Patterns of host specificity and transmission among parasites of wild primates

Multihost parasites have been implicated in the emergence of new diseases in humans and wildlife, yet little is known about factors that influence the host range of parasites in natural populations. We used a comprehensive data set of 415 micro- and macroparasites reported from 119 wild primate hosts to investigate broad patterns of host specificity. The majority (68%) of primate parasites were reported to infect multiple host species, including animals from multiple families or orders. This pattern corresponds to previous studies of parasites found in humans and domesticated animals. Within three parasite groups (viruses, protozoans and helminths), we examined parasite taxonomy and transmission strategy in relation to measures of host specificity. Relative to other parasite groups, helminths were associated with the greatest levels of host specificity, whereas most viruses were reported to infect hosts from multiple families or orders. Highly significant associations between the degree of host specificity and transmission strategy arose within each parasite group, but not always in the same direction, suggesting that unique constraints influence the host range of parasites within each taxonomic group. Finally characteristics of over 100 parasite species shared between wild primates and humans, including those recognised as emerging in humans, revealed that most of these shared parasites were reported from multiple host orders. Furthermore, nearly all viruses that were reported to infect both humans and non-human primates were classified as emerging in humans.     

Group-living and the richness of the parasite fauna in Canadian freshwater fishes

Summary An increased transmission of ectoparasites among individual animals is considered to be an inevitable cost of living in groups, since several kinds of ectoparasites require close proximity between large numbers of hosts for successful transmission. However, we do not know whether individuals belonging to group-living species incur a greater risk of ectoparasitism than individuals of solitary species. Here, using published data from 3 families (60 species) of Canadian freshwater fishes, I test the hypothesis that group-living species are host to more species of contagious ectoparasites (copepods and monogeneans) than solitary host species. As the different fish species have been studied with varying intensity, I used the mean number of parasite species recorded per study as a standard measure of parasite numbers. Multiple regression analyses were performed separately for each family to determine the effects of group-living and of 3 other variables (host size, age, and range) on the richness of the recorded parasite fauna. Once the effects of the other variables were removed, I found no significant effect of sociality on the richness of the parasite fauna per fish species, for contagious ectoparasites and other types of parasites. Neither of the other variables had any influence on the numbers of parasite species per fish species. These results suggest that a richer ectoparasite fauna is not a cost of group-living in fishes.     

Demersal fish parasite fauna around the South Shetland Islands: high species richness and low host specificity in deep Antarctic waters

A total of nine Antarctic fish species belonging to five families were examined for their endohelminth parasite fauna. The fishes Parachaenichthys charcoti (Bathydraconidae), Chaenocephalus aceratus (Channichtyidae), Paradiplospinus gracilis (Gempylidae), Muraenolepis microps (Muraenolepididae), Gobionotothen gibberifrons, Lepidonotothen larseni, L. nudifrons, L. squamifrons, and Trematomus eulepidopus (Nototheniidae) were caught between 80 and 608 m trawling depth off the Antarctic Peninsula (Elephant Island, King George Island) in 1996. Nineteen different parasites species comprising five Digenea, two Cestoda, four Nematoda, and eight Acanthocephala were found. Pseudophyllidean cestodes, the nematodes Contracaecum radiatum and C. osculatum as well as the acanthocephalan Corynosoma bullosum were the most common, infesting eight of the fish species studied with prevalences reaching 100%. Pseudoterranova decipiens s.l. was the only parasite that was isolated from all studied fish species; however, at a lower intensity. The observed parasite host specificity was low, and the species richness in a single fish ranged from one to eleven in a C. aceratus. This icefish and the moray cod M. microps were the most heavily infested fish, harbouring many adult and larval parasitic stages. The benthodemersal P. gracilis had only two larval parasite species, while the nototheniids had very similar parasite communities, harbouring a total of 8–14 species. Larval mammalian parasites were found to utilize fish, especially the nototheniids and channichthyids, as a common transmission route into their final hosts. The fish parasites parallel explored different benthic host systems to reach the most suitable host. In contrast to the coast and continental shelf, the meso/bathypelagiac zone appears to be species poor and is inhabited by few larval forms. The fish parasite fauna off the South Shetland Islands can be characterized by generalistic parasites that distribute within Antarctic waters according to the feeding ecology and depth range of their teleost hosts, not only horizontally but also extending vertically into the deep sea.     

Geography and host specificity: two forces behind the genetic structure of the freshwater fish parasite Ligula intestinalis (Cestoda: Diphyllobothriidae)

Parasite species with global distributions and complex life cycles offer a rare opportunity to study alternative mechanisms of speciation and evolution in a single model. Here, genealogy and genetic structure, with respect to geography and fish host preference, have been analyzed for Ligula intestinalis, a tapeworm affecting freshwater fish. The data analyzed consisted of 109 tapeworms sampled from 13 fish host species in 18 different localities on a macrogeographic scale. Two mitochondrial genes, cytochrome oxidase subunit I and cytochrome B, and the nuclear sequence of intergenic transcribed spacer 2 (ITS2) were used for the genetic reconstruction. Different evolutionary patterns were found at the local and at the global geographic scales. On a local scale, the flat genetic structure was mainly attributed to contiguous range expansion. Migrating birds are the most likely cause of the homogenisation of the whole population, preventing the creation of significant genetic barriers. By contrast, on a global scale, genetically distant and well-separated clusters are present in different geographic areas. Reproductive isolation was found even between clades living in sympatry and infecting the same definitive host, suggesting the existence of efficient biologically determined genetic barriers, and thus possibly separate species. Although the ITS2 sequences were found to display considerable intragenomic variability, their relationships were generally in good agreement with the topology derived from mitochondrial genes.     

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

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

Gastrointestinal helminth fauna of Enyalius perditus (Reptilia: Leiosauridae): relation to host age and sex

The purpose of this study was to determine how the gastrointestinal helminthofauna varies according to the age and sex of the lizard, Enyalius perditus, captured in Ibitipoca State Park in the state of Minas Gerais, Brazil, and to discuss the ecological and behavioral significance of these relationships. Fifty-five specimens of E. perditus were captured in drop traps, then killed, necropsied, and examined for the presence of helminths in the gastrointestinal tract. Nematodes, including Strongyluris oscari, Oswaldocruzia subauricularis, and Aplectana vellardi, were found. This was the first record of the last-named species in reptiles, and the first record of the first 2 species in E. perditus. The number of helminths increased with snout-vent length and, therefore, age of the lizards. Male E. perditus lizards were more heavily infected by nematodes than females; the largest numbers of nematodes occurred in the caecum and large intestine.     

Diversity and biogeographical relationships of the Australian cestode fauna

The Australian cestode fauna remains poorly documented with a total of 342 species recorded to date. The best-studied host groups are the elasmobranchs and the marsupials, but even in these groups, only 32 and 25% of known host species, respectively, have been examined for parasites. Overall, cestodes have been reported from only 5% of the known vertebrate species. Representatives of virtually all cestode orders and most of the cyclophyllidean families have been recorded from Australia. In spite of these deficiencies, some biogeographical patterns are discernible. In the elasmobranchs, a significant proportion of the known cestodes is endemic while other associations exist with eastern Pacific and Indo-west Pacific faunas. Also identifiable is a group of cosmopolitan species. The nematotaeniids of amphibians suggest Gondwanan affiliations, while the known proteocephalideans, parasitic in reptiles and amphibians, may represent an Asian invasion. Associations of the avian cestodes represent an unexplored but potentially rewarding avenue of biogeographical study. The cestodes of mammals include families with a Gondwanan distribution (Linstowiidae, Hymenolepididae) as well as those (Anoplocephalidae) with an apparent origin in southeast Asia. In addition, a number of genera of cyclophyllidean cestodes (Anoplotaenia, Dasyurotaenia) occurring in marsupials represent biogeographical challenges, not being accommodated within any of the known cestode families. The Australian cestode fauna therefore provides potentially outstanding opportunities for studies of the biogeographical relationships of a number of cestode groups.     

Origins, diversification, and historical structure of the helminth fauna inhabiting neotropical freshwater stingrays (Potamotrygonidae).

Members of the freshwater stingray family Potamotrygonidae occur throughout the major river systems of eastern South America that empty into the Atlantic Ocean. Ichthyologists have tended to assume that the ancestor of the potamotrygonids was an Atlantic marine or euryhaline stingray that dispersed into freshwater, presumably during the last marine ingression 3-5 million years ago. The helminth parasites that inhabit potamotrygonids suggest an alternative perspective on their origin. Phylogenetic and biogeographic analysis of the helminths inhabiting potamotrygonids suggest that the hosts are derived from an ancestral Pacific urolophid stingray that was trapped in freshwater by the uplifting of the Andes beginning perhaps as early as the early Cretaceous period and ending by the mid-Miocene epoch, changing the course of the Amazon River, which previously had flowed into the Pacific Ocean.     

Bayesian inference supports the host selection hypothesis in explaining adaptive host specificity by European bitterling

Generalist parasites have the capacity to infect multiple hosts. The temporal pattern of host specificity by generalist parasites is rarely studied, but is critical to understanding what variables underpin infection and thereby the impact of parasites on host species and the way they impose selection on hosts. Here, the temporal dynamics of infection of four species of freshwater mussel by European bitterling fish (Rhodeus amarus) was investigated over three spawning seasons. Bitterling lay their eggs in the gills of freshwater mussels, which suffer reduced growth, oxygen stress, gill damage and elevated mortality as a result of parasitism. The temporal pattern of infection of mussels by European bitterling in multiple populations was examined. Using a Bernoulli Generalized Additive Mixed Model with Bayesian inference it was demonstrated that one mussel species, Unio pictorum, was exploited over the entire bitterling spawning season. As the season progressed, bitterling showed a preference for other mussel species, which were inferior hosts. Temporal changes in host use reflected elevated density-dependent mortality in preferred hosts that were already infected. Plasticity in host specificity by bitterling conformed with the predictions of the host selection hypothesis. The relationship between bitterling and their host mussels differs qualitatively from that of avian brood parasites.     

Metazoan parasites of freshwater cyprinid fish ( Leuciscus cephalus): testing biogeographical hypotheses of species diversity

The diversity and similarity of parasite communities is a result of many determinants widely considered in parasite ecology. In this study, the metazoan parasite communities of 15 chub populations (Leuciscus cephalus) were sampled across a wide geographical range. Three hypotheses of biogeographical gradients in species diversity were tested: (1) latitudinal gradient, (2) a 'favourable centre' versus 'local oasis' model, and (3) decay of similarity with distance. We found that the localities in marginal zones of chub distribution showed lower parasite species richness and diversity. A latitudinal gradient, with increasing abundance of larvae of Diplostomum species, was observed. There was a general trend for a negative relationship between relative prevalence or abundance and the distance from the locality with maximum prevalence or abundance for the majority of parasite species. However, statistical support for a 'favourable centre' model was found only for total abundance of Monogenea and for larvae of Diplostomum species. The phylogenetic relatedness of host populations inferred an important role when the 'favourable centre' model was tested. Testing of the hypothesis of 'decay of similarity with geographical distance' showed that phylogenetic distance was more important as a determinant of similarity in parasite communities than geographical distance between host populations.     

Optimal immune specificity at the intersection of host life history and parasite epidemiology

Hosts diverge widely in how, and how well, they defend themselves against infection and immunopathology. Why are hosts so heterogeneous? Both epidemiology and life history are commonly hypothesized to influence host immune strategy, but the relationship between immune strategy and each factor has commonly been investigated in isolation. Here, we show that interactions between life history and epidemiology are crucial for determining optimal immune specificity and sensitivity. We propose a demographically-structured population dynamics model, in which we explore sensitivity and specificity of immune responses when epidemiological risks vary with age. We find that variation in life history traits associated with both reproduction and longevity alters optimal immune strategies–but the magnitude and sometimes even direction of these effects depends on how epidemiological risks vary across life. An especially compelling example that explains previously-puzzling empirical observations is that depending on whether infection risk declines or rises at reproductive maturity, later reproductive maturity can select for either greater or lower immune specificity, potentially illustrating why studies of lifespan and immune variation across taxa have been inconclusive. Thus, the sign of selection on the life history-immune specificity relationship can be reversed in different epidemiological contexts. Drawing on published life history data from a variety of chordate taxa, we generate testable predictions for this facet of the optimal immune strategy. Our results shed light on the causes of the heterogeneity found in immune defenses both within and among species and the ultimate variability of the relationship between life history and immune specificity.     

Effect of the digenean parasite Proterometra macrostoma on host morphology in the freshwater snail Elimia livescens

Parasitism can affect size in gastropods by altering the host's growth rate, but other morphological effects of parasitism have rarely been examined. In this study, the relationship between variation in host morphology and parasitism was examined in a population of the freshwater snail Elimia livescens. Differences were found in the morphology of snails infected with the digenean Proterometra macrostoma and uninfected snails. In order to differentiate between 2 hypotheses to explain these differences in morphology, snails were experimentally infected in the laboratory and several morphological traits were measured after 180 days. One hypothesis suggests that parasite-induced changes in shell development explain differences in morphology between infected and uninfected snails. The other hypothesis suggests that selective mortality of infected hosts explains the difference. In the experiment, differences were found between infected snails and uninfected snails in overall size but not in any measurements of shape. The short duration of the experiment relative to the duration of most infections may account for why field-infected snails differed in shape but experimentally infected snails did not. Parasite-induced changes in growth rate are the most likely explanation for the larger size of infected snails relative to uninfected snails.     

Variation in costs of parasite resistance among natural host populations

Organisms that can resist parasitic infection often have lower fitness in the absence of parasites. These costs of resistance can mediate host evolution during parasite epidemics. For example, large epidemics will select for increased host resistance. In contrast, small epidemics (or no disease) can select for increased host susceptibility when costly resistance allows more susceptible hosts to outcompete their resistant counterparts. Despite their importance for evolution in host populations, costs of resistance (which are also known as resistance trade‐offs) have mainly been examined in laboratory‐based host–parasite systems. Very few examples come from field‐collected hosts. Furthermore, little is known about how resistance trade‐offs vary across natural populations. We addressed these gaps using the freshwater crustacean Daphnia dentifera and its natural yeast parasite, Metschnikowia bicuspidata. We found a cost of resistance in two of the five populations we studied – those with the most genetic variation in resistance and the smallest epidemics in the previous year. However, yeast epidemics in the current year did not alter slopes of these trade‐offs before and after epidemics. In contrast, the no‐cost populations showed little variation in resistance, possibly because large yeast epidemics eroded that variation in the previous year. Consequently, our results demonstrate variation in costs of resistance in wild host populations. This variation has important implications for host evolution during epidemics in nature.     

Extreme host specificity by Microdon mutabilis (Diptera: Syrphiae), a social parasite of ants

Larvae of the syrphid fly Microdon mutabilis are social parasites which live up to two years, feeding on ant brood in nests of Formica lemani ants. We questioned why M. mutabilis is extremely localized when its host is widespread and abundant. Like endoparasitic diseases, social parasites must penetrate formidable defences before ''infecting'' their hosts. This occurs during the egg stage of M. mutabilis: females are sedentary and oviposit at F. lemani nest entrances, which workers treat as part of their nest, leaving the thin-shelled eggs vulnerable to attack for 10 to 14 days before hatching. We describe experiments which show a strong maternal effect in M. mutabilis. New-laid eggs had > 95% survival when introduced to the individual ant colony that reared each mother fly or to its close neighbours, but survival declined as a sigmoidal logistic function of distance from the mother nest, with F. lemani colonies from 2 and 30 km away killing 80 and > 99% of eggs, respectively, within 24 h. Attacks on eggs also increased in proportion to the delay before introduction to laboratory nests. We suggest that they may be coated with a mimetic chemical disguise that lasts for three to four days after oviposition. The results indicate extreme local adaptation by an M. mutabilis population not simply to one species of host, but to an individual host population and possibly to local strains or family groups within an F. lemani population. This conclusion is discussed in terms of virulence, transmission and coevolution in parasitic diseases.     

Making host specificity testing more efficient: Exploring the use of abridged test plant lists

Testing the specificity of candidate agents is a key component of risk analysis in weed biological control. This step is often time-consuming due to the numerous plant species that need to be tested under quarantine conditions in the invaded country of the weed species. Here, we examined whether an abridged phylogenetically based test list could be used in the weed's native range to quickly screen the host specificity of candidate agents. Ten plant species were used to test the host specificity of a promising candidate for the biological control of Sonchus oleraceus in Australia, the gall midge, Cystiphora sonchi. No-choice and choice tests were carried out in the native Mediterranean range of the midge. The results showed the midge has potential to threaten native Australian species, as those species showed high infestation levels in no-choice tests and produced significantly higher numbers of galls in choice tests. As a result of this approach, C. sonchi was rapidly discarded from the list of agents to be imported into Australian quarantines for further tests. This study demonstrates that testing a few key phylogenetically related species in the native range may save cost and effort in a weed biological control programme.     

From individual heterogeneity to population-level overdispersion: quantifying the relative roles of host exposure and parasite establishment in driving aggregated helminth distributions

In most host-parasite systems, variation in parasite burden among hosts drives transmission dynamics. Heavily infected individuals introduce disproportionate numbers of infective stages into host populations or surrounding environments, causing sharp increases in frequency of infection. Parasite aggregation within host populations may result from variation among hosts in exposure to infective propagules and probability of subsequent establishment of parasites in the host. This is because individual host heterogeneities contribute to a pattern of parasite overdispersion that emerges at the population level. We quantified relative roles of host exposure and parasite establishment in producing variation in parasite burdens, to predict which hosts are more likely to bear heavy burdens, using big brown bats (Eptesicus fuscus) and their helminths as a model system. We captured bats from seven colonies in Michigan and Indiana, USA, assessed their helminth burdens, and collected data on intrinsic and extrinsic variables related to exposure, establishment, or both. Digenetic trematodes had the highest prevalence and mean abundance while cestodes and nematodes had much lower prevalence and mean abundance. Structural equation modeling revealed that best-fitting models to explain variations in parasite burden included genetic heterozygosity and immunocompetence as well as distance to the nearest water source and the year of host capture. Thus, both differential host exposure and differential parasite establishment significantly influence heterogeneous helminth burdens, thus driving population-level patterns of parasite aggregation.     

A method for testing the host specificity of ectoparasites: give them the opportunity to choose

Host-choice experiments were carried out with rodent and bat ectoparasites on Ilha Grande, state of Rio de Janeiro, Brazil. We constructed experimental chambers that enclosed three different rodent or bat host species, and then introduced a selected set of ectoparasitic arthropods. When given the opportunity to choose among host species, the ectoparasites showed a strong tendency to select their primary hosts, and reject novel host species. These kinds of simple experiments can be valuable tools for assessing the ability of ectoparasites to locate and discern differences between host species, and make choices about which hosts to infest, and which hosts to avoid.     

Micro-evolutionary change and population dynamics of a brood parasite and its primary host: the intermittent arms race hypothesis

A long-term study of the interactions between a brood parasite, the great spotted cuckoo Clamator glandarius, and its primary host the magpie Pica pica, demonstrated local changes in the distribution of both magpies and cuckoos and a rapid increase of rejection of both mimetic and non-mimetic model eggs by the host. In rich areas, magpies improved three of their defensive mechanisms: nest density and breeding synchrony increased dramatically and rejection rate of cuckoo eggs increased more slowly. A stepwise multiple regression analysis showed that parasitism rate decreased as host density increased and cuckoo density decreased. A logistic regression analysis indicated that the probability of changes in magpie nest density in the study plots was significantly affected by the density of magpie nests during the previous year (positively) and the rejection rate of mimetic model eggs (negatively). These results are consistent with a hypothesis (the intermittent arms race hypothesis) of spatially structured cyclic changes in parasitism. During periods of parasitism, host defences continuously improve, and as a consequence, the fitness gains for parasites decrease. When host defences against parasites reach a high level, dispersing parasites have a selective advantage if they are able to emigrate to areas of low resistance. Once parasites have left an area hosts will lose their defensive adaptations due to their cost in the absence of parasitism. The scene is then set for re-colonization by great spotted cuckoos. Received: 7 May 1998 / Accepted: 24 August 1998     

Helminthic host defense peptides: using the parasite to defend the host

Parasitic helminths are destined to share niches with a variety of microbiota that inevitably influence their interaction with the host. To modulate the microbiome for their benefit and defend against pathogenic isolates, helminths have developed host defense peptides (HDPs) and proteins as integral elements of their immunity. These often exert a relatively nonspecific membranolytic activity toward bacteria, sometimes with limited or no toxicity toward host cells. With a few exceptions, such as nematode cecropin-like peptides and antibacterial factors (ABFs), helminthic HDPs are largely underexplored. This review scrutinizes current knowledge on the repertoire of such peptides in helminths and promotes their research as potential leads for an anti-infective solution to the burgeoning problem of antibiotic resistance.