theories applied in the study of host–parasite systems indicate that lineages exhibit progressive trends in response to reciprocal selective pressures. Avian brood parasites have generated intense interest as models for coevolutionary processes. Similar to avian cuckoos, Polistes wasp social parasites usurp a nest and exploit the parental care of a congeneric species to rear their own brood. In the present study, we show a coevolutionary arms race in the daily activity pattern in a Polistes host–parasite pair. We measured the daily activity rate, in constant laboratory conditions, of both host and parasite females during the period in which nest usurpations occur. The parasites showed a hyperkinesis in the middle of the day. As the field observations suggested, this mid-day activity is used to perform host nest usurpation attempts. Timing the usurpations allows the parasite to maximize its usurpation attempts during daytime when the host defence is lower. A field comparison of host presence on the nest in two populations with different parasitism rates showed that populations under strong parasitic pressure exhibit timing counteradaptations to optimize nest defence. This study provides the first example of a mutual coadaptation in timing activity in a parasite–host system.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 96 , 399–405.     

Infection of Gymnodinium sanguineum by the dinoflagellate Amoebophrya sp.: effect of nutrient environment on parasite generation time, reproduction, and infectivity

Preliminary attempts to culture Amoebophrya sp., a parasite of Gymnodinium sanguineum from Chesapeake Bay, indicated that success may be influenced by water quality. To explore that possibility, we determined development time, reproductive output, and infectivity of progeny (i.e. dinospores) for Amoebophyra sp. maintained on G. sanguineum grown in four different culture media. The duration of the parasite's intracellular growth phase showed no significant difference among treatments; however, the time required for completion of multiple parasite generations did, with elapsed time to the middle of the third generation being shorter in nutrient-replete media. Parasites of hosts grown in nutrient-replete medium also produced three to four times more dinospores than those infecting hosts under low-nutrient conditions, with mean values of 380 and 130 dinospores/host, respectively. Dinospore production relative to host biovolume also differed, with peak values of 7.4 per 1,000 microm3 host for nutrient-replete medium and 4.8 per 1,000 microm3 host for nutrient-limited medium. Furthermore, dinospores produced by "high-nutrient" parasites had a higher success rate than those formed by "low-nutrient" parasites. Results suggest that Amoebophrya sp. is well adapted to exploit G. sanguineum populations in nutrient-enriched environments.