Combining phylogenetic and ecological information into a new index of host specificity

Host specificity has 2 independent facets: the extent to which different host species are used by a parasite, and the phylogenetic distances among these hosts. Although the number of host species exploited by a parasite commonly is used as a measure of host specificity, it fails to capture ecological and phylogenetic differences among hosts. Here, a new index of host specificity, S(TD)*, is developed and illustrated. This index measures the average taxonomic distinctness among the host species used by a parasite, weighted for the parasite's prevalence in the different hosts. For a given number of host species, the index approaches its minimum value when a parasite achieves high prevalence in a few closely related host species, and the index approaches its highest value when a parasite reaches its highest prevalence values in distantly related host species. Simple hypothetical examples are used to demonstrate the index's computation and some of its properties. The new index is influenced independently both by the taxonomic (or phylogenetic) affinities of a set of host species and by the distribution of prevalence values among these hosts. A single value cannot truly capture all the nuances of a phenomenon as complex as host specificity; nevertheless, the proposed index incorporates the features of specificity that are most relevant to parasitologists and will be a useful tool for comparative studies.     

Host traits associated with species roles in parasite sharing networks

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

Host-parasite associations and host-specificity in haemoparasites of reed bed passerines

The host specificity and host sharing of avian haemoparasites (genera Haemoproteus and Plasmodium) is still poorly known, although they infect a large proportion of several studied bird populations. This study used molecular techniques to detect haemoparasites in marsh warblers and in other passerines that feed in reed beds, at 4 sites in Portugal. The host-specificity of the parasite lineages was analysed and compared with other cases described in the literature to assess whether apparent host specificity changes according to the studied system. Nine lineages of Haemoproteus and 15 of Plasmodium were found, of which only 10 Plasmodium were proven to have local transmission. Each lineage was confined to a distinct set of host species. The distribution of parasites in the host species was non-nested, meaning that specialist lineages did not always share hosts with generalists. The most prevalent lineages were those with a wider host range, indicating that the ability to infect more hosts will enhance a parasite's prevalence in its entire host range. We also found that in our areas, a specialist parasite (H. MW1) appears to have a more generalist character than described in the literature, suggesting that a parasite's apparent specialization can depend on the type of host species sampled.     

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.     

Circulation of parasites among fishes from lakes in the Caribou Mountains,Alberta, Canada

Circulation of 24 macroparasite species among 12 species of fish was evaluated within samples of hosts collected from 9 lakes on an isolated plateau in northern Alberta, Canada. Twenty-seven parasite taxa (24 species plus the larval stages of Triaenophorus crassus, T. stizostedionis, and Raphidascaris acus) had the potential to be circulated among hosts. Sixteen parasite taxa were recovered from a single host species within a lake. Of the 11 remaining nonspecialist taxa, 4 were larval stages that matured in fish or birds and 7 were adults. Eight of the 11 cases of circulation among hosts involved lake whitefish, and this host was involved in the transmission of 5 species to piscivorous fishes. Despite evidence for the circulation of 7 taxa among the 4 species of sympatric Salmonidae, 60-99% of all worms were recovered from just 1 species of host. These results indicated that approximately 60% of the parasite taxa that infected fish in these lakes were absolute host specialists. The remaining 40% of parasite taxa had restricted host ranges, with most examples of parasite circulation limited to the 2 species of sympatric coregonid.     

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.     

Prevalence and intensity of Pseudodelphis oligocotti n. gen., n. sp. (Dracunculoidea; Guyanemidae) in the tidepool sculpin, Oligocottus maculosus (Scorpaeniformes; Cottidae)

Pseudodelphis oligocotti n. gen., n. sp. (Dracunculoidea; Guyanemidae) is described from the tidepool sculpin, Oligocottus maculosus (Scorpaeniformes; Cottidae), from various localities in coastal British Columbia. The species is placed in Guyanemidae because of its reduced buccal capsule, divided esophagus, functional vulva, and single ovary. It is distinguished from Guyanema, the only other genus in the family, by the absence of caudal alae and the arrangement of caudal papillae in the male. Females of the new genus are distinguished from those of Guyanema by the presence of a blind uterine diverticulum, without associated oviduct and ovary, extending anteriorly from the junction of the posterior uterus and vagina, and a more posteriorly positioned vulva. Fish were sampled every 2 wk throughout 1988. Worms were overdispersed in the host population. Prevalence and mean intensity of infection were highest from February to March.     

Niche breadth in parasites: an evolutionarily stable strategy model, with special reference to the protozoan parasite Leishmania.

A parasite's host range essentially defines its niche breadth, which, as foraging theory predicts, is influenced by resource availability. For parasites, the interaction of infection and transmission characteristics with host population dynamics determines host availability. An epidemiological model, involving two host types and describing competition between a "generalist" parasite strain and a related "specialist" strain, is used to examine the interplay among host range, relative host availabilities, and adaptational compromises engendered by increased host range. Results show that the generalist can predominate even when it cannot maintain itself in either host alone, but that the specialist can persist if its reproductive rate attains some threshold relative to either of the generalist's respective rates in its two hosts. The model is in rough, qualitative agreement with observed dynamics of two Leishmania parasite-host systems, and overall results suggest that infection of two species with a common parasite can lead to complex, indirect coevolutionary dynamics.     

Variation in infection parameters among populations within parasite species: intrinsic properties versus local factors

Within any parasite species, variation among populations in standard infection parameters (prevalence, intensity and abundance) is an accepted fact. The proportion of hosts infected and the mean number of parasites per host are not fixed values across the entire geographic range of any parasite species. The question is whether this inter-population variation occurs within a narrow, species-specific range and is thus driven mainly by the biological features of the parasite, or whether it is substantial and unpredictable, leaving population parameters at the mercy of local conditions. Here, the repeatability of estimates of prevalence, intensity and abundance of infection was assessed across populations of the same parasite species, for 77 metazoan parasite species of Canadian freshwater fishes. Overall, parameter values from different populations of the same parasite species were more similar to each other and more different from those of other species, than expected by chance alone. Much of the variation in parameter values in the dataset was associated with differences between parasite species, rather than with differences among populations within species. This was particularly true for intensity and abundance of infection; in contrast, prevalence values, while somewhat repeatable among populations of the same species, still showed considerable variation. Among the higher taxa investigated (monogeneans, trematodes, cestodes, nematodes, acanthocephalans, copepods), there was no evidence that species of one taxon display intrinsically greater variation in population parameters than species of other taxa. Overall, the results suggest that intensity and abundance of infection are real species characters, though somewhat variable. This conclusion supports the view that the biological features of parasite species can potentially override local environmental conditions in driving parasite population dynamics.     

Life history interactions with environmental conditions in a host–parasite relationship and the parasite's mode of transmission

The microsporidian parasite Edhazardia aedis is capable of vertical or horizontal transmission among individuals of its host, the mosquito Aedes aegypti, and either mode of transmission may follow the other. We show that following the horizontal infection of host larvae, the parasite's subsequent mode of transmission largely depends on host life history traits and their responses to different environmental conditions. In two experiments the intensity of larval exposure to infection and the amount of food available to them were simultaneously manipulated. One experiment followed the dynamics of host development and the parasite's production of spores while the other estimated the outcome of their relationship. Host life history traits varied widely across treatment conditions while those of the parasite did not. Of particular importance was the host's larval growth rate. Horizontal rather than vertical transmission by the parasite was more likely as low food and high dose conditions favoured slower larval growth rates. This pattern of transmission behaviour with host growth rate can be considered in terms of reproductive value: the potential vertical transmission success that female mosquitoes offer the parasite decreases as larval growth rates slow and makes them more attractive to exploitation for horizontal transmission (requiring host mortality). However, the lack of variation in the parasite's life history traits gave rise in some conditions to low estimates for both its vertical and horizontal transmission success. We suggest that the unresponsive behaviour of the parasite's life history traits reflects a bet-hedging strategy to reduce variance in its overall transmission success in the unpredictable environmental conditions and host larval growth rates that this parasite encounters in nature.     

Ecosystem consequences of fish parasites*

In most aquatic ecosystems, fishes are hosts to parasites and, sometimes, these parasites can affect fish biology. Some of the most dramatic cases occur when fishes are intermediate hosts for larval parasites. For example, fishes in southern California estuaries are host to many parasites. The most common of these parasites, Euhaplorchis californiensis, infects the brain of the killifish Fundulus parvipinnis and alters its behaviour, making the fish 10–30 times more susceptible to predation by the birds that serve as its definitive host. Parasites like E. californiensis are embedded in food webs because they require trophic transmission. In the Carpinteria Salt Marsh estuarine food web, parasites dominate the links and comprise substantial amount of biomass. Adding parasites to food webs alters important network statistics such as connectance and nestedness. Furthermore, some free‐living stages of parasites are food items for free‐living species. For instance, fishes feed on trematode cercariae. Being embedded in food webs makes parasites sensitive to changes in the environment. In particular, fishing and environmental disturbance, by reducing fish populations, may reduce parasite populations. Indirect evidence suggests a decrease in parasites in commercially fished species over the past three decades. In addition, environmental degradation can affect fish parasites. For these reasons, parasites in fishes may serve as indicators of environmental impacts.     

Long-term prevalence data reveals spillover dynamics in a multi-host (Artemia), multi-parasite (Microsporidia) community

In the study of multi-host parasites, it is often found that host species contribute asymmetrically to parasite transmission. Yet in natural populations, identifying which hosts contribute to parasite transmission and maintenance is a recurring challenge. Here, we approach this issue by taking advantage of natural variation in the composition of a host community. We studied the brine shrimps Artemia franciscana and Artemia parthenogenetica and their microsporidian parasites Anostracospora rigaudi and Enterocytospora artemiae. Previous laboratory experiments had shown that each host can transmit both parasites, but could not predict their actual contributions to the parasites’ maintenance in the field. To resolve this, we gathered long-term prevalence data from a metacommunity of these species. Metacommunity patches could contain either or both of the Artemia host species, so that the presence of the hosts could be linked directly to the persistence of the parasites. First, we show that the microsporidian A. rigaudi is a spillover parasite: it was unable to persist in the absence of its maintenance host A. parthenogenetica. This result was particularly striking, as A. rigaudi displayed both high prevalence (in the field) and high infectivity (when tested in the laboratory) in both hosts. Moreover, the seasonal presence of A. parthenogenetica imposed seasonality on the rate of spillover, causing cyclical pseudo-endemics in the spillover host A. franciscana. Second, while our prevalence data was sufficient to identify E. artemiae as either a spillover or a facultative multi-host parasite, we could not distinguish between the two possibilities. This study supports the importance of studying the community context of multi-host parasites, and demonstrates that in appropriate multi-host systems, sampling across a range of conditions and host communities can lead to clear conclusions about the drivers of parasite persistence.     

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.     

Local adaptation and enhanced virulence of Nosema granulosis artificially introduced into novel populations of its crustacean host, Gammarus duebeni

Local adaptation theory predicts that, on average, most parasite species should be locally adapted to their hosts (more suited to hosts from local than distant populations). Local adaptation has been studied for many horizontally transmitted parasites, however, vertically transmitted parasites have received little attention. Here we present the first study of local adaptation in an animal/parasite system where the parasite is vertically transmitted. We investigate local adaptation and patterns of virulence in a crustacean host infected with the vertically transmitted microsporidian Nosema granulosis. Nosema granulosis is vertically transmitted to successive generations of its crustacean host, Gammarus duebeni and infects up to 46% of adult females in natural populations. We investigate local adaptation using artificial horizontal infection of different host populations in the UK. Parasites were artificially inoculated from a donor population into recipient hosts from the sympatric population and into hosts from three allopatric populations in the UK. The parasite was successfully established in hosts from all populations regardless of location, infecting 45% of the recipients. Nosema granulosis was vertically (transovarially) transmitted to 39% of the offspring of artificially infected females. Parasite burden (intensity of infection) in developing embryos differed significantly between host populations and was an order of magnitude higher in the sympatric population, suggesting some degree of host population specificity with the parasite adapted to its local host population. In contrast with natural infections, artificial infection with the parasite resulted in substantial virulence, with reduced host fecundity (24%) and survival (44%) of infected hosts from all the populations regardless of location. We discuss our findings in relation to theories of local adaptation and parasite-host coevolution.     

Community ecology of the parasites of adult spot, Leiostomus xanthurus, and Atlantic croaker, Micropogonias undulatus (Sciaenidae) in the Cape Hatteras region

Twenty-three species of metazoan parasites were recorded from adult spot and 26 from adult croaker. Of the 33 parasitic species found, 17 occurred in both spot and croaker. No significant differences in intensity of parasites occurred between sexes of either spot or croaker. All of the parasites had over-dispersed, or clumped, distributions among hosts. Adult spot and croaker collected offshore had much greater species-richness, diversity, and total number of individual parasites than juvenile fishes collected in adjoining estuaries during another study. The juvenile spot and croaker had less time to acquire parasites and inhabited less diverse and more confined habitats in inshore estuaries, which resulted in less diverse parasite communities than offshore fishes. The number of species and diversity of parasites in adult fish was greater in croaker than spot. However, when only gastrointestinal helminths were considered, spot had greater species-richness as well as greater numbers of individual helminths, suggesting that they had a more diverse diet and that they fed on more infected intermediate hosts than croaker. In both adult spot and croaker the mean number of parasitic species was greater than those of freshwater fishes and fewer than those for birds and mammals. The total number of individual parasites was similar to that of freshwater fishes. The opportunistic diet and the migratory habits of both spot and croaker contribute to their diverse parasite faunas. Comparison of adult spot and croaker parasite faunas collected offshore indicated that their respective parasite component communities were distinct and that similar parasite infracommunity variability existed in both hosts and that their communities were not ‘random’ samples, but restricted subsets of the compound community. Although the parasite dominance hierarchy in adults of both species varied slightly between areas and seasons sampled, there appeared to be a predictable dominant species that was accompanied by subordinate, less predictable species. However, the variability in both relative intensities and presence-absence of parasites within communities resulting from their diverse diets make them less predictable than those of other vertebrates with less diverse diets such as the lesser scaup duck and more like those of other marine fishes.     

Differential resistance among host and non-host species underlies the variable success of the hemi-parasitic plant Rhinanthus minor

BACKGROUND AND AIMS: Rhinanthus minor is a root hemiparasitic plant that attacks a wide range of host species which are severely damaged by the parasite. Rhinanthus minor also attempts unsuccessfully to form connections to a range of non-hosts which in contrast are not damaged by the parasite; however, the underlying physiological basis of these differences is not fully understood. METHODS: Biomass of host-parasite combinations was studied, and histology, electron microscopy and FT-IR microspectroscopy were used to determine the cellular-level interactions between Rhinanthus haustoria (the parasite's connective structure) and the roots of a range of potential host species. RESULTS: Two distinct defence responses were observed in the non-host forbs Plantago lanceolata and Leucanthemum vulgare. Firstly, L. vulgare was able to encapsulate the parasite's invading structures preventing it from gaining access to the stele. This was supported by FT-IR microspectroscopy, used to monitor lignification in response to Rhinanthus haustoria. Secondly, host cell fragmentation was observed at the interface between the parasite and P. lanceolata. Growth data confirmed the non-host status of the two forbs whilst, in contrast, grasses and a legume which were good hosts showed no evidence of defence at the host/parasite interface. CONCLUSIONS: Variable resistance to Rhinanthus is shown for the first time to be controlled by cellular-level resistance to haustoria by either cell fragmentation or lignification at the host/parasite interface.     

Comparison of the parasitic fauna of Aplocheilus panchax and A. melastigma

The metazoan parasite fauna of two species of freshwater fishes Aplocheilus panchax and A. melastigma collected from a stream at Waltair is compared; 17 parasite species were found. Aplocheilus panchax served as a host to 13 parasite species and A. melastigma to 10 parasite species. Of the 17 parasites collected, 12 were larval helminths to which the fishes act as intermediate and paratenic hosts. This has been attributed to the interaction between terrestrial birds, mammals and fishes in determining the parasite fauna in the biocoenosis. The parasite fauna of these fishes is divided into typical and less typical according to their frequencies. Among less typical there are peripheral division parasites which are abundant in other fishes in the stream. Only six parasite species occurred in both A. panchax and A. melastigma and both fish shared most of their parasite fauna with other fishes. Differences in the parasite fauna of these fishes are attributed to the morphological, behavioural or ecological features of these fishes.     

Diversity, distribution and exchange of blood parasites meeting at an avian moving contact zone

Research on contact zones has paid relatively little attention to host-parasite interactions, although these situations have important but different implications depending on whether one considers the host or the parasite's perspective. We investigated both the role of a host contact zone in parasite expansion and whether parasites could influence contact zone dynamics. We studied the diversity and the patterns of parasite exchange (genera Haemoproteus and Plasmodium) infecting two parapatric sibling passerines meeting at a moving contact zone in western Europe. We amplified and sequenced a fragment of the parasite cytochrome b gene. The expanding host harboured more diverse parasites, which might indicate a superior ability to face a diverse parasite fauna than the receding host. Prevalence was very high in both hosts, due to the frequent occurrence of two sister Haemoproteus lineages. Despite the recent movement of the contact zone, these two parasites fitted almost perfectly to the geographic range of their main host species. Yet, we found several cases of cross-species infection in sympatric areas and evidences of asymmetrical spreading of parasites from the expanding host towards the receding host. Altogether, our results suggest that the host contact zone mainly acts as a barrier to parasite expansion even if recurrent host shifts are observed. Besides, they also support the idea that parasite-mediated competition might contribute to the displacement of hosts' contact zones, thereby emphasizing the role of parasitism on the population dynamics of sympatric species.     

Information about transmission opportunities triggers a life-history switch in a parasite

Many microbial pathogens can switch to new hosts or adopt alternative transmission routes as environmental conditions change, displaying unexpected flexibility in their infection pathways and often causing emerging diseases. In contrast, parasitic worms that must develop through a fixed series of host species appear less likely to show phenotypic plasticity in their transmission pathways. Here, I demonstrate experimentally that a trematode parasite, Coitocaecum parvum, can accelerate its development and rapidly reach precocious maturity in its crustacean intermediate host in the absence of chemical cues emanating from its fish definitive host. Juvenile trematodes can also mature precociously when the mortality rate of their intermediate hosts is increased. Eggs produced by precocious adults hatch into viable larvae, capable of pursuing the parasite's life cycle. In the absence of chemical cues from fish hosts, the size of eggs released by precocious trematodes in their intermediate hosts becomes more variable, possibly indicating a bet-hedging strategy. These results illustrate that parasitic worms with complex life cycles have development and transmission strategies that are more plastic than commonly believed, allowing them to skip one host in their cycle when they perceive limited opportunities for transmission.     

Circulation pattern and transmission dynamics of the supra-population of the nematode Cystidicoloides tenuissima (Zeder) in the River Swincombe, England

The circulation pattern and transmission dynamics of larval and adult Cystidicoloides tenuissima in all its intermediate and definitive hosts were investigated and quantified at three sites in a small upland stream over a period of 1 year. Both brown trout, Salmo trutta , and salmon parr, S. salar , were suitable definitive hosts, but because of the greater importance of the mayfly intermediate host in the diet of trout, between 73 and 98% of the parasite infrapopulation in fish circulated through this species. Trout was the only required host, and was alone responsible for the perpetuation of the parasite suprapopulation in the river. Around 99% of the parasite's eggs produced originated from trout but, of these, 90% or more failed to be ingested by an insect. Larval parasites were found in 18 species of insects, but could develop to the infective third stage in only one species, the mayfly Leptophlebia marginata. Two common but unsuitable species harboured up to 80% of the larval parasites, and less than 10% actually circulated through L. marginata. Differences in circulation pattern between sites could be related more to differences in fish feeding preferences than to differences in fish or insect density, but monthly differences in transmission rate reflected both fish diet and insect abundance. The overall mean transmission rate of eggs to larvae in L. marginata varied between 0.25 and 0.87%, but transmission rates of these larvae to fish were far higher, from 10.8 to 39.8%. The relative importance of ecological factors, host community structure and parasite specificity in determining circulation routes and transmission efficiencies are discussed.